Waste Gas Biofiltration: Advances and Limitations ... - ACS Publications

Critical Review pubs.acs.org/est

Waste Gas Biofiltration: Advances and Limitations of Current Approaches in Microbiology T. Komang Ralebitso-Senior,†,* Eric Senior,‡ Renzo Di Felice,§ and Kirsty Jarvis∥ †

School of Science and Engineering, Teesside University, Middlesbrough, TS1 3BA, United Kingdom Clean Environment Management Centre, School of Science and Engineering, Teesside University, Middlesbrough, TS1 3BA, United Kingdom § Department of Chemical and Process Engineering ‘G.B. Bonino’, Genoa University, 16145, Genoa, Italy ∥ Graduate Research School, Teesside University, Middlesbrough, TS1 3BA, United Kingdom ‡

ABSTRACT: As confidence in gas biofiltration efficacy grows, ever more complex malodorant and toxic molecules are ameliorated. In parallel, for many countries, emission control legislation becomes increasingly stringent to accommodate both public health and climate change imperatives. Effective gas biofiltration in biofilters and biotrickling filters depends on three key bioreactor variables: the support medium; gas molecule solubilization; and the catabolic population. Organic and inorganic support media, singly or in combination, have been employed and their key criteria are considered by critical appraisal of one, char. Catabolic species have included fungal and bacterial monocultures and, to a lesser extent, microbial communities. In the absence of organic support medium (soil, compost, sewage sludge, etc.) inoculum provision, a targeted enrichment and isolation program must be undertaken followed, possibly, by culture efficacy improvement. Microbial community process enhancement can then be gained by comprehensive characterization of the culturable and total populations. For all species, support medium attachment is critical and this is considered prior to filtration optimization by water content, pH, temperature, loadings, and nutrients manipulation. Finally, to negate discharge of fungal spores, and/or archaeal and/or bacterial cells, capture/destruction technologies are required to enable exploitation of the mineralization product CO2.

1. INTRODUCTION Joining, and even surpassing, energy production and water provision, slowing the inexorable momentum of inimical climate change poses a major challenge to the scientific community and society in general. As a consequence, every environmental perturbation is subject to scrutiny to appraise both its contribution to this and its impact on sustainability. Thus, all atmospheric discharges, rather than a selected range of pernicious emissions, are targeted. Although amelioration of malodorant/toxic gases has been practised sporadically for more than 80 years, the methods adopted have often simply transferred the problem from the gas phase to a liquid or solid phase and so incurred further treatment. Also, where singlestage biofiltration has been employed, a lack of understanding of, and/or confidence in, the microbiology has resulted in high bioreactor volumes facilitating dilution rates well below the maximum specific growth rates of the catabolic species. To address this paucity of knowledge, definitive fundamental studies must be made, particularly where complex microbial associations (multispecies gene pools) underpin the mineralizations, to inform reduced footprint biofilter design. The ultimate goals must be to reduce treatment cost and, hence, improve industrial competitiveness, minimize residuals, reduce the © 2012 American Chemical Society

carbon footprint, and most important, ameliorate malodorant/toxic molecule gaseous discharges with attendant environment/public health protection and public acceptance. Detail of every aspect of gas biofiltration is out with the scope of this review and the reader is directed to seminal treatises such as Devinny et al. 1 and Kennes and Veiga 2 for comprehensive appraisals of the biotechnology. Instead, key references are given to contextualize the focus on packing material/microorganism-facilitated gas catabolism in conventional biofilters (BF) and biotrickling filters (BTF). Since publications have been limited in this area, complementary molecular microecophysiology studies are considered in relation to odorant/toxic gas amelioration. Also, where microbial communities are employed, molecular analysis is the focus rather than a more general consideration of the biomass. For nonanosmiatic individuals, odor sensation depends on contact of the stimulating molecule(s) with an appropriate Received: Revised: Accepted: Published: 8542

November 2, 2011 June 25, 2012 June 28, 2012 June 29, 2012 dx.doi.org/10.1021/es203906c | Environ. Sci. Technol. 2012, 46, 8542−8573

Environmental Science & Technology

Critical Review

Table 1. Examples of Waste Gas Source Industries, Pollutants, Biofilter Types and Scale, Support Materials and Implications for Microbial Communities (Nutrients, Buffering Capacity, Adhesion, Microecophysiology Analyses) source industries Food Industries bakeries abattoirs meat rendering plants

example pollutants

hydrogen sulfide

dimethyl sulfide methanol vegetable oil production fish processing fat processing gelatine production flavour and fragrant manufacture

coffee and cocoa roasting yeast drying pet food manufacture animal fodder production poultry batteries fattening plants livestock air hatcheries

Chemical Industries plastics processing agro-chemical adhesives production chemical storage

aldehydes acetaldehyde formaldehyde isobutyraldehyde sulfur compounds acetic acid

biofilters and scale (oxic / anoxic) laboratory, pilot and field scale − BF

laboratory scale − dry tubular biofilm reactor laboratory scale − two-stage BTF

support media

microbiological implications re support media

ferric oxide granular porous carbon molecular sieve zeolite bark polyurethane foam sugarcane bagasse coconut fibre bark polyurethane foam sugarcane bagasse coconut fibre sphagnum moss peat sapwood pozzolan synthetic UP20

example references

successful treatment under extremely acidic conditions in the listed order

30

no obvious decrease in reactor performance during a five-year operation. Zeolite addition to bark had minimum effect on efficiency

31, 32

32−37

ceramic rings

complete removal of low methanol loads under xerophilic conditions high total hydrocarbon removal efficiencies (≥90%) during 150 days of operation

laboratory scale

38 39 40−44

successful for mixed VOC but reduced efficacy with a decrease in reactor pH; effective acetic acid removal with recirculating water scrubber at pH ∼ 7

porous silicate pellets hydrogen sulfide VOC VOC nitrous oxide ethylene

acetone toluene trichloroethylene

compost and polystyrene spheres/perlite/gypsum peat

toluene xylenes ethylbenzene trimethyl benzene butyl acetate methyl ethyl ketone

bulking with polystyrene spheres, perlite, gypsum and wood chips

12, 46−48

laboratory scale laboratory scale

cow manure compost vermicompost

bench scale laboratory scale

zeolite peat-soil

51 52

laboratory scale

pozzolan pozzolan and compost

53, 54

pall rings

93, 105 −107 137 160

acetone toluene

11, 45, 46

laboratory scale − BF and BTF

laboratory scale − BF and BTF

potential source of inocula and nutrients; approaching 100% removal at 35 °C and 25−50% moisture content

agricultural residue pellets perlite porcelite (nutrient-augmented porous ceramic) polyurethane foam rock wool-compost compost polyurethane foam

8543

perlite has good hydrodynamic and mechanical properties; highest performance for micro-/macro-nutrient containing cattle bone porcelite

49 50

36, 61−73

dx.doi.org/10.1021/es203906c | Environ. Sci. Technol. 2012, 46, 8542−8573


Critical Review

Table 1. continued source industries

example pollutants methyl isobutyl ketone hexane (VOC) triethylamine siloxanes dichloromethane

trichloromethane methane thiol dichloroethane trichloroethane ethane trichloroethene propane n-butane isobutane pentane α-pinene

biofilters and scale (oxic / anoxic)

laboratory scale − BF and TBAB

poly(ethylene carbonate)/ pine sawdust/peat composites compost

79 80 81 82 51 53 83 84

natural zeolite

perlite/pall rings

methyl acetate ethyl acetate

laboratory scale − TBAB

good hydrodynamic and mechanical properties; effective treatment by fungi at 30 ° C with nitrate-N augmentation; good potential to withstand shock loads potential abiotic attenuation; successful (75%) removal via inoculation with preexisting geosim-degrading biofilm

sand

peat

good moisture holding capacity; potential source of nutrients; successful long-term removal

sintered glass peat/glass beads ceramic beads vermiculite

laboratory scale − oxic

toluene

laboratory scale

coconut fibre digested sludge compost peat pine leaves

VOC

laboratory scale

lava rock and pine nuggets

laboratory scale

graft polymerized wood sawdust and peat perlite

laboratory scale − TPPB

pilot and commercial scale

polyurethane coconut fibre sugarcane bagasse fern chips

wood-based (proprietary) inorganic medium

8544

85

86

55 63

43 87 88 57, 89−91

laboratory scale − BTF

toluene

methyl ethyl ketone propylene glycol monomethyl ether acetate dipropylene glycol monomethyl ether

76 77 78

laboratory scale laboratory scale − anaerobic laboratory scale − TBAB

laboratory scale

example references

74, 75

laboratory scale − TBAB

laboratory scale − oxic, pH 4 and 7

film coating laminate production


laboratory scale one-/two-liquid-phase stirred tank BF and BF laboratory scale − BF, BTF, and modified RBC laboratory scale − two-stage BF.

geosmin

dimethyl ether thioanisole pyridine styrene

support media

fungal spores as inoculum; higher toluene bioavailability through aerial mycelia probably resulted in increased enzyme activity potential sources of inocula; different capacities for porosity and moisture holding capacity; fungal predominance due to decrease in pH; generally, good reactor efficiency and recovery independent of support medium high porosity and, potentially, longevity; lower pressure drop for lava rock; different reduction efficiencies for specific gas components; inconsistent but approximately 48% odor reduction good porosity and moisture holding capacity; potential source of inocula perlite has better hydrodynamic and mechanical properties and good porosity; better efficiency in acid biofilters with fungi than bacteria good partitioning coefficient from polymer; but its addition (20%) led to severe microbial inhibition

92

93

94

95 96

97

98 99

76, 100



Critical Review


example pollutants


support media


example references

1-3-5 triazine-2-4-6 triamine triethylamine compost oil refining

BTEX

petrochemical production

chlorobenzene

laboratory scale

good moisture holding capacity; potential source of inoculum; prone to compaction

compost sugarcane bagasse/compost/ GAC press mud

dichlorobenzene

laboratory scale xerophilic conditions laboratory scale

animal manure and sawdust pellets peat/maple wood chips/chicken manure/soil

hydrogen sulfide

laboratory scale

polyurethane foam sugarcane bagasse coconut fibre sea shells

ethylene ethylbenzene

ethane thiol

resin processing Waste Treatment waste oil petrochemicals

ethanol propanol butanol phenol phenol formaldehyde chlorophenol carbon monoxide

hydrogen sulfide ammonia VOC

laboratory scale

laboratory mid-scale − twin BTF

landfill gas

hydrogen sulfide methane

good hydrodynamic and mechanical properties; no clogging with inoculated Thiobacillus thioparus

peat-soil rice hulls pine leaves sphagnum moss peat rock wool-compost

laboratory scale − BTF laboratory scale

laboratory scale

laboratory scale

106

107 108

35

109

52 110

composite has large surface area, high chemical persistence, high porosity and good water holding and buffering capacities; reduced compaction and pressure drop; maximum elimination efficiency obtained at 48 s EBRT with nutrient addition high porosity; good removal efficiencies by inoculated strains

porous ceramic pellets

65

62 111 112 113 114 115

laboratory scale − BTF laboratory scale

ammonia

MTBE BTX

good porosity and moisture holding capacity; low incidence of compaction; potential source of inocula good moisture holding capacity; successful but reduced efficacy with increased inlet concentration potential sources of nutrients and good porosity; good moisture holding capacity dichlorobenzene-contaminated soil provided inocula; stable, limited pressure drop and no clogging similar elimination capacities independent of support material

75, 101 −104 105

116 43, 117, 118

lava rock

waste straw cortex charcoal activated carbon polyurethane foam sugarcane bagasse coconut fibre calcium alginate

33, 35, 102, 119, 120,

satisfactory to high efficiency recorded during first week; scale-up criteria established

polyurethane sponge cubes coated with zeolite/activated carbon polyurethane foam cubes

compost soil

8545

121

122

BTX-degrading microbial community as inoculum; MTBE reduced removal efficiency

123, 124

125−127 76, 86, 125, 128, 129, 130 dx.doi.org/10.1021/es203906c | Environ. Sci. Technol. 2012, 46, 8542−8573


Critical Review


example pollutants VFA


VOC ammonia VOC

fibrous support medium

pilot scale

compost wheat bran/red wood powder/ diatomaceous earth bark polyurethane foam bark compost covered argyle pellets wood chip and compost compost/plastics

laboratory scale

VFA (butyric acid)

full scale laboratory scale

tobacco processing effluents

benzene toluene

laboratory scale − oxic, mesophilic and thermophilic conditions

piggery slurry animal manure composting, and storage

methane

laboratory scale

ammonia

ammonia methylamine

municipal solid waste treatment facilities wastewater treatment plants

acetaldehyde formaldehyde ethanol acetic acid hydrogen sufide ammonia VOC

compost soil


cattle manure

laboratory scale

granulated sludge

laboratory scale

granular activated carbon

laboratory scale

agricultural residue pellets coconut fibre porous silicate pellets


benzene toluene dimethyl sulfide methanol

toluene

wood chip and rock wool with earthworm compost rockwool compost compost/perlite polyurethane foam bark compost covered argyle pellets compost soil

laboratory scale

dimethylamine trimethylamine trimethylamine distillery dried grains



BTEX

foundry effluents composting plants

support media

131 132 133 69

anti-clogging system effected high removal efficiency

mixed support medium has lower pressure drop than compost alone high ammonia elimination capacity with 70% removed in wood chip section

negligible biomass accumulation, thus low/ no clogging

134−136 137−139

134 140 132 137 141

possible sources of nutrients and inocula; high water retention capacity; prone to clogging; necessitate regular unclogging and, thus, potential disturbance of community stability support medium properties as above; maximum methanotrophic activity recorded at mesophilic temperature

142

sawdust, urea and “rock” phosphate augmentation for 30:1 C/N ratio; ammoniaoxidizing and nitrite-oxidizing bacteria coexisted on biofilm good moisture holding and buffering capacity; potential source of inoculum

143

inherent buffering capacity also from ammonia adsorption by support medium; DGGE showed 25 operational taxonomic units; inoculated Arthrobacter sp. still dominant numerically

142

144

145−147

147, 148 low acetaldehyde removal at start-up; successful for mixed VOC, which was reduced with a decrease in reactor pH

41, 43

polyurethane foam

negligible biomass accumulation, thus low/ no clogging

35, 38, 39, 102, 141

sugarcane bagasse

potential nutrient source; bed compression can cause pressure drops

coconut fibre waste straw cortex composite-ceramic and organic clay laboratory scale − BF operated in down-flow mode laboratory scale

example references

granular activated charcoal/carbon porous ceramic pellets/ saddles/rings

8546

moisture content can be modified; high flow rate especially at low moisture content

porous medium ideal for fungal mycelia development; water retention capacity and porosity can be modified; high potential to reduce clogging

149

33, 34, 150, 151 152



Critical Review


Miscellaneous storage tanks print shops pulp, paper and wood products

plywood production wood drying tobacco processing

leather industries

engine combustion power plants

construction

example pollutants


support media


example references

hydrogen sulfide

pilot scale

peat

potential nutrient source; high porosity but requires additional support to obviate clogging

153

carbon disulfide


lava stones

good hydrodynamic and mechanical properties; inoculated Thiomonas sp. WZW showed high catabolic efficiency

118, 154

hydrogen sulfide


VOC benzene toluene dimethyl sulfide


polyurethane foam sugarcane bagasse coconut fibre polyurethane foam

35, 155, 156 negligible biomass accumulation thus low/ no clogging

141

predominance of Bacillus sphaericus

157, 158

bench scale − oxic and mesophilic conditions bench scale

sterilized wood chips and cow dung/compost compost and wood chips

hydrogen sulfide VOC benzene toluene hydrogen sulfide


polyurethane foam

141, 162

163

nitric oxide

laboratory scale − RDB anoxic and mesophilic conditions

polyurethane foam sugarcane bagassecoconut fibre spongy-type polymer foam

mercury carbon monoxide gasoline kerosene VOC

laboratory scale − BTF laboratory scale − two-stage TBF and BF hybrid

diethyl sulfide monoterpenes

pilot scale

carbon foam /lava polyurethane foam lava rock

compost

159, 160 161

high efficiency of packing materials with even biomass distribution and no clogging efficient removal (100%) with SOB inocula effective removal when carbon monoxide mixed with formaldehyde and methanol

164 165 166 43, 167

168

Various physical (adsorption,20,21 absorption,20,21 condensation) or chemical (catalytic combustion, 22 scrubbing,8 oxidation23) methods have been used to resolve the problem while other, dual treatments, such as granular activated carbon trapping followed by slurry (e.g., moving sand filter bed) bioreactor treatment, gas solubilization followed by conventional wastewater treatment, and UV photodegradation combined with biofiltration,24,25 may be considered. They are, however, invariably expensive in terms of plant and operating costs. Thus, a more cost-effective and sustainable approach is the use of biofiltration26 particularly where definitive study can result in lower volume bioreactors.

receptor cell in the olfactory epithelium with millions of odorants detected in low concentrations.3 Other, often odorless, gases may, however, diminish or enhance odorant perception with methane, for example, having an enhancing effect.4 The intensity of an odor, which varies from individual to individual,5 with age6 and with gender,7 is quantified in concentrations of odorant units m−3 air while personal perception8 is based on character (type), hedonic tone (pleasantness/unpleasantness) and intensity (strength). The emission rate (E), which is the product of the concentration (C) of a specific chemical compound and the flow rate (Q) of the gas stream emitted, is quantified as E = C × Q.9 By combining the results of various sensory measurements with odorant dispersion modeling,10−12 a total odorant emission rate (ou h−1), and the odor impact13 area over a year, can be estimated. For many industrialized nations, regulations exist on the permissible annual maximum exposure times of citizens to malodorant molecule gaseous discharges11,14,15 from, for example, manufacturing plants,16 animal rearing facilities,11,12 municipal wastewater treatment plants10 and landfills.17 When exposure limits are likely to be exceeded, where the odorant emitted permeates the background odorant of the neighborhood, exclusion zones around particularly sensitive point- and nonpoint source emissions are delineated. Alternatively, the gas is either treated at source or its migration is prevented by gasimpermeable membranes18 or barriers to intercept it and facilitate atmospheric venting.19 For industrialized nations, the high population densities negate the “luxury” of exclusion zones and legislation dictates odorant gas attenuation at source.

2. APPLICATIONS The efficacy of biofiltration was recognized in the 1950s when it was introduced for wastewater treatment plants to address emissions of hydrogen sulfide, organic sulfides, mercaptans, organic molecules and nitrogen-based compounds. Since then, various reactor configurations have emerged including biotrickling filters, bioscrubbers (BS), continuous stirred tank bioreactors (CSTB), activated sludge diffusion, dual liquid phase, membrane and monolith and have incorporated singlelayer open-bed, single-layer closed-bed, multilayer, multilayer rotating drum,27 two-stage (e.g., two-phase partitioning bioreactors (TPPB)),28 multistage, modular, step-feed and membrane29 operation under both aerobic and anaerobic conditions. Diverse industries have been targeted and, as a consequence, the range of molecules has grown (Table 1). With time, these molecules have become increasingly complex 8547



Critical Review

Table 2. Waste Gas Types and/or Classes with Respective Catabolic Microbial Strains, Phylogenetic Groups and Functional Genes (Where Available/Determined) pollutant/class ammonia

taxanomic phylum and class/order β-Proteobacteria γ- Proteobacteria β-Proteobacteria γ- Proteobacteria β-Proteobacteria

catabolic species

observations

Nitrosomonas europaea Vibrio alginolyticus Stenotrophomonas nitritireducens L2 Luteimonas mephitis B1953/27.1 Pseudoxanthomonas broegbernensis B1616/1 Nitrosomonas-like spp.

NOB gene expressed; yellow pigmented isolates driving a unique denitrification reaction

references 119 188 189

novel freshwater amoA gene recorded closely affiliated with Nitrosomonas oceanus; methane monooxygenase gene expressed from γ- Proteobacteria methane oxidizers

cited by Andrés et al274

Nitrosospira-like spp. ammonia and VOC

β-Proteobacteria γ- Proteobacteria

Nitrosospira sp. Nitrococcus mobilis

AOB (amoA) and NOB genes expressed; new organic compounds produced by biofilm

190

BTEX, ethylbenzene and o-xylene BTX and MTBE

α-Proteobacteria

Sphingomonas sp. D3K1

a decrease in nutrient augmentation reduced o-xylene mineralization in mixed BTEX biofilter MTBE reduced maximum individual elimination capacities of benzene, toluene and xylene; MTBE cometabolized via tod and tol pathways by BTX-induced enzymes expected predominance of thermophiles for a thermophilic biofilter; enhanced removal efficiency due to yeast extract augmentation. Some inhibition of toluene degradation

68

successful enrichment and isolation from activated sewage sludge; thiosulfate augmentation enhanced CS2 removal to 99%

154

γ- Proteobacteria Firmicutes Actinobacteria

Rubrobacter xylanophilus Mycobacterium hassiacum

carbon disulfide

β-Proteobacteria Burkholderiales

Thiomonas sp.WZW

dimethyl sulfide

Actinobacteria γ- Proteobacteria β-Proteobacteria

Microbacterium sp. NTUT26 Pseudomonas putida Thiobacillus thioparus TK-m Bacillus sphaericus Bacillus megaterium Paenibacillus polymyxa

dimethyl sulfide and butyric acid

Actinobacteria β-Proteobacteria

Microbacteria spp. Gordonia spp. Dietzia spp. Rhodococcus spp. Propionibacterium spp. Janibacter spp.

dimethyl sulfide and methanol

α-Proteobacteria β-Proteobacteria

Hyphomicrobium spp. Thiobacillus spp.

ethyl acetate

Actinobacteria

Rhodococcus fascians

ethylene

Actinobacteria

Mycobacterium strain E3

hydrogen sulfide

γ- Proteobacteria Thermoprotei β-Proteobacteria β-Proteobacteria

Acidithiobacillus thiooxidans Sulfolobus metallicus Thiobacillus sp. Thiobacillus thioparus

β-Proteobacteria ε-Proteobacteria

Thiothrix spp. Thiobacillus spp. Sulfurimonas denitrif icans Pseudomonas sp. Moraxella sp. Acinetobacter sp. Exiguobacterium sp.

γ- Proteobacteria Firmicutes

hydrogen sulfide and ammonia hydrogen sulfide, ammonia and VOC

Actinobacteria

Arthrobacter oxydans

Firmicutes γ- Proteobacteria

Bacillus sp. Pseudomonas sp.

123

141

91

effective DMS treatment demonstrated in bench-scale biofilters and on site

157, 158 52 192

Hyphomicrobium spp. specific growth rate reduced due to decrease in pH in the presence of dimethyl sulfide

193

194 biofilter operated efficiently at 10 °C so ideal for horticultural storage facilities emissions

T. thioparus was the principal component of the H2S degrading community SOB gene expression

significant change in community structure in up, middle and down layers; eukaryotic populations detected only in down layer, which also had highest diversity

52

195 196 197 198 199

153

200 predominance of heterotrophic bacteria, with fungi (Penicillium sp.) and actinomycetes also detected 8548

102



Critical Review

Table 2. continued pollutant/class

taxanomic phylum and class/order

catabolic species

observations

references

α-Proteobacteria

Paracoccus denitrif icans

malodorant gases

Firmicutes

Lactobacillus plantarum KJ-10311

ammonia, methylamine, dimethylamine and trimethylamine

Actinobacteria α-Proteobacteria

Arthrobacter sp. Paracoccus denitrif icans

inoculated Arthrobacter sp. remained the dominant strain; P. denitrif icans probably central to ammonia oxidation and anaerobic denitrification

146

nitric oxide

β-Proteobacteria γ- Proteobacteria cytophaga-flexibacteria-bacteroides

Clostridium spp.

efficient removal in anoxic rotating drum biofilter; no detected effect of temperature change around the optimum of 30 °C

164

odorant compounds

γ- Proteobacteria

Pseudomonas sp.

202

o-xylene

Actinobacteria

Rhodococcus sp.

203

styrene

Actinobacteria Actinobacteria

Rhodococcus rhodochrous Rhodococcus pyridinovorans

91 94

toluene, ethylbenzene and p-xylene

actinomycetales Burkholderiales Xanthomonadales Actinobacteria α-Proteobacteria β-Proteobacteria γ- Proteobacteria Actinobacteria Firmicutes Verrucomicrobia δ-Proteobacteria thermomicrobia

Burkholderia cepacea Pandoraea pnomenusa

VOC

201

xerophilic biofilters; predominance of filamentous actinomycetales and fungi

Rhodococcus erythropolis T902.1 Mesorhizobium sp. Afipia sp. Nitrobacter sp. Devosia sp.

107

205 206

Sphingomonas sp. Burkholderia sp. Methylophilales sp. Ideonella dechloratans Alcaligenes def ragrans Methylobacillus glycogenes Stenotrophomonas sp. Escherichia sp. Shigella sp. Enterobacter sp. Caulobacter crescentus, etc.

ethanol

Ascomycota Saccharomycetes

Candida utilis

hexane

Ascomycota Sordariomycetes

Fusarium sp. Fusarium solani

Ascomycota Dothideomycetes

Cladosporium sp.

96

monoterpenes

Basidiomycota basidiomycetes

Phanerochaete chrysosporium

161

styrene

Ascomycota Euascomycetes

Sporothrix variecibatus

57, 90

toluene and ethylbenzene

Ascomycota Chaetothyriales (order) acomycota Chaetothyriales (order)

Exophiala lecanii-corni

toluene, ethylbenze and p-xylene toluene

Ascomycota Euascomycetes

207

greater efficiency in acid biofilters with fungi than bacteria; hydrophobic aerial hyphae contact odorant directly and adsorb hydrophobic compounds

homogentisate-1,2-dioxygenase activity measured; target gene expression numbers consistent with biofilter performance

96, 208

209, 210

Exophiala oligosperma

107

Scedosporium apiospermum TB1

211

8549



Critical Review

Table 2. continued pollutant/class

taxanomic phylum and class/order Ascomycota Chaetothyriales (order) Ascomycota Eurotiomycetes Ascomycota Eurotiomycetes Ascomycota Eurotiomycetes

catabolic species

observations


references

dominant inoculated strains with high elimination efficiency; fungi outcompeted bacteria in mixed inocula

187

first report of toluene degradation by nematophagous fungus and its hydrophobin protein higher toluene bioavailability due to aerial mycelia; increased toluene oxygenase and benzyl alcohol dehydrogenase activity

212

Paecilomyces variotii Paecilomyces lilacinus Paecilomyces variotii CBS115145

toluene, ethylbenzene and p-xylene

Ascomycota Chaetothyriales (order)


VOC

Ascomycota Euascomycetes Ascomycota Eurotiomycetes

Scedosporium sp.

xerophilic conditions

92

107

213

Paecilomyces sp.

tions,172,173 chars can be tailored for specific applications174 including gas biofiltration. Thus, elevated production temperature175 and hold time176 increase the aromatic component and, hence, water retention capacity, surface area, porosity and recalcitrance but decrease the surface functionality and cation exchange capacity. With new methods of char production, such as hydrothermal carbonization,177 pressurized pyrolysis178 and microwave pyrolysis,179 being researched, products with different properties may be produced. Selection of a specific char could then be made relative to the target biofiltration molecule(s). Polar molecules, such as o-cresol, for example, have been shown180 to sorb to a higher degree than apolar molecules such as cyclohexane. Studies with neutral organic molecules (benzene and nitrobenzene) and Triticum aestivum L. chars (300/700 °C) revealed different adsorption patterns with carbonized surface adsorption dominant for the higher temperature material and surface adsorption and lower partition into the residual organic phase characterizing the 300 °C char. During biofilter start up, residual adsorbed pyrolysis products, such as bio-oils, and recondensed materials,181 including acids, alcohols, carbonyls, polycyclic aromatic hydrocarbons, cresols and xylenols, must also be considered as additional electron donors or co-oxidation energy sources. To a lesser extent, chars also contain limited concentrations of nutrients,182 which could promote microbial activity. The longevity of their impacts will, however, be dependent on the char source material and production conditions. 3.2. Molecule Transfer. As reviewed by Kraakman et al.,183 this parameter involves gas−liquid transfer and liquid phase transport to the microorganisms. Here it is important that the target gas is characterized fully in relation to its discharge concentration and flow rate, temperature and solubilized pH. Consideration must also be given to the costs of adjusting the gas temperature to facilitate gas solubilization for optimum microbial catabolism. Subsequently, the electron donor and electron acceptor concentrations must also be considered together with the redox potential. 3.3. Catabolic Population. A bacterial or fungal monoculture or a microbial community46,62,97,133,135,157,184−187 may be used and some reported strains are highlighted in Table 2 with a number of fungal species used in dual cultures with mites214 or protozoa.215 If the biofilter is packed with organic

hence efficient treatment of mixed waste gases, commonly designated VOC, often with unknown compositions, is an additional challenge. Despite this, the reported successful treatments of single and mixed pollutant waste streams possibly reflect our growing confidence in both the efficacy of catabolic monocultures and, particularly, microbial communities and control of cometabolism.169

3. BIOREACTOR For effective gas biofiltration three key requirements must be satisfied in the bioreactor: the presence of a support medium (organic/inorganic) for microbial attachment and biofilm formation; gas molecule transfer to the liquid phase; and a catabolic population with a mineralization rate approximating to the gas−liquid mass transfer rate. 3.1. Support Media. Organic and inorganic support media (Table 1) are chosen primarily on the basis of cost, availability (e.g., ref 170) and recalcitrance and, as a consequence, materials such as compost and coconut fiber have been used extensively. Considerations of media physical, chemical and biological properties are, however, either overlooked or are limited to surface modification to improve microbial adhesion. The key criteria of any material are that the pH, redox potential, moisture content (water activity) and minerals in the biofilter must be nonlimiting; the pollutant and nutrient adsorption capacities must be nonlimiting; there must be a large surface area (intraparticle porosity) to maximize microbial attachment sites, sorption capacity and reactive sites; and there must be minimal bed compaction and high (interparticle) porosity to prevent pressure drops and maintain the gas retention time. Despite only limited use until now in laboratory- and industrial-scale biofilters, appraisal of one organic medium, charcoal, exemplifies both the need for detailed scrutiny prior to packing material selection and the potential to produce bespoke supports for specific gases. Charcoal (char) has received unprecedented attention not only as sequestered carbon, to slow the momentum of climate change, but also for its exploitation potential in contaminated land remediation and restoration, composting and agriculture.171,172 Its characteristic features include large surface area, cation exchange capacity, pore size, volume and distribution, elemental composition, and high water holding capacity, making it an ideal packing material. Through feedstock and pyrolysis conditions manipula8550



Critical Review

conditioning layer of adsorbed organic carbon residues on the wetted support medium. For bacteria, the formation of a biofilm is controlled by intracellular signaling and is dominated by fast-growing species. First, bacteria approach the surface with some motile species capable of a positive chemotactic response while nonmotile strains rely on random Brownian motion to bring them close enough for adhesion to occur.229 For a bacterium such as Escherichia coli, however, the initial attachment is dependent on motility but not chemotaxis. Thus, advection, dispersion and entrainment all influence the subsequent deposition.230 The initial phase of adhesion is reversible and is mediated by short-range interactions, including hydrophobic or ionic forces.231 Bacterial motility may, thus, be required to overcome repulsive forces at the surface-medium interface and facilitate biofilm spread across the surface.232 Bacteria move to form microcolonies and a three-dimensional structure of pillars of cells and water channels forms.233 The extracellular structures involved in polymer building vary and include pili, fimbrae and extracellular polymer substances (EPS). At this stage, environmental variables, particularly pH and ionic strength, influence the bacterial attachment density.234 As introduced above, pili may also be strong attachment determinants: type IV in Vibrio cholerae235 and type I in Escherichia coli.232 Type IV pili are also vital for the aggregation of a monolayer of Pseudomonas f luorescens into microcolonies on surfaces.236 Irreversible sorption occurs over several hours after which the bacteria no longer exhibit Brownian motion.237 This process relies partly on the formation of EPS, which bind to the solid support,238 and partly on hydrogen bonds, hydrophobic interactions and dipole−dipole, dipole−induced dipole, and ion−dipole interactions.237 Extracellular polymer substances are generally low in nitrogen but constitute 50−90% of the biofilm.239 The vast majority of EPS are polysaccharides. Common sugars, such as glucose, galactose, rhamnose, Nacetylglucosamine, glucuronic acid, galacturonic acid, mannuronic acid, guluronic acid, dextran, and 2-keto-3-deoxygalactonic acid, are typical constituents together with organic acids, such as pyruvic and acetic,240 and polypeptides, particularly polyglutamic acid, proteins, nucleic acids and lipids. Most polysaccharide accumulation occurs when the physiological status of the cells shows maximum stress so advanced rates of adhesion are often recorded with starved cells. These observations should, therefore, be given consideration for biofilter start-up and subsequent operation although the much more sophisticated approaches of altering genetic circuits and cell signaling to control biofilm formation are now being considered.241 Together with microorganism aggregation, the EPS trap solubilized nutrients from both the liquid phase and cellular byproducts and promote precipitation of minerals such as calcium carbonate. They also provide a highly hydrated gel, and often charged matrix, in which the microbial cells (and other particles) embed and establish stable interacting associations,242,243 which are protected from hydraulic shearing and biocidal attack.244,245 Fungal biofilm mechanisms have also been considered. Although discussed within a medical context, Fanning and Mitchell246 reviewed fungal biofilm architecture, gene expression/genetic determinants together with exchange modes. For the latter, mating and cell fusion were the principal mechanisms, which contrasted extracellular DNA-mediated exchanges in bacteria. Also, studies with Candida albicans and Aspergillus f umigatus confirmed distinct biofilm and planktonic

material such as compost or granulated sludge an appropriate inoculum may be present or an acclimatized culture may be added216 but a synthetic support medium must be inoculated with a specific monoculture or microbial community. Typically, inocula have been sourced from wastewater treatment plants or existing biofilters and biotrickling filters. As an inoculum source, sewage/activated sludge can be trickled over or inoculated directly into a support medium. Alternatively, inocula can be cultured in feed reactors to specific biomass concentrations prior to introduction of the waste gas.144,217,218 As reviewed by Nelson and Bohn,219 soil/ compost bed reactors may be ideal inocula sources since they manifest the inherently high phylogenetic and functional diversities of soils. Use of landfill site covering soil, for example, could be particularly appropriate since pre-enrichment should have been facilitated through microbial contact with >80 gas components and >240 different leachate molecules. Methanotrophic communities would thus be present for methane biofiltration220,221 at laboratory-128,142 and field-scale.126,222 Following reactor inoculation, the start-up time may be slow and this has been addressed for fungal biofilters.223 Once established, however, the functional capacities of the inoculated strains must be retained as exemplified by the two fungi Exophiala oligosperma and Paecilomyces variotii outcompeting Pseudomonas and Bacillus spp. and so remaining dominant in toluene catabolism under steady-state conditions.187 3.3.1. Enrichment and Isolation of Catabolic Species and Microbial Communities. As the chemical complexities of molecules have grown there is the need to use specific monocultures or microbial communities. To obtain appropriate cultures, various methods of enrichment and isolation may be considered in relation to the target molecule(s). These include open and closed cultivation (static and shaken, with and without gas collection), both aerobic and anaerobic, and in situ protocols. If, however, the substrate inhibitor concentration (Ki) is exceeded in the enrichment/isolation the highest sub-Ki association or monoculture should be subjected to culture efficacy improvement with the goal of raising the critical substrate concentration to not only match the loading but also accommodate biofilter elevated load perturbations.21,90 Different microbial taxa (bacteria, archaea and fungi) exhibit different specific Ki values for the target pollutant.223,224 Also, microbial growth and substrate utilization rates for the same strain or microbial community differ between batch and continuous systems, and are dependent on specific operational parameters within similar reactor configurations. As a result, microbial community profiling of efficient operational biofilters, prior to use as inocula sources for attenuation of specific molecules, including in similar reactor configurations and with comparable operational parameters, would be central to successful exploitation. At this stage it would also be appropriate to make kinetic analyses to determine the maintenance energy, saturation constant, maximum specific growth rate, and pH and oxygen limitations.225 It must be recognized, however, that within the biofilter both growth rate-dependent (free-living) and growth rate-independent (surface-attached) microbial monocultures or communities will be operative. 3.3.2. Microbial Attachment. For effective microbial attachment to the support medium the critical factors are the physicochemical properties of the cells, the packing material type,226 the liquid phase227 and the specific characteristics of the microorganisms.228 The adhesion process is initiated from a 8551



Critical Review

biofilters that are operated long enough to reach steady-state to ensure that biological attenuation is not confused with the initial physicochemical effects of adsorption and absorption. 3.3.3. Microbial Characterization. As reported by PrenafetaBoldú et al.107,259 most definitive research has focused on aerobic bacteria-based biofiltration of aromatic compounds, whereas fungi-based processes have received less attention. With microbial associations, however, the paucity is even greater. For microbial communities, unfortunately, despite centuries of exploitation in different environmental biotechnologies, few definitive fundamental studies of multispecies gene pools have been made due to “experimental uncontrollability”. This is perhaps unsurprising with two species associations effecting nine possible outcomes,260 whereas three species effect 54. Thus, even for culturable species only, rather than the complete communities, classification on the basis of zoological labels261 or structure262 is problematic. As a consequence, communities have often been studied as single entities or a reductionist approach has been adopted with monocultures examined singly or in dual or triple culture. A more realistic approach is to combine the two to examine the microorganisms in isolation (exclusive habitat domains) but retain the constraints of the association (overlapping activity domains) while taking due cognizance of the complementary microorganism−environmental variable and environmental variable−environmental variable interactions. Through conventional culturing studies and physiological profiling, insights of catabolic populations of models developed in the 80s263−265 were gained although the communities were violated. Other than possible species identification, such results now have limited value particularly since molecular methods (semiquantitative denaturing gradient gel electrophoresis (DGGE), quantitative real time and reversetranscription (RT) polymerase chain reaction (PCR), clone libraries, sequencing, GeoChip 2.0/3.0, PhyloChip and bespoke functional microarray analysis), to determine the numerically and functionally dominant members and the dominant gene sequences, can be used to make definitive fundamental studies in situ. As reviewed by Fierer and Lennon266 molecular analyses, even with their known caveats and limitations, have facilitated study of the dynamics, breadth and spatiotemporal (biogeographical) variability of microbial diversity. Also, factors that determine the deviations and changes in richness and diversity patterns are identified simultaneously in natural or managed communities and ecosystems. Specifically toward an increased understanding and efficacy of the biofiltration process, Cabrol and Malhautier267 extended this discourse and presented a comprehensive discussion of spatial and temporal dynamics on microbial density, diversity and community structure. Thus, the physiological, phenotypic, genotypic, functional and enzymatic responses, and catabolic pathways adopted by biofilter microbial communities to effect resilience, memory, stability and resistance, and ultimately a robust process, were explored at considerable depth. The authors suggested that since biofilters are characterized by controlled and monitored inputs and outputs, they are essentially model ecosystems and ideal tools to study the biodiversity−ecosystem function relationship. Nevertheless, there is an inexplicable paucity in the application of ecogenomic tools in gaseous waste remediation compared to their extensive development and application in wastewater treatment (e.g., ref 268) and/or for specific functional clades.269 A few example applications made for water treatment and

phenotypes with changes in transcription factor expression indicative of highly regulated processes. Since fungal biofilms are characterized by architectural ranges, the authors highlighted that detailed investigations for biofilm formation regulators, which are most likely conserved in individual species, with unique genes for protein and extracellular matrix syntheses, adhesion expression, etc., were essential. For gas biofiltration, existing data96,107 have exemplified the need for parallel biofilm composition assessments and attendant monitoring of environmental/bioreactor parameters, such as pH, molecule hydrophobicity and inlet concentration, for successful start-up and long-term efficacy. Once attached, acclimation to the targeted gas stream is also important and for self-inoculated biofilters this may take from 10 days to 10 weeks or more to enrich the appropriate catabolic species with respect to cell membrane transport proteins and intra/extra-cellular enzymes. If a microbial community is employed, it would be expected, as in wastewater treatment, that bacteria would tend to dominate in terms of activity and the individual species would stratify in the biofilter with high population densities of each developing nearer the gas inlet.247 Work with a bench-scale, peat/glass beads-packed biofilter inoculated with Rhodococcus rhodochrous AL NCIMB 13259, targeting styrene, recorded such a stratification with a linear relationship between the gas organic loading and the biomass concentration along the packing medium regardless of the flow rate.91 To minimize such uneven biomass distribution, an increased loading could be applied158 or gas flow directional switching could be considered.247 Stratification could, however, be a key element of mixed gas stream/microbial community biofiltration.248 It has been speculated, for example, that biomass distribution could be indicative of both catabolic sites and possible removal mechanisms249 thus commending molecular analyses for comprehensive study. The molecular processes and pathways of biofilm development continue to be investigated with new knowledge introduced constantly on quorum sensing in single-species biofilms and intercellular signaling and the role of extracellular macromolecules (lipids and nucleic acids) in multispecies structures.235,248,250−256 For example, metabolic profiling, twodimensional gel electrophoresis, mass spectrometry and peptide mass fingerprinting were used to investigate protein expression underpinning initial microbial (Streptococcus mutans) surface attachment.257 Also, although applied in acid mine drainage, mass spectrometry-based proteomic analysis revealed posttranslational modifications and/or genetic variations, which affected directly the composition and succession of specific cytochromes during biofilm development and maturation.258 Due to their capacity to tolerate acidic and low humidity conditions, fungal communities/strains often proliferate in the bioremediation of air pollutants especially hydrophobic molecules. As a result, analysis of their functional proteins has also been made as exemplified by the Class I hydrophobinlike proteins identified by peptide mass fingerprinting (matrixassisted laser desorption/ionization time-of-flight) for a Paecilomyces lilacinus that degraded gaseous toluene.212 Therefore, novel transcriptomic and (meta)proteomic analyses to link microbial community structure to function, track the development and maintenance of functioning/efficient biofilms and explain the mechanisms of failure and/or suboptimal reactor (biofilm) performance, are essential for contemporary biofilter (re)design. Investigations toward this must be underpinned by 8552


8553

laboratory scale − TBAB laboratory scale−BF laboratory and pilot scale−BF laboratory scale−BF and BTF industrial scale−upflow operated filter bed

nitric oxide

TCE

VOC

H2S, NH3 and VOC

H2S, animal rendering plants

butyric acid and dimethyl disulfide

NA

DG-DGGE or DGGE-GE

t-RFLP

LH-PCR

SSCP

FISH

MAR-FISH

STAR-FISH

H2 S

laboratory scale−BF, BTF, RDB (anoxic), SBB, TBAB

ethylbenzene, H2S, methyl ethyl ketone, methyl isobutyl ketone, NH3, nitric oxide, p-xylene, styrene, toluene, BTX, methyl tert-butyl ether, VOC

D/TGGE

NA

full scale −trickling biofilters

laboratory scale

laboratory scale−RDB

laboratory scale − BF

ethanol

ARISA

gas biofilter scale and type

most microecophysiology studies of gas biofiltration have relied on 16S rRNA gene or DNAbased protocols

application in waste gas treatment

DNA

target biomolecule and protocol

specificity of functional strain/community occurrence

quantitative detection of specific functional communities; rapid detection of radiolabelled biomolecules

functional strain/community occurrence; cellular activity and ribosome content; shifts in numbers within bacterial communities. Spatial scaling of specific functional communities

simple, rapid, and cost-effective community structure profilings

rapid and cost-effective; community profiling using amplicons of SSU rRNA gene variable regions potentially from individual species; highly reproducible results

rapid and cost-effective community structure or composition profiling; may allow predictions of organisms that might be present. Multiple restriction enzymes increase specificity

increased resolution of co-migrated DGGE bands or single bands that harbour heterogeneous mixtures of rDNA from multiple operational taxonomic units

rapid and cost-effective community structure profiling; used frequently in biofiltration studies, often targeting the 16S rRNA gene; some studies have targeted the 18S rRNA gene

rapid and cost-effective community profiling. Relies on variable region between highly conserved 16S and 23S rRNA genes. Potential to distinguish close to species level

extraction and subsequent amplification steps are often rapid and successful; a range of extraction protocols, including commercial kits, are available; reagents and kits are available for DNA concentration measurements if (semi-) quantitative downstream analysis is required

significance

radioactive-labelled substrates; probe design, availability and specificity

probe design and availability; dependent on prior knowledge of phylogenetic affiliation of expected active communities

probe design, availability and specificity. Novel probe design can be labour intensive; successful detection, analysis and elimination of false-positive and false-negative mismatches; number of target vs. hybridised probes; limited application for phylogenetically diverse/versatile groups, e.g. sulfide-oxidizing bacteria; limited permeability of some functional glades to oligonucleotide probes

high rate of single-stranded DNA reannealing; may reduce artificially diversity estimates, or increase abundance measurements, especially of complex communities.

individual peaks may monitor the dynamics of more than one species or genus. No indication of function

subject to database restrictions and PCR bias; fluorescent labels can retard fragment migration; non-specific or incomplete digestion can result in diversity overestimation

potentially laborious and time consuming; variable success in resolving some comigrating operational taxonomic units, including from different species

subject to DNA extraction and amplification biases; primer specificity and sensitivity becoming increasingly important; one band does not necessarily represent one operational taxonomic unit; detection limits of less abundant members in complex communities

subject to DNA and PCR limitations or biases; preferential amplification of shorter 16S-23S intergenic region templates; bias due to secondary structure or flanking DNA; number of fragments relative to community diversity

sample pre-treatment is sometimes required. Extraction optimization via different protocols may be necessary depending on ecosystem under study; variable cell lysis efficiencies; generally, DNA-based protocols do not necessarily provide conclusive evidence of the metabolic or functional roles of the analysed communities or strains

example limitations

Table 3. Microbiological Characterization and Analysis Techniques and Their Current or Potential Applications in Gaseous Waste Stream Treatmenta

Environmental Science & Technology Critical Review


NA

industrial scale−BF

laboratory scale−BF NA

DMS, toluene, ethylbenzene, methanol, p-xylene

no reported application in gas biofiltration but specific application for aromatic compounds in wastewater highlights direct relevance

NA

animal rendering plant

ammonia and TCE.

NA

NA

very few microecophysiology studies of gas biofiltration to date have used RNA-based protocols

Q-PCR

metagenomic analysis

microarrays, e.g., GeoChip 2.0/ 3.0 and PhyloChip

clone library and ARDRA

clone library and sequencing

454-/Pyro-sequencing

BIPES

8554

RNA

NA

NA

laboratory scale−BF pilot scale− BF

full scale− trickling biofilters

butyric acid and dimethyl disulfide

DNA-SIP + DGGE/tRFLP

NA


NA


Raman-FISH


Table 3. continued

high metabolic turnover rates in biofilters should ensure successful RNA recovery; increased availability of reagents that minimize RNA degradation during sample storage, processing and extraction; as for DNA, a range of extraction protocols, including commercial kits, available; reagents and kits available for RNA concentration measurements if (semi-) quantitative downstream analysis is required; commercial kits for 1-Step RT-PCR minimize contamination and facilitate successful amplification

high throughput sequencing; attempts to increase accuracy of data analysis and interpretation while decreasing costs

high throughput generation of more and complex environmental sequence data

more cost-effective sequence identity than pyro-/454-sequencing

rapid screening and analysis of large clone libraries

high throughput, quantitative and simultaneous analysis of phylogenetic structure and function

high throughput analysis of genetic diversity in microbial communities; potential for identification of novel enzymes; can be targeted towards specific functional groups; links microbial community structure and function

quantitative; potentially multiplex; can be modified to ensure specificity; measures gene expression

functional community profiling by labelling genomes of active members

qualitative analysis/resolution of monoculture and community dynamics; physiological shift detection; use of 16S rRNA gene probes for specific functional community analysis

significance

sample pre-treatment is sometimes required; successful extraction of high quality high quantity RNA can be a limiting step; extraction optimization via different protocols may be necessary depending on ecosystem under investigation; variable cell lysis efficiencies; RT-PCR protocol requires additional controls to increase amplification data reliability; generally, RNA-based protocols provide more conclusive evidence of the metabolic or functional roles of the analysed communities or strains than DNA-based techniques

still more costly than Sanger sequencing; large data sets necessitate careful and methodical analysis

costs; sequence error detection and management

as above; potentially laborious and time consuming during unique clone selection

clone library quantitative composition may differ from in situ profile; potential for biased diversity estimates; clone library composition affected by cell lysis. DNA extraction and amplification efficiencies; chimeras can bias diversity; choice of primers and cloning system; comparative sequence analysis dependent on submitted sequence size relative to those available in database

simultaneous sensitivity and specificity of multiple probes. Limited to available probes; data analysis; potential for false-positive and false-negative mismatches; no indication of the number of community components expressing genes differentially. Inability to locate differential gene expression in biofilms

subject to DNA extraction bias; metagenomic library screening, management and analysis can be labour intensive

subject to PCR bias

cost of stable isotope-labelled substrates. Decision on labelling C, N, or H depending on the target substrate. Incubation periods for labelling efficacy, which require optimization studies; potential for microbial growth inhibition by isotope labels; potential isotopic effect on chromatographic properties of biomolecules, e.g. fatty acid methyl esters; cross-feeding; potential loss of stable isotope label to organic support matrices

subject to appropriate calibrations; data analysis; applicability in complex microbial communities and “dirty” samples; probe design, availability and specificity

example limitations



8555

styrene, hexane, chicken farm

NA

FISH

(meta)transcriptomics

toluene

toluene

toluene

NA

SDS-PAGE

peptide mass fingerprinting coupled with MALDI-TOF

protein-/amino acid-SIP

NA

Protein enzyme activity

clone library and sequencing

NA

NA

RNA-SIP

16S rRNA microarrays

NA

DT-DGGE

ammonia and ethylbenzene

H2S

DGGE

catabolic gene expression and sequencing

TCE and ethylbenzene


RT-PCR


Table 3. continued

NA




NA

NA


NA

laboratory and industrial scale − BF.

NA

NA




combined benefits of tracking functional communities and expression of specific enzymes

peptide identification

rapid and cost-effective; determines target protein molecular weight; 2D SDS-PAGE can be the first step in purification and sequencing of unknown protein

establishes the expression and activity of specific known catabolic enzymes; links reactor performance and metabolic measurements; determines catabolic pathway; can be costeffective depending on assay

sequence identity of functional community members

high throughput analysis of functional communities; as above for DNA arrays

stronger profiling of function and linked to identity

functional gene expression by targeting community transcripts (mRNA); identifies expressed proteins; enables understanding of microbial community functional dynamics at global scale

facilitates identification process; specific probe design to differentiate within genera

high RNA turnover rate; more confirmatory functional profiling

identification of specific community members that display increased activity in response to defined environmental conditions; significant band intensity changes potentially indicate relative metabolic activity of target strains/populations

rapid and cost-effective functional community profiling; as above for DNA-based DGGE

quantitative detection of specific catabolic genes

significance

limitations as above for any SIP-based protocol; subject to recovery of high biomass and high quantity protein

availability of comparable sequence in database

no indication of protein function or identity; coupling with HPLC and MALDITOF can address identity

subject to recovery of high biomass and high quality protein/enzyme

as above for DNA-based clone library and sequencing; potential RNA degradation and thus biased profiling and analysis

as above for DNA arrays

successful and unbiased RNA recovery

successful recovery of high biomass; successful extraction of high quality and high quantity mRNA

reactor conditions such as pH can reduce bacterial activity, ribosome number and detection probe rates

cost of stable isotope-labelled substrates and cross-feeding; RNA degradation may lead to bias

subject to availability of group-specific primers; subject to PCR bias

subject to RNA extraction, degradation and amplification biases; as above for DNA-based DGGE

subject to recovery of high quality high quantity RNA and PCR bias

example limitations



styrene

PLFA-SIP

8556

NA

Raman spectroscopy

NA


Laboratory scale − BF.


laboratory and full scale − BF


laboratory scale − BF, bench scale BF and on site


NA


qualitative analysis/resolution of mono culture and community dynamics; can be linked with 16S rRNA gene probes for specific functional community analysis

analyses of biofilm development, architecture and maintenance during reactor start-up, operation and down-time; can be linked with 16S rRNA gene probes for targeted architectural analysis

simultaneous analysis of packing medium, biofilm structure and microbial morphology; assesses growth trends and abundance on support medium

identifies metabolic shifts in intact microbial communities; Applicable for oxic and anoxic cultures

high labelling of characteristic fatty acids facilitates correct catabolic taxon identification; availability of large fatty acid data ensures constitutive lipid marker identification independent of environmental physico-chemical parameters; alternative labelling of substrates with 2H often more cost effective

high labelling of characteristic fatty acids facilitates correct catabolic taxon identification; availability of large fatty acid data ensures constitutive lipid marker identification independent of environmental physico-chemical parameters

cost-effective; studies community physiology; in combination with other tools, e.g., quinone analysis, 16S rRNA sequencing, can aid phylogenetic clustering

identify protein expressed during biofilm formation; identify expressed functional enzymes

assesses in situ microbial metabolism; links community structure to function; gains potential to understand microbial community functional dynamics

significance

data analysis; applicability in complex microbial communities and ‘dirty’ samples; dependent on appropriate calibrations; careful data analysis and interpretation

presence of inorganics, e.g., elemental sulphur, and excess polysaccharide can limit detailed analysis; representative sampling effects

presence of inorganics, e.g., elemental sulphur, and excess polysaccharide can limit detailed analysis; representative sampling effects

subject to the bias and limitations of culture-based techniques

dependent on large data set of lipid profiles; chromatographic modification and shifts of labelled (e.g., 2H) fatty acids necessitate careful analysis for compounds with similar retention times

dependent on database and large data set of lipid profiles

subject to reference database

subject to availability of known standards

successful recovery of high biomass; requires recovery of high quality high quantity protein; subject to availability of comprehensive databases

example limitations

a BF: biofilter; BTF: biotrickling filter; DG-DGGE: double gradient-DGGE; DGGE-GE: DGGE gel expansion; DT-DGGE: differential transcription; DGGE NA: technique not yet applied in gas biofiltration; RDB: rotating drum biofilter; SBB: sequencing batch biofilter; SDS-PAGE: sodium dodecyl sulphate polyacrylamide gel electrophoresis; TBAB − trickle-bed air biofilter.

toluene, VOC

scanning confocal laser microscopy

Microbial Community or Biofilm Architecture SEM H2S, toluene, ethylbenzene, p-xylene, hexane

Microbial Community Metabolic Profiling CLPP ethanol

animal rendering plants, hexane, methane, VOC

PLFA

ammonia, animal rendering plants, dimethyl sulphide

toluene

mass spectrometry

Fatty Acids fatty acid/FAME

NA


(meta)proteomics


Table 3. continued




Critical Review

wastewater attenuation entailed fluorescent in situ hybridization (FISH), functional qPCR for nirS gene expression, terminal restriction fragment length polymorphisms (t-RFLP), DNAstable isotope probing (SIP) and sequencing in a thermophilic upflow anaerobic filter reactor, aerated biofilters, an ultrapure water producing plant (mixed bed ion-exchange resin) and a sequencing batch integrated fixed film activated sludge reactor, treating awamori distillery wastewater, pig manure, and glycerol wastewater. 270−273 These analyses should, similarly, be applicable and relevant to gas biofiltration since the same technologies and reactors are used and, often, to treat similar molecules. Consequently, a summarized overview of the most applied microecophysiology techniques and their potential applications and limitations in waste gas attenuation studies is shown in Table 3. The use of versatile toolkits is central to address the multiple challenges of realistic mixed odorant streams in particular. Thus, probing for degradative microbial community structure and functional capacity across physical and biochemical gradients of water activity, temperature, pH, redox potential, and electron donor/acceptor availability is paramount for optimum operation of conventional and small footprint biofilters. A review by Andrès et al.274 reported the application of culture-based (plating, community level physiological profiling) and molecular techniques (PCR, DGGE, FISH, tRFLP, automated rRNA intergenic spacer analysis (ARISA), phospholipid fatty acid analysis (PLFA), catabolic gene expression and sequencing) in 22 gas biofiltration studies since 1997. These have, subsequently, been extended and some examples include the application of toluene oxygenase and benzyl alcohol dehydrogenase assays to determine enzyme activity in the degradation of toluene by Paecilomyces variotii CBS115145 with analysis for intermediates (metabolomics) then confirming the adopted catabolic pathway.92 The authors reported a strong correlation between enzyme activity and toluene elimination efficiency. Also, the latter was higher than with bacteria-augmented degradation, most probably due to better fungal biofilm architecture, which facilitated increased transfer of hydrophobic compounds and oxygen. Since growth kinetics can be dependent on pH conditions, Hayes et al.193 used qPCR of catabolic 16S rRNA genes to study the specific growth rates of batch cultures degrading dimethyl sulfide (DMS) and methanol. Thus, 16S rRNA gene sequences from a clone library developed by the same researchers from a biofilter cotreating the two waste gas components were used to design qPCR primers and probes targeting bacteria, Hyphomicrobium, Thiobacillus, and Chitinophaga groups. Although very little change was observed from growth on methanol, higher specific growth rates were recorded for Hyphomicrobium spp. on DMS at pH 7, independent of the use of ammonia- or nitrate-N media, with a significant decrease to ≤0.20 h−1 in response to a pH reduction to 5. In contrast, Thiobacillus spp. showed constant specific growth rates, albeit lower than those of the Hyphomicrobium strains, despite changes in pH. Overall, these trends were matched by 16S rRNA gene copy numbers for both functional clades per μmol of consumed DMS or methanol. The authors also suggested potential mechanisms, catabolic pathways, and enzymes adopted during cotreatment of the gaseous wastes by mixed communities at different pH values, including the role of Chitinophaga spp. in carbon cycling instead of DMS degradation per se. Gene expression has been measured with qRT-PCR during fungal- (Exophiala lecanii-corni) mediated biofiltration of

ethylbenzene with organic load perturbation, waste molecule variation and reactor down time.209 A study of toluene biotrickling filtration entailed viable staining, protein and dry weight content determinations and DGGE to link bioreactor performance to the occurrence and distribution of active or inactive biomass relative to a specific packing material.60 Xue et al.143 used a biotrickling filter to treat a mixture of odorant gases including ammonia and volatile organic carbons from a cattle manure composting plant with ammonia- and nitriteoxidizing bacteria, Nitrosospira sp. and Nitrococcus mobiliz, as revealed by DGGE. Chen et al.275 adopted 16S rRNA gene DGGE and sequencing of major bands to elucidate microbial diversity in a rotating drum biofilter for nitric oxide denitrification with and without Cu II (EDTA) nutrient supplementation. They recorded a predominance of Clostridium spp., β-Proteobacteria, γ-Proteobacteria, and Cytophaga-Flexibacter-Bacteroides clades with denitrification facilitated by members of the γ-Proteobacteria in particular. Trichloroethylene (TCE)-degrading diazotrophic microbial communities, enriched/isolated from soil, were supported on wood charcoal and subjected to batch and continuous operation modes, TCE loading rate changes and reactor shut downs of 10 days.276 Subsequent characterization by RT-PCR, RFLP, cloning and sequencing for nif H gene expression revealed the presence of α-Proteobacteria with a predominance of Azospirillum-related species. The authors highlighted the significance of this first report of the occurrence of diazotrophic nitrogen-fixing communities, which remediated TCE-contaminated air under nitrogen limited conditions. Mi et al.277 studied a microbial community that attenuated a waste gas and, with single strand conformation polymorphism profiling (SSCP) and scanning electron microscopy, confirmed degradative capacity with a predominance of Bacillus spp. A pilot-scale biofilter treating hydrogen sulfide from an anaerobic wastewater treatment plant with an inlet concentration range of 227−1136 mg m−3 and empty bed retention time of 60 s, was similarly analyzed by SSCP and revealed different microbial community structures in the up, middle and down layers and increased occurrence of fungal populations in the down layer concomitant with higher removal efficiencies and a decrease in pH.153 All successful eco-/meta-genomic analyses are dependent on the recovery of high quality, high quantity biomarkers and removal of potential inhibitors, which, for biofiltration, are influenced further by the support material. This can then necessitate preliminary investments in protocol optimization, from extraction to downstream analysis, for successful representation of the biofilter microbial communities.184 As in other environmental biotechnologies, the use of fingerprinting techniques such as DGGE, complemented by clone libraries and sequencing, is common to explore the composition, phylogeny and spatial distribution of microbial communities198,206,275,278−281 that often degrade single-compound and, infrequently, mixed143,282 waste gas streams. The study of increasingly mixed feeds, which are more likely to be treated with greater efficacy by complex microbial communities, will mandate the application of more sophisticated and powerful tools. For example, although still relatively costly, novel and high throughput platforms such as pyrosequencing are being applied in microecophysiological analyses of soils, marine systems, deep mines, the atmosphere, the human gut, extreme/unique ecosystems, etc.283−289 Also, microarrays such as GeoChip 2.0/3.0 and PhyloChip have revealed greater 8557



Critical Review

predominance of sulfur-oxidizing sequences belonging to Thiothrix spp., Thiobacillus spp., and Sulf urimonas denitrif icans in a biotrickling filter that was designed to remove hydrogen sulfide from biogas under fully established pseudostate conditions over 249 days, prior to energy recovery.199 In addition, marked shifts in community composition and diversity were recorded over time with gradients and stratification in the relative abundances of aerobes along the filter and facultative anaerobes at the reactor inlet. Most molecular based analyses have, so far, explored the (functional) microbial communities of laboratory- and/or pilotscale biofilters. Nonetheless, a few full-scale examples include the application of FISH by Juhler et al.190 to study ammoniaoxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB) in a two-section SKOV-type trickling biofilter treating ventilation exhaust air from a pig farm at 3-, 15-, and 41week intervals. In general, aerobic heterotrophs dominated the biofilter, Nitrosomonas eutropha-like AOB were distributed unevenly toward the second section of the bioreactor, whereas low numbers of NOB, of the Nitrobacter genus, were recorded especially during weeks 3 and 15. The AOB activity was confirmed further by qPCR, mass balance calculations, ammonia oxidation potential determinations, microsensor analysis for oxygen uptake, etc. Unsurprisingly, considering its amenability to in situ analysis of operational large-scale facilities, as demonstrated extensively in wastewater treatment plants, FISH was again applied206,297 where the researchers used/re-evaluated published probes, and developed 16S rRNA targeting oligonucleotide probes de novo, to study catabolic communities that treated a mixed waste gas from an industrialscale animal rendering plant. Samples collected for specific months during a two-year period showed a general predominance of β-Proteobacteria members followed by Actinobacteria, α-Proteobacteria, Cytophaga-Flavobacteria, Firmicutes, and γ-Proteobacteria. Stratification was, however, recorded with depth at some sampling points such as the mean percentages of 17.0% and 9.6% for α-Proteobacteria and Cytophaga-Flavobacteria, respectively, at 160 cm in January 2001. Interestingly, developments or improvements of FISH-based protocols, including substrate-tracking autoradiography (STARFISH), informed and selective use of broad-spectrum phylogenetic group-specific probes, and omission of the fixation step, continue to be made in bulk soil, rhizosphere and wastewater treatment studies.298−302 Despite common technologies with the latter, there is apparent limited application in waste gas attenuation. Despite this, recent elegant proof-ofconcept studies such as Raman-FISH303,304 and combinations of genechips with FISH have been developed and used to monitor both bacterial and fungal populations.305 These should be applicable directly to odorant amelioration where the attendant limitations for “dirty” environmental samples such as soils, compost, etc., will be reduced especially with largely homogenous and clean support matrices such as glass beads, perlite, plastics, and sea shells. The application of stable isotope-labeled substrates replaced quickly the use of their radiolabeled counterparts, making the identification of functional microbial communities safer and more accessible. Specifically, the rRNA-stable isotope probing protocol was developed for a phenol-degrading community in a laboratory-scale reactor treating industrial wastewater,306 and has since been improved to also target mRNA.307,308 Novel modifications now entail fatty acid-, protein- and amino acid-

microbial diversity in different pristine and contaminated ecosystems than with 16S rRNA or functional gene clone libraries alone.290−292 Lazazzera293 discussed in detail the use of DNA microarrays to assess gene expression in biofilms. As exemplified by Stanley et al.,251 bespoke microarrays have been designed and applied to study physiological regulation of monospecies biofilm formation. The differential expression of 519 genes and environmental signals involved in key biofilm formation processes, including metabolism, motility, and transition between planktonic and surface-attached phases, were elucidated with a DNA microarray comprising 4074 of the 4100 open reading frames of the Bacillus subtilis genome. Therefore, these high throughput techniques, that also circumvent the known limitations of culture- and PCR-based protocols, could be applied for comparative analyses of gene expression underpinning biofiltration of different single- and multiple-component gaseous waste streams, from various sources and treated under different reactor configurations, operations and environmental conditions. As a result, detailed microbial mechanisms and responses to biofilter vs biotrickling filter mechanics, oxygen and nutrient limitations, moisture content, contaminant adsorption relative to the support medium and irregular biofilm development, as discussed by Devinny and Ramesh,248 could, potentially, be explored simultaneously. Concomitant with protocol upgrades and modifications to address specificity (to phylogenetic and functional occurrence/ distribution), sensitivity (of signal detection), competitive chemistries (for multiple probes) and subsequent requisite analysis of the typically large comprehensive data sets, are attempts to reduce analytical costs and, consequently, widen tool applicably and availability. As a result, advances in pyrosequencing have led to the development and application of barcoded Illumina paired-end sequencing (BIPES), which for example, was used by Zhou et al.294 to study the V6 tag of the 16S variable region. The authors, however, observed that this approach had a high sequencing error rate, which should be corrected by sequence reads overlap, removal of sequences with one or more mismatches within 40−70 bp and careful data analysis. Sequencing has been used in odorant remediation to identify, characterize, and reclassify functionally important strains and compare catabolic fungal strains with humanpathogenic phylotypes.189,259,295 Therefore, the new platforms should, subsequently, provide the recognized comprehensive high throughput and taxonomic identification capacity of pyrosequencing, relative to the Sanger approach, but with justifiable expenses particularly for the often comparatively simpler microbial communities underpinning waste gas biofiltration. As introduced above, study of microbial, chemical, and physical characteristics of biofilms is important for biofilter efficacy. Furthermore, investigations should, in principle, be made without compromising the integrity of the developing and/or mature biofilms. As a result, fluorescent in situ hybridization, largely developed and applied in wastewater treatment, is still one of the more popular techniques for ecogenomic analysis of gaseous waste stream attenuation, probably due to the use of similar treatment methods and technologies. Hence, 16S rRNA targeting probes and scanning confocal laser microscopy were applied for quantitative in situ distribution and three-dimensional visualization, respectively, of Pseudomonas putida in a toluene degrading biofilter.296 Similarly, cloning, sequencing and FISH analyses revealed a 8558



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The approaches discussed above are being extended increasingly with observational and modeling tools to explore defining biofilm properties in specific environments and/or measure variations across different environmental parameter gradients.190,250,296,314 These can be complemented further with microscopy, spectroscopy, fluorometry and cytometry techniques that are ideal either in situ for whole communities or ex situ with minimal disruption. Some examples include Raman spectroscopy, Fourier transform infrared spectroscopy and confocal Raman microspectroscopy,254,315−317 which have been applied specifically in molecular microecophysiology. Ultimately, although made in different contexts, these investigations have demonstrated that, where possible, optimum architectural design and spatiotemporal distribution re microbial diversity-function relationships should be studied in greater detail for subsequent gas biofiltration management and manipulation. Several researchers have suggested that the (physicochemical) characteristics of packing materials influence the deodorization capacities of biofilters since they facilitate biofilm formation and protect microbial communities from inhibitory compounds.30,60,274 The adoption of new materials as support matrices, for example, biochar, while commendable due to crucial properties of reduced costs, availability, buffering capacity, drainage, mechanical structure, and water retention,274 will mandate the use of novel cutting-edge molecular techniques. While some key methods were deliberated especially within the context of soil,171 most of these are transferable to biochar-supported gas biofilters. With the exception of soil- or compost-supported bioreactors, most of the challenges relative to “dirty” environmental samples would be alleviated considerably. Furthermore, the properties of biochar, such as high water-holding capacity, large internal surface area, a wide range of pore sizes, volume, and distribution, and the ability to protect microbial communities from desiccation and predation,318,319 should make it especially applicable. Therefore, the increased potential to create unique microgeographical habitats would, possibly, facilitate niche differentiation toward increased biodiversity and subsequent biofiltration process efficacy.267,320 The potential irreversible adsorption of the waste gas component(s) and/or microbial communities would, however, possibly reduce molecule bioavailability and requisite representative microecophysiological analyses, respectively. Overall, the microbial communities that facilitate odorant remediation are generally simple re species richness with common species identified in most studies. Comprehensive analyses are, however, still essential for the targeted maintenance of key functional strains and communities for efficient and consistent amelioration of single- and/or mixedmolecule waste gas streams under specific reactor configurations and operating conditions. In their review of 10 years of biofiltration literature, Cabrol and Malhautier267 noted similar trends of discrepancies depending on whether the microbial communities were characterized by high or low diversity and/ or dynamic or stable profiles. As a result, they emphasized the combined requirement for engineered ecosystem (biofilter)specific studies and global analysis and interpretation. Ultimately, this must be the focus, especially with the principal aims of improved reactor design and management, reduced footprints, and development of more stringent guidelines for increased odorant treatment efficacy and, thus, enhanced sustainability. Therefore, the realization, which has been made

SIP to explore, simultaneously, functional communities, for example in a benzene-degrading biofilm at several trophic levels.309 Also, although explored in gasoline-contaminated aquifers, the use of stable isotope-labeled MTBE, tert-butyl alcohol and BTEX, to then facilitate methyl esters detection in PLFA-SIP for in situ catabolic capacity probing, was demonstrated.310 Thus “biotraps” saturated with 13C-labeled contaminants were used to recover catabolic biofilms for subsequent SIP analysis of the intact structures. Currently, most laboratory-scale gas biofiltration studies employ waste streams with a single odorant molecule, which should facilitate DNA-, RNA-, and lipid-based stable isotope probing. Initially, application of the SIP-based protocols for the mono compound waste gases, on relatively simple, clean and homogenous support matrices, would potentially present simpler challenges for analyzing the dynamics of the ecologically relevant phylogenetic and metabolic communities and genes. For example, the issue of “cross feeding”, where the isotopic enrichment cascades to nonprimary substrate degraders resulting in a skewed representation of the principal catabolic strains, would be, possibly, minimized. The individual molecule models could then be used as baseline data for complex mixed waste odorant streams that are more representative of real industrial emissions. Generally, extensive reviews of the limitations and potential of SIP analysis in different systems311,312 provide core knowledge that is equally relevant to gas biofiltration. One of the earlier model studies313 used [2H8]styrene as a substrate for monocultures of styrene-degrading Gordonia sp. D7 and Pseudomonas sp. D26 as components of an experimental biofilter and involved gas chromatography−mass spectrometry (GC-MS) analysis for PLFA-SIP. The results of the requisite FAME deuteration optimization studies were then used to demonstrate the PLFA-SIP protocol on samples from a full-scale biofilter after 5 and 10 days of exposure to [2H8]styrene. Differences in fatty acid labeling patterns indicated styrene degradation by Pseudomonas-like strains in the experimental- and full-scale filters, but with the latter also characterized by members of the Pasteurellaceae clade, microeukaryotes and a then unidentified if potentially important styrene-degrading strain. The authors also observed an absence or unlabeling of characteristic fatty acids and concluded that this could provide useful evidence for the quantitative and functional (un)importance of the microbial genera/communities represented by these acids in the analyzed filters. The use of isotope-based analysis was reported latterly by Kristiansen et al.192 who applied DNA-SIP and microautoradiography-fluoresence in situ hybridization (MAR-FISH) to explore the microbial communities that degraded butyric acid and dimethyl disulfide in two full-scale biotrickling filters treating waste gas from a pig facility. Detailed molecular analysis focused, subsequently, on the more efficient of the SKOV-type filters. Thus, MAR-FISH quantitative probing identified Actinobacteria as the predominant phylum for the butyric acid-degrading communities while coupled 16S rRNA gene sequencing of a 39-member clone library from the heavy isotope-labeled DNA identified the presence of Microbacterium, Gordonia, Dietzia, Rhodococcus, Propionibacterium, and Janibacter spp. from this clade. The DMS assimilating members were confirmed by a combination of DNA-SIP and MAR-FISH and were found to consist mostly of Actinobacteria with some Flavobacteria and Sphingobacteria strains. 8559



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distribution and EPS accumulation control must be exercised together with excess removal. These can be effected by physical (mechanical/hydraulic), chemical (load controls or additions of oxidants, surfactants, bactericides or hydrolyzers) and biological methods (predation), and improved design and operation249 within the context of reduced reactor footprint. 4.1. Moisture Content. Typically, water applications may be made via inlet gas humidification, direct bed additions or humidification and periodic direct bed applications. 335 Although moisture content was identified as the single most important factor of biofilter operation,336 particularly in biotrickling filters where excess water facilitates molecule absorption, its control can be quite difficult due to: drying, through low inlet humidity,337 exothermic microbial activity, and reactor surface cooling/heating; and wetting, by watersaturated inlet flow, reactor surface cooling/heating, and oxidative generation.338 The goal is to satisfy the water activity requirements of the catabolic species while maintaining the mass transfer rates of the target molecule (including its adsorption/desorption behavior re the biofilm or support medium), oxygen and catabolic intermediates/products.338 In addition, the water content contributes to the buffering capacity.339 Work with a compost-packed biofilter for toluene demonstrated the importance of water content when an elimination capacity decrease of 50% resulted from a matric potential change from −20 to −300 cm water.338 Characteristically, the literature records optima between 40 and 60% (wet weight) with inlet humidity >99%. A higher moisture range of 65−70% was, however, reported in the bench-scale biofiltration (compost/wood chips support) of dimethyl sulfide by a microbial community of Bacillus sphaericus, Bacillus megaterium, and Paenibacillus polymyxa, as identified by FAME analysis.157 Overall, increased removal efficiency resulted due to an improved empty bed contact time (EBRT) of 384 s from a low DMS inlet rate (0.484 g m−3 h−1). Where the content is suboptimal, problems can develop such as high back pressure and low gas retention times; oxygen transfer limitations due to a limited air/water interface and, hence, anoxic zones; and low pH. Despite these, PrenafetaBoldú et al.107 reported successful amelioration of toluene, ethylbenzene, and p−xylene by mixed bacterial and fungal communities in xerophilic (20%) biofilters. Parallel 16S and 18S rDNA DGGE profiling, qPCR, sequencing and scanning electron microscopy were used to determine community composition, structure, abundance and distribution in the inoculum, support medium (pre- and postbiofiltration) and operational biofilters. Stable and variable gene copy numbers were recorded for bacteria and fungi, respectively, for p-xylene and toluene, while a predominance of fungi, particularly Exophiala oligosperma, on the pelletized animal manure/ sawdust support medium resulted for toluene degradation. 4.2. pH. Although pH values between 6 and 8 are regarded as optimal for gas biofiltration, it has been shown that mineralization of hydrophilic compounds such as reduced organic acid vapors and ammonia is favored near neutrality while hydrophobic styrene and methyl mercaptan require acidic conditions.340 For hydrogen sulfide, as the first odorant gas to be ameliorated by biofiltration, it is unsurprising that this molecule continues to receive attention.37 Reduced mass transfer limitations commend alkaline pH regimes for its solubilization. Work with a biotrickling filter operated at pH 10 and inoculated with a sulfoxidizing microbial community demonstrated that with a gas contact time of ≤6 s and a gas

for nonbiological methods, for example, ionization for reduced odorant concentration,321 must be matched for microbial communities whose geographical spatiation, architecture, structure and activity drive the biofiltration process. While taking cognizance of their inherent limitations, the well established potential of molecular microecophysiology techniques, for bacterial, archaeal, and fungal catabolic strains, as applied in other ecosystems and waste management biotechnologies, should also be advocated in gas biofiltration. For example, a microbiological biogeography survey of 1010 soil types (sampling squares of 2331 km2 each) across the U.K. that entailed ecogenomic protocols such as t-RFLP and sequencing and implemented during 2007, has been reported.322 Although ambitious, a similar audit could be considered for gas biofiltration, perhaps first by industry, molecule or bioreactor type/configuration. This could be expedited by exploiting developments and improvements in (targeted) metagenomic analysis, in particular, with screening for specific functional communities underpinning the degradation of individual and/ or mixed air polluting molecules such as aromatic compounds.323−325 Also, in contrast to other ecosystems, odorant attenuation studies often include the recording of metadata such as gas flow or hydraulic loading rate, organic loading rate, hydraulic retention time, pH, temperature, humidity, etc. These, in combination with the increasingly high throughput microbial ecology analyses, should facilitate comparisons between different reactors and treatments.266,267 Such investments would ensure a greater depth of knowledge toward more robust, reliable and sustainable biological alternatives for odorant treatment to then counter the still considerable reliance on engineered physical and chemical methods.

4. PROCESS OPTIMIZATION Process optimization must be made for each molecule, in fluctuating loadings, with respect to the key variables of waste gas composition, inlet concentration, flow rate, moisture content, pH, temperature, nutrients, stress response (including EPS production), etc. Yang et al.249 reviewed the load control of biofilm growth rate and identified decreasing rates across the biofilter. The workers developed equations, complementing previous microbial kinetic parameter determinations,326 to describe biofilm thickness variations with time, which accounted for biomass accumulation and decay (detachment/ hydraulic scouring). They also considered the complexity of microbial association biofilms in which primary and secondary catabolisms,327 predation, cryptic growth and endogenous respiration are all operative. Although, as reviewed by Yang et al.,249 models for biofiltration248,328−330 and the component pore networks331 have been developed, their efficacies in bioreactor design and operation have still to be realized fully. It is clear, however, that both uneven biomass distribution and accumulation can result in suboptimal biofiltration through clogging139,332 (possibly necessitating removal by physical and chemical interventions333), pressure drop and gas channelling.334 A physical approach was demonstrated by Ryu et al.139 who used a pilot-scale anticlogging biofilter system with intermittent excess biomass removal to treat ammonia and VOCs at efficiencies ≥97% independent of fluctuating inlet gas concentrations. It must be recognized also that a proportion of the biomass may be inactive247,267 and this may increase with time, thus necessitating regular monitoring and analyses such as viable staining and SIP-/FISH-based ecogenomics.60,91 In general, to retain protracted biofilter efficacy, biomass 8560



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thermophilic benzene and toluene catabolic strains dominated by Rubrobacter xylanophilus and Mycobacterium hassiacum. 4.4. Nutrients, Waste Gas Composition, and Pollutant Concentration. If the gas is the carbon/energy source, depending on its composition, concentration and bioavailability, and the packing material, there may be a requirement for periodic additions of carbon, nitrogen, phosphorus, and trace elements to the bed or by an aerosol or recycled liquid stream, with the latter also obviating pressure drop.348 The importance of nutrient supplementation was demonstrated in n-hexane Rhizoctonia solani biofilters when high elimination efficiencies (160 g m−3 h−1) and shortest acclimation times (7 days) for the critical load of 55 g m−3 h−1 were recorded in the presence of wheat bran.223 Similar efficacy increases were recorded when sawdust, urea, and rock phosphate supplementation was made to a cattle manure support medium to realize a C/N ratio of 30:1 to treat ammonia and VOC from a manure composting facility.143 For methane biofiltration, Ménard et al.128 recorded a successful elimination capacity of 39 g m−3 h−1 at 28−30 °C but reducing the nutrient supplementation from 1500 to 250 mL d−1 increased clogging. Huang et al.142 also researched methane oxidation and explored the impacts of gas flow rate, packing material, moisture content, pH, and concentrations of N, P, K, Mn, and Cu. The key factor of nitrogen limitation of biomass growth was shown in a compostpacked toluene biofilter when additions of ammonia or nitrate raised the elimination capacity by a factor >10.338 The required concentrations of key elements can be determined relatively simply through biofilm chemical analysis and reference to the growth-limiting substrate concentration of the target molecule(s). As a result, attendant detailed analyses have determined nutrient bioavailability from the waste gas, support media, and specific supplementations during the attenuation of different molecules. If an organic support medium is used this, initially, could be the nutrient source. So, for example, with a packing material such as char, as introduced above, limited concentrations of nutrients181 could be released to support the microbial population. Alternatively, a constituted support, such as the nutrient containing polyvinyl alcohol/peat/potassium nitrate composite bead,349 could be used to maintain high percentage removals during extended operation. Indeed, Gaudin et al.217 developed a calcium carbonate-based packing medium specifically to provide N as diammonium phosphate (Am) or urea phosphate (UP) and enable C, Ca, and P release assessment. Laboratory-scale biofilters packed with UP 20 and pine bark to treat hydrogen sulfide and ammonia showed increased removal efficiency for concentrations ≥100 mg m−3 for the former. An inherent buffering capacity was also recorded from the substratum with the biofilter pH maintained generally at or near neutral. Protein determination, microbial growth and oxygen consumption analyses also showed the fastest and highest growth, whereas cohesion capacity experiments recorded sustained biomass attachment and biofilm integrity on UP20. The addition of vitamins and trace elements may be necessary, especially in anoxic reactors. Thus, as already discussed, the addition of CuII(EDTA) to the nutrient medium in a rotating drum biofilter enhanced nitric oxide attenuation with the denitrifying removal efficiency increasing from 85 to 99.1%.275 Concomitant shifts in microbial profiles were confirmed by 16S rRNA gene-based DGGE and sequencing. Despite being labile substrates, influent waste gases can also, potentially, inhibit microbial activity through load fluctuations

concentration range of 2.5−18 ppm, 98% oxidation to sulfate resulted.341 Similar efficacies were also reported for filters packed with polyurethane foam, sugarcane bagasse and coconut fiber, at near neutral pH,35 and fresh carbon and exhausted carbon although the pH values were not stated.31 In contrast, maximum removal of the gas in a compost-packed biofilter was reported at pH 3.2.342 Microbial catabolic activities under both oxic and anoxic conditions can affect reactor pH with either inhibitory or noninhibitory outcomes. For example, acidogenesis that exceeds downstream oxidation during the initial steps of ethanol degradation can lead to biofilter failure. Steele et al.343 studied this phenomenon during the attenuation of 100 ppm ethanol at a 1.5 L min−1 air flow rate and 20 s EBRT. In general, despite a relatively high diversity acclimatized community at pH 4, failed treatments were reported subsequently at pH 4.5 and 5 for lava rock and sand-supported biofilters, respectively. In contrast, in hydrogen sulfide treatment, although there were fluctuations, Omri et al.153 recorded a decrease in pH from 7.8 to 2.5, due to sulfate production, in the down layer where the sulfide concentration and subsequent oxidation, catabolic microbial diversity and dominance of eukaryotic populations were highest. The importance of pH control was demonstrated in a study of 1,2-dichloroethane oxidation by Xanthobacter autotrophicus GJ10 in the presence of carbon dioxide.127 Although dehalogenation in elevated CO2 concentrations was unaffected at pH values around 6, more acidic conditions reduced the transformation rate coefficient by 25%. Successful conversion of ammonia to nitrogen gas in a two-stage process (biotrickling filtration nitrification followed by denitrification) also necessitated careful pH control.344 Since it cannot be measured directly in the biofilm but only indirectly as an aqueous extract from the support medium and/ or liquid stream (of biotrickling filters), accurate/representative pH measurement, which is independent of the extraction protocol, remains a key challenge. Nonetheless, with low cost a principal driver of all waste treatments, pH control may be made by the addition of a solid buffering agent such as dolomitic limestone,341 lime, chalk, marl or oyster shells. 4.3. Temperature. Preheating/precooling the influent gas controls the temperature between 20 and 40 °C. For methane biofiltration it has been shown that in a laboratory-scale reactor the optimum elimination capacity (39 g CH4 m−3 h−1) for an inlet load of 67 g CH4 m−3 h−1 was obtained with the temperature range of 28−30 °C.128 For hydrogen sulfide, a temperature decrease from 25 to 7.5 °C resulted in a removal efficiency decrease of 80%.342 It must be recognized, however, that microbial activity can result in temperature elevations of 10−20 °C above ambient346 and lower both solubilization of the target molecule(s)339 and enzyme activity, and accelerate cell death.347 Nevertheless, thermophilic biofiltration was reported by Cho et al.141 who isolated a catabolic inoculum from a high-temperature compost for subsequent attenuation of a hot mixture of gaseous benzene and toluene (0.2−12 g m−3) with and without yeast extract augmentation. Maximum elimination rates of 1650 g m−3 h−1, equating to ≥90% removal efficiencies, were recorded at 60 °C during 170 days of operation, with increased microbial community and reactor stability in the yeast extract supplemented biofilter. Despite higher degradation rates for benzene than toluene by some members (suggesting a degree of inhibition), DGGE profiling and sequencing confirmed generally the occurrence of 8561



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cation). More elegant proof-of-concept studies with fluorescent and stable isotope probe-based techniques such as FISH, DNA-/RNA-/PLFA-SIP, etc., could then be coupled with sequencing for subsequent identification of the community members that are grazed preferentially in relation to the recorded biofilter success or inefficacy. 4.6. Porosity. Clogging and channelling have been recorded in response to some support media (e.g., compost and soil), molecule mineralization (e.g., VOC), nutrient augmentation and the predominance of specific taxa and genera that are filamentous and/or high producers of EPS.190,198,331 Thus, regular assessment for bacterial- and fungal-derived clogging indicators should be central to biofilter efficacy monitoring. As already discussed, tools such as 16S/18S rRNA/rDNA DGGE are effective, whereas carbon and nitrogen mass balance calculations could be used to determine the role of nutrients in EPS production.220 Stable isotope- and radio-labeling could effect more precise mass balance determinations with SIP/ radiolabeled microecophysiology techniques then providing simultaneous linkages to microbial community structure and function. Although both intra- and interparticle porosity are essential characteristics of effective support media, the correlation between them and successful gas biofiltration is tenuous. Nevertheless, air-filled porosity determinations by air pycometry for organic matrices such as compost and wood chips have been reviewed extensively by Ruggieri et al.,351 and have direct relevance to biofiltration, especially to facilitate calculations of the actual retention times. Although air pycometry was not employed, Sakuma et al.60 made detailed analyses of particle size, dry packed bed density, packed bed porosity, microporosity, and crushing strength of cattle bone PorCelite (CBP), PorCelite, perlite, and open-pore polyurethane foam. Their efficacies for toluene degradation in reactors operated for >8 months under three different conditions of biotrickling filtration with nutrients, and biofiltration with or without nutrients were then compared. DAPI staining, protein analysis and DGGE profiling indicated increases in cell density and viable cell counts and differences in diversity concomitant with maximum toluene elimination capacity (∼75−80 g m−3 h−1) without pressure drop increases in the CBP-supported biofilters. Thus, following the multiplex detailed analysis, the researchers confirmed previous conclusions1 that support/ packing micro-, meso-, and macropore structure and distribution, chemical composition, surface chemistry, and absorption capacity played important roles in biofilter performance.

and chemical interactions in mixed gas streams. For example, although it could be cometabolized in their presence, MTBE addition reduced the maximum individual elimination capacities of benzene, toluene and xylene to 75, 100, and 300 g m−3 h−1, respectively.123 Also, macrokinetic analysis of mixed gas treatment in an upflow-operated biofilter showed that pxylene degradation was inhibited by toluene, whereas toluene attenuation was enhanced by p-xylene.350 The authors proposed several causal mechanisms including steric hindrance and outcompetition for similar catabolic enzymes and pathways. For molecules with low water solubility, additions of nonaqueous phases such as silicone oil, large-branched alkane or plastic polymer have been made to facilitate gas transfer, reduce microbial toxicity and buffer concentration fluctuations. A detailed review by Kraakman et al.183 presented findings of studies made between 1999 and 2011 on different target molecules (BTEX, hexane and methane), catabolic taxa/strains, nonaqueous phases and biofilter configurations, with a predominance of stirred tank reactors. In general, different nonaqueous phases effected removal efficiencies that were pollutant- and biofilter-specific. These deliberations and previous work on microbe-oil interactions have, however, exemplified their complexity. Thus, additional considerations for successful biomass recovery, to ensure extraction of high quality high quantity biomolecules (RNA, DNA, proteins, and fatty acids), would be particularly central to successful and representative phylogenetic, functional and structural ecogenomic analyses underpinning reactor efficacy determinations. Generally, substrate and electron acceptor bioavailability have direct impacts on microbial community structure and distribution, and thus, biofilter efficacy. As a consequence, HNO2-based inhibition and oxygen consumption outcompetition by heterotrophic strains led to stratification and restriction of ammonia-oxidizing bacteria to the outlet section of a trickling biofilter.190 Reactor stability and efficacy can, however, be maintained singly by robust microbial “super” strains but, most likely, by communities that are functionally, compositionally, and spatiotemporally dynamic and diverse. 4.5. Predation. As discussed above, predation can have direct impacts on microbial diversity, density, community structure, stability, and thus, dynamic functional capacity. Grazing reduces biofilm thickness to maintain efficient gas migration, keep airflow resistance low and obviate basal sloughing. Thus, although growth of Tetrahymena pyriformis was inhibited by 3.35 g m−3 toluene, for lower loadings (1.16− 1.33 g m−3), the protozoa decreased the toluene-degrading bacteria by 80%.215 Similarly, mites were reported to predate fungi in styrene gas attenuation.214 It is apparent that profiling of biofilter microbial communities during inoculation, reactor start-up, efficient operation, failure (due to clogging, pH, channelling, biofilm destruction, etc.) and down-time phases should become part of the structured monitoring, maintenance and management protocol.146,190,267 Initially, rapid and costeffective profiling methods (Table 3) can establish the community spatiotemporal dynamics, in relation to structure, composition, diversity, and function at these stages, and predation-related reactor efficiency or malfunction. Specifically, where possible, predators can be recovered, lysed and the ingested microbial strains characterized. Thus, simple experiments could first entail tracking a constructed single gas molecule-degrading microbial community using known prey and predator inocula sizes (D.A. Wright, personal communi-

5. BIOFILTRATION EFFICACY To evaluate this, five key parameters may be considered: empty bed contact/residence time;27,62,57,90,142,157,352,353 removal efficiency,27,33,49,69,128 which should approach 100%; elimination capacity,90,128 which is the maximum amount of target molecule eliminated per unit volume; mass loading,69 where cognizance must be taken of the critical substrate concentration and the possibility of filter bed clogging;354 and surface loading, including intermittent loading355 and nonsteady state operation,356 where high loading rates must not be accompanied by bed drying. Also, the effect of carbon/energy source limitation357 must be determined. In field situations, biofilters are operated in transient-states and are subjected to shock-loads and variations in feed, inlet gas flow rate, moisture content and temperature together with intermittent shut-downs, excess biomass removal, 8562



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etc.75,107,209,333,356 Inevitably, these perturbations “challenge” the catabolic species and, therefore, the short- and long-term bioreactor performance so necessitating attendant physiological, phylogenetic and phenotypic microbial characterization. Potentially, a cyclic structural and functional community profile, fluctuating between phases of acclimatization, stable/steadystate, efficacy and failure, may result independent of the total reactor operation time. Ultimately, dynamic and robust responses underpinned by microbial communities with resilience, memory, stability, and resistance267 should then define efficient, successful, and reliable biofiltration. In general, comprehensive macroscale analysis should be used increasingly with relevant microecophysiology tools to facilitate links between improved microbial community stability, pollutant removal, and overall reactor efficacy.60,102,146,267,277 This may be implemented for specific reactor types under a range of variables, for example, polluting molecule/class, pressure, operation strategy, oxic/anoxic conditions, temperature, pH, support medium, nutrients, hydraulic and organic loading, etc. Finally, it must be recognized that although some biofiltrations, such as rotating drum nitric oxide attenuation,164 are operated under anoxic conditions, potentially, anoxic microhabitats can be present in aerobic reactors where their occurrence and distribution depend on a range of parameters including the reactor type/configuration, nutrient and temperature regime, support matrix and the dominant microbial taxa/ strains, for example, EPS producers. Consequently, parallel ecogenomic probing for taxa-specific aerobic and anaerobic catabolic microbial communities should be made since this will reflect the total functional capacity and, hence, efficiency of the biofilter.

The costs of aerosol control and analysis can be offset by exploitation of the aerobic (carbon dioxide) and anaerobic (methane/carbon dioxide) mineralization products, which in turn, eliminate their inimical potential to climate change. Direct carbon dioxide exploitations include generation of refrigerant, methane, and reduced organic acids and higher plant (cucumbers/tomatoes) growth promotion. Via algae, biocides, antibiotics, organic acids, liquid hydrocarbon fuels, and olefins can also be produced.

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SUMMARY Although gas biofiltration was first used in 1923 to ameliorate wastewater treatment plant hydrogen sulfide emissions, it was not until the 1950s that it became more routinely practised. Since then, the range and complexity of gases have continued to increase with approaching 70 molecules documented by 2010. Physical and chemical methods, either singly or combined with biological treatment, have also been used while different aerobic/anaerobic bioreactor configurations, with various organic/inorganic/combination support media, have emerged. Biofiltration is the most cost-effective and sustainable technology despite the tendency for bioreactor overdesign. Support medium selection does, however, often overlook the physical/chemical/biological properties in favor of low cost, availability and recalcitrance. Appraisal of one support, char, exemplifies the selection criteria that must be considered. Although organic media, such as compost, pelletized fertilizer, and granulated sludge, can provide catabolic populations, most biofilters require inoculation. Thus, enrichment/isolation (and culture improvement) can be key elements of treatment success. Where a gas mixture or complex molecule is the target, a microbial community would be the more likely outcome and would require detailed molecular characterization to optimize process operation. In contrast to soils or sediments, gas biofilters are “clean” and characterized probably by more catabolically active communities, albeit dependent on individual reactor configuration, waste stream and process operation. Nevertheless, the challenges of representative sampling, particularly of industrial-/full-scale operations, and the presence of potential inhibitors, for example, for efficient DNA/RNA extraction, PCR and downstream analysis, remain. Therefore, existing microecophysiology tools, their advantages and limitations, as well as their current and potential applications in gas biofiltration have been discussed. Many studies have, however, lacked this scrutiny with the microbial biomass considered in toto. Essential support medium attachment is dependent on the cell physicochemical properties, the packing material type and the liquid phase together with the start-up protocol. Treatment improvement must target biofilter microbial stratification (numerical/species) and control/removal to direct reduced footprint redesign, possibly incorporating multistage systems, and operation (moisture content, pH, temperature, nutrients, and loadings). For the discharge gas stream, increasingly mandatory bioaerosol capture/destruction facilitates, in turn, mineralization product exploitation.

6. BIOAEROSOL EMISSION CONTROL Despite cost implications, bioaerosols of fungal spores and/or archaeal and/or bacterial cells in the effluent gas stream must not be discharged to the environment. A review by PrenafetaBoldú et al.259 highlighted the biohazard potential from the enrichment of possibly pathogenic fungal strains especially during biofiltration of aromatic hydrocarbon gases. Consequently, a range of capture/destruction technologies have been developed and these include (nano)fibrous filtration with358/ without359 microwave irradiation, titanium dioxide-coated stainless steel sieving360 and titanium dioxide thin films/glass reactor filtration with UV radiation,361 carbon nanotube filtration,362 photocatalysis,363,364 microwave irradiation,365 dielectric barrier discharge,366 hybrid UV-thermal,367 and biofitration/bioscrubbing. For the last, a 1 year field study showed 11% and 71% reductions of mesophilic bacteria and thermophilic fungi, respectively,368 whereas decreases in total bacterial (25 to >90%) and fungal (≥60%) counts resulted from a half technical-scale investigation of piggeries.369 Similar efficacy was reported for an organic medium of halloysite (20%), compost (40%), and peat (40%), which effected 99% removal of Gram-negative bacteria (16% total bacterial population) from a chicken hatchery gas biofiltration.370 Each of these physicochemical and biological technologies has advantages and limitations in relation to efficacy, specifically when the gas effluent discharge and process time are considered, hence these must be evaluated carefully and also in relation to attendant costs. Ultimately, to determine emissions treatment success both culture dependent371 and culture independent372,373 methods may be employed.

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AUTHOR INFORMATION

Corresponding Author

*Phone: +44 (0) 1642 342525; fax +44 (0) 1642 342401; email: [email protected]. Notes

The authors declare no competing financial interest. 8563



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ACKNOWLEDGMENTS We thank the three anonymous referees for their critical appraisal and constructive comments. The Teesside University International Visiting Academics Scheme is also acknowledged for supporting this work.

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