Monitoring Bacterial Twitter: Does Quorum Sensing Determine the

Critical Review pubs.acs.org/est

Monitoring Bacterial Twitter: Does Quorum Sensing Determine the Behavior of Water and Wastewater Treatment Biofilms? Joshua D. Shrout*,†,‡ and Robert Nerenberg† †

Department of Civil Engineering and Geological Sciences, University of Notre Dame, Notre Dame, Indiana, United States Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana, United States

‡

ABSTRACT: Bacteria have their own form of “twitter” communication, described as quorum sensing (QS), where bacteria emit and sense chemical signal molecules as a means to gauge population density and control gene expression. Many QS-controlled genes relate to biofilm formation and function and may be important for some water and wastewater treatment biofilms. There is a need to better understand bacterial QS, the bacteria biofilm aspects influenced by QS in engineered reactors, and to assess how designs and operations might be improved by taking this signaling into account. This paper provides a critical review of QS and how it relates to biofilms in engineered water and wastewater treatment systems and identifies needs for future research.

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INTRODUCTION Bacterial biofilms are ubiquitous, present in nearly every environmental system where there is flowing water. Accordingly, biofilms are found in many water and wastewater treatment systems, where they may play beneficial or detrimental roles. For example, robust biofilms are needed for treatment processes such as trickling filters, moving bed biofilm reactors (MBBRs), and granular sludge.1−3 However, biofilms and associated extracellular polysaccharides (EPS) are a nuisance in nanofiltration (NF) systems and membrane bioreactors (MBRs), decreasing membrane filtration fluxes.4−11 Also, biofilms in potable water distribution systems and their points of service (e.g., shower heads) may harbor pathogens, and it is not clear if these biofilms are prone to upset and release of pathogens.12−14 Table 1 lists biofilms commonly found in water and wastewater treatment systems and their effects. Since biofilms play such an important role in the water and wastewater treatment field, developing new means to encourage or discourage biofilm growth, or manipulate their function, is of great practical interest.15,16 While biofilm formation and behavior traditionally has been thought to depend only on environmental conditions, such as substrate concentrations, we now understand that some bacterial species may modify their behavior in a coordinated fashion, using a type of cell-to-cell signaling known as quorum sensing (QS). QS signaling takes place via chemical signal molecules, which are emitted and detected as a means to gauge population density. When a quorum is detected, the expression of certain genes is induced. Such “sociomicrobiology” traits can © 2012 American Chemical Society

Table 1. Bacterial Biofilms Important to the Water and Wastewater Environments area drinking water

wastewater

process

role of biofilms

reference

filtration membranes

negative, biofouling

6,110−112

biologically active filters riverbank filtration membrane-supported biofilm reactors integrates fixed-film activated sludge moving bed biofilm reactor membrane bioreactors tertiary filters

positive, biocatalyst

113−115

positive, biocatalyst positive, biocatalyst; negative, biofouling positive, biocatalyst

116 16,117,118

positive, biocatalyst

1,120

negative, biofouling

2,121,122

positive, biocatalyst; negative, biofouling positive, biocatalyst

123

granular sludge

119

3,124,125

be important in initial biofilm formation, defining the composition of the biofilm, and determining the behavior of biofilm communities.17−21 This sensing may be manipulated to encourage or discourage biofilm formation and other aspects of biofilm behavior.22−24 Received: Revised: Accepted: Published: 1995

November 3, 2011 January 14, 2012 January 20, 2012 January 20, 2012 dx.doi.org/10.1021/es203933h | Environ. Sci. Technol. 2012, 46, 1995−2005

Environmental Science & Technology

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Table 2. Quorum Sensing Bacteria Present in Water and Wastewater Treatment Systems bacterial genus Acinetobacter Aeromonas Arcobacter Bacillus Comamonas

Variovorax Vibrio Xanthomonas

potential pathogen unknown

Corynebacterium Legionella Nitrobacter Nitrosomonas Nocardia Pseudomonas Sphingomonas

a

significance/role unknown unknown unknown unknown unknown, but displays robust heterotrophic metabolism unknown potential pathogen nitrification: nitrite oxidation nitrification: ammonia oxidation filamentous bulking of activated sludge unknown, but displays robust heterotrophic metabolism unknown, but displays robust heterotrophic metabolism unknown, but degrades many compounds

signal type

QS-regulated activities

reference

AHL AHL, AI-2 AI-2 AI-2 AHL

unknown biofilm formation unknown sporulation hormone degradation

66,126 70,127,128 127, Genbank search 65,129 65,130,131

AI-2 AHK AHL AHL Peptide AHL, PQS

unknown virulence unknown unknown antibiotic production (bacteriocins) biofilm formation, EPS production, interspecies competition and denitrification unknown

65, Genbank search 42,127,132 67,133 67,134 135 18,63,65,66,127,128,136

degradation of other species AHLs

67,106

biofilm formation, virulence EPS production

42,43,127,128 60,66

AHL AHLdegradersa AI-2, AHK DSF

66,137

Variovorax paradoxus displays no AHL signaling system but degrades other species signals.

“quorum sensing” because it depends on the bacterial cell density, where a minimum population, or quorum, is required to initiate the behavior.28,30,34 QS typically involves production of an extracellular signal that affects a concentration-dependent response. In general, the production of signal molecules is continuous at some basal level for each cell, but responses are only initiated when signal reaches a threshold concentration. A quorum of bacteria is required to produce signal concentrations above the threshold. As bacteria grow and the population increases, the concentration of signal increases because there are more signal producers present (Figure 1).28,30 Thus,

An ongoing question is whether QS effects are present and significant in mixed-culture biofilms in water and wastewater treatment systems. In such systems, not all of the community members are capable of QS, and initial biofilm formation and subsequent biofilm behavior may be governed by non-QS species. A table of bacterial species that are identified in water or wastewater systems and are known to possess QS mechanisms is shown in Table 2. Certainly this list includes only select microorganisms important to water and wastewater treatment systemsbut the number of QS species continues to increase with further study of QS regulation and interspecies interaction. Most of the bacteria identified in these treatment systems have not been cultured, much less specifically studied to understand their genetic and physiological attributes; application of recent advances in microbial ecology and sequencing point to water treatment system microbes that possess signaling traits.25,26 QS was first described by Tomasz in 1965 who detailed a “competence factor” required for DNA uptake in Streptococcus pneumonia.27 Numerous QS signal molecules and communication pathways have been elucidated since then.28−31 Although the pathways are often complex, a universal feature is that a small group of signaling chemicals play key roles. The universality of this bacterial communication suggests that manipulating bacterial communication may be a viable strategy to control biofilm growth formation, composition, and behavior. The potential for “jamming” QS circuitry has been reviewed previously for the control of infectious diseases;32,33 however, no previous publication has comprehensively addressed QS with respect to environmental engineering processes. Here, we review QS bacterial communication in the context of water and wastewater treatment biofilms and discuss the importance to the water and wastewater field.

Figure 1. Acyl homoserine lactone (AHL) structure. Variations to the acyl side-chain are common at the R-position (hydroxyl or ketone group) The acyl side-chain length (n) is typically 4−14 carbons in length; a select few AHLs contain unsaturated carbon bonds.

bacteria are capable of monitoring their own population density and use information to coordinate their activity. Numerous types of signaling molecules are used by bacteria, and a variety of different genes are regulated by QS for different bacteria, as discussed in the following section.

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TYPES OF QS SIGNALS There are several types of QS signaling mechanisms used by bacteria. Variations to the regulatory scheme include the chemical structure of the signal molecule and the detection mechanism.28 The main mechanisms are described below. Acyl-Homoserine Lactone Signals of Gram Negative Bacteria. To date, the predominant Gram negative bacterial QS signaling pathways utilize acyl-homoserine lactone (AHL) signal molecules. The AHL structure consists of a fatty acid chain linked by an amide bond to a lactonized (i.e., cyclic ester) homoserine (Figure 1).28,29,35−37 More than 100 species of Proteobacteria are known to contain AHL signal genes. AHLs

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QUORUM SENSINGBACTERIAL SYNCHRONIZED ACTIVITY QS is a method of cell-to-cell communication that affects gene expression and physiological behavior of entire microbial communities. First used in 1994, the phenomenon is called 1996

dx.doi.org/10.1021/es203933h | Environ. Sci. Technol. 2012, 46, 1995−2005


Critical Review

Figure 2. Schematic of Gram negative bacterial AHL-type QS. Transcription of QS-regulated “target genes” occurs by LuxR-homologue proteins only when sufficient AHL signal is present, which requires a minimum threshold, or “quorum”, bacterial cell population.

variable for different bacterial species, but many influence biofilm formation. While the functional details continue to be investigated by many researchers, AHLs have been shown to influence EPS production, surface motility, interspecies competition, and growth regulation for specific bacterial species in laboratory experiments. Minor variations to AHL signals and regulatory networks have recently been identified for Rhodopseudomonas palustris, Bradyrhizobium japonicum, and Silicibacter pomeroyi.39,40 Of these three examples, the signal molecule and its regulatory proteins are best detailed for R. palustris. The R. palustris LuxI/ LuxR homologues RpaI/RpaR produce and respond to an aromatic-containing homoserine lactone (p-coumaroylHSL).39,41 An additional variation to AHL signaling is the alphahydroxyketone (AHK) signals used by Legionella pneumophila and Vibrio cholerae. Signal production of AHKs appears similar to that of LuxI homologues where LqsA of L. pneumophila (or CqsA of V. cholerae) produces a freely diffusible signal molecule.42 Subsequent gene regulation differs, however, from AHL signaling as AHK signals cue a two-component signaling cascade more similar to the peptide signal regulation for Gram positive bacteria (described below). The AHK signals for L. pneumophila and V. cholerae appear to be important for virulence and have been linked specifically to biofilm formation in V. cholera.42,43 Peptide Signals of Gram Positive Bacteria. Most Gram positive QS bacteria utilize amino acid peptides as signal molecules. Precursor signal proteins are synthesized within the cell by ribosomes. Active signal molecules are generated by

are amphipathic molecules that are freely diffusible through cell membranes and are stable for long periods in aqueous solution. AHLs contain fatty acid chains of varying length but most often contain an even number of carbonsthis variation in side chain length, flexibility at the three-carbon position (hydroxyl or ketone group), and degree of saturation give great specificity to these signals, which can be differentially distinguished by bacteria. AHL QS signaling requires three key components for function: 1) the AHL signal molecule, 2) an AHL synthase protein to create the AHL signal, and 3) a regulatory protein that responds to the local concentration of AHL signal. A generalized schematic of AHL QS is shown in Figure 2. The AHL synthase and cognate regulatory protein are mostcommonly designated in context to their homology to the first known AHL proteins required for regulation of bioluminescence in the marine bacterium Vibrio f ischeri. V. f ischeri bioluminescence is controlled by the luciferase enzyme, and the genes and proteins important for luciferase production all bear the designation “lux”.38 The LuxI protein, named “I” for inducer, is the AHL synthase for V. f ischeri. Subsequently, proteins homologous to LuxI that produce AHL signal molecules in other bacteria are called LuxI homologues.28−31 Similarly, LuxR (“R” stands for regulator) homologous proteins sense the concentration of AHL signal and initiate a coordinated response by individual bacteria when a threshold AHL concentration is reached. The LuxR-homologue regulatory proteins initiate transcription of select genes when cued by a threshold concentration of AHL signal (Figure 2). The genes regulated by the various LuxR homologues are widely 1997



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before, during, and/or after transport.46 Besides proteolytic cleavage of some amino acid residues, peptide signals can be post-translationally modified in a number of fashions including amino acid dehydration.46 Thus, the peptide signals utilized for QS by Gram positive bacteria show great diversitythis presents a significant challenge to identify a global method of altering such signaling. Some signal peptides also function as antibiotics. Peptide signals known as bacteriocins have been identified in some Gram positive bacteria.47 Such dual function peptides are thought to serve bacteria trying to establish an ecological niche in a competitive environment. Perhaps the best-studied system of this subgroup of signals is nisin, produced by Lactococcus lactis−nisin is a lantibiotic, which are cationic peptides belonging to class I (modified peptides) antimicrobial peptides.46 Additional bacteriocins include Subtilisin of B. subtilis, carnobacteriocin of Carnobacterum piscicola LV17B, and Plantaracin A of Lactobacillus plantarum C11.47 Lastly, a bacteriocin called Nocardithiocin has recently been identified for a species of Nocardia.48 As Nocardia species are common disruptors of activated-sludge treatment systems, such signal peptides may be important to mixed-species engineered reactors in ways that are currently not understood. Bacteriocin-producing bacteria use their bacteriocins to control the competition in mixed-species systems to improve their access to nutrients. It would be useful to better understand the kinetics of bacteriocin effects upon mixed-species water and wastewater bacterial cultures to more effectively prevent upsets and potentially use bacteriocins as a method to control unwanted biofilm growth. AI-2 MoleculesInterspecies Signals. One of the more recently discovered group of QS signals, called AI-2, provides for the possibility of interspecies communication.31 AI-2 signaling appears to allow interspecies quorum sensing as many bacteria have a gene called luxS, required for synthesis of AI-2 signal.49 Multiple AI-2 signals are possible; variations form from rearrangement and spontaneous reaction of 4,5dihydroxy-2,3-pentanedione (DPD) synthesized by LuxS.50 Discovery of LuxS in both Gram positive and Gram negative bacteria supports the widespread prevalence of AI-2-type signaling. Homologues of the luxS gene have been identified in over 350 sequenced bacterial genomes51 and also in other bacteria whose genomes are yet to be sequenced. While many luxS genes have been identified and predicted using genomic techniques, few of the functions of AI-2 signaling are known. This represents a significant area of future research. AI-2 signaling was first described for the marine bacterium Vibro harveyi, where AI-2 regulates transcription of the luxCDABE operon involved in bioluminescence.45 AI-2 is also linked to pathogenic virulence, for example, AI-2 controls toxin production (α-, κ-, and θ-toxin) related to causing gas gangrene in Clostridium perf ringens.52 AI-2 signaling appears to be involved in biofilm formation for several bacteria, including Escherichia coli, Shewanella onedensis, Porphyromonas gingivalis, Salmonella typhi, and Streptococcus mutans.45,53,54 This is an active area of research as most of the specific functions controlled by AI-2 signaling that influences biofilm formation are not yet known. Perhaps the most has been determined for E. coli, where AI-2 signaling influences genes important to toxicity, cell growth, and EPS production55−57 AI-2 signaling has also been shown to be important to mixed-species aerobic granule formation in laboratory scale sequencing batch reactors.58

cleaving translated proteins to form short peptide chains, and for some bacteria these peptides become further modified before they are active signals.30,44 The QS principle is the same as in Gram negative bacteriathe cell ultimately senses and responds to a buildup of the extracellular signal concentration. However, unlike most Gram negative AHL signals, the peptide signal does not freely diffuse across the cell membrane.44 Export of signal peptides from the cell requires energy in the form of ATP to power an ABC transporter (Figure 3).44

Figure 3. Schematic of Gram positive bacterial peptide-type QS. A presignal peptide chain is synthesized in the cell. This peptide chain is exported from the cell via an ATP-dependent transport protein where the active signal molecule is either modified in the cell (shown) or external to the cell (not shown). Transcription of QS-regulated “target genes” ultimately occurs by sufficient extracellular peptide signal initiating a cascade of responses: a sensor kinase protein phosphorylates a response regulator protein that initiates transcription of target genes.

These peptide signals are then sensed by the cell using a dual-response regulatory cascade that utilizes phosphorylation to regulate activity.44 Most often, the peptide signal sensing begins at the cell surface by a dedicated receptor protein that functions as a histidine kinase sensor. Such histidine kinase sensors are, in general, well-studied two component regulatory systems and are common for regulation of many bacterial processes.30 Sensor kinases function by transferring phosphate to activate proteins. The interaction of the peptide signal with the sensor kinase in the cell membrane results in autophosphorylation of the sensor. This phosphoryl group gets transferred inside the cell to a cytoplasmic, DNA-binding, two-component system response regulator homologue. The phosphorylated form of the response regulator then modulates expression of quorum sensing-regulated genes. Gram positive bacterial peptide signals can be modified in multiple ways before they are fully active. The signal peptides tend to be small, very stable, and subject to post-translational modifications.30,44 The primary roles of these modifications are thought to affect activation and stability of the signaling molecule. The peptide signals can be linear or cyclic and typically range in size from 5 to 26 amino acid residues.44,45 Depending upon the bacterium, the signal peptide is processed 1998



Critical Review

Table 3. Bacteria Present in High Quantity in Select Membrane Systemsa bacterial genus Bosea Bradyrhizobium Burkholderia Flavobacterium Geothrix Ideonella Pseudomonas Ralstonia Rheinheimera Rhodopseudomonas Sphingomonas a

membrane system/source water RO/treated potable water; RO/tertiary? wastewater effluent RO/treated potable water NF/tertiary wastewater effluent NF/tertiary wastewater effluent RO/treated potable water RO/seawater desalination NF/tertiary wastewater effluent; RO/surface water NF/tertiary wastewater effluent RO/seawater desalination RO/tertiary? wastewater effluent RO/surface water; NF/tertiary wastewater effluent

EPS characteristics

reference

uncharacterized

138,139

B. japonicum EPS is a glucose, mannose, and galacturonic acid pentasaccharide B. tropica EPS is a glucose, rhamnose, and glucuronic acid polysaccharide uncharacterized uncharacterized uncharacterized P. aeruginosa produces 3 polysaccharides: alginate, Psl, and Pel; Psl and Pel are linked with QS. R. solanacearum EPS I is an acidic heteropolymer known to be regulated by QS uncharacterized uncharacterized S. chungbukensis EPS is a glucose, mannose and galactose polysaccharide

138,140 141,142 141 138 143 83,84,141,144 141,145,146 143 139 141,147−150

RO-reverse osmosis; NF-nanofiltration.

Other QS Signals. A “natural small molecule” (NSM)triggered potassium-leakage pathway of biofilm formation was recently elucidated in Bacillus subtilis.59 Under conditions such as nutrient stress, bacteria secrete small biologically active organic compounds called NSMs. Certain NSMs can insert into cell membranes and form channels that allow leakage of potassium and a cascade of events that affect EPS synthesis and biofilm formation. The diffusable signal factor (DSF) utilized by Xanthomonas spp. is a long-chain fatty acid; for Xanthomonas campestris the DSF signal is cis-11-methyl-2-deodeconic acid.60 At least one DSF-regulated function relates to biofilm formation as the bacterium seems to coordinately monitor nutrient conditions and DSF signal concentration; rich media conditions and the presence of DSF lead to a bacterial dispersion, while starvation and absence of DSF lead to EPS production, aggregation, and biofilm formation.61 The bacterium Pseudomonas aeruginosa also produces a nonAHL signaling molecule called Pseudomonas quinolone signal (PQS). PQS, a 2-heptyl-3-hydroxy-4-quilinone, plays a significant role in controlling some aspects of P. aeruginosa biofilm formation and has also been shown to significantly regulate denitrification.62,63

full-scale enhanced biological phosphorus removal reactor; they further assessed functionality of active bacteria using fluorescent in situ hybridization (FISH).26 These combined approaches allow for an advanced understanding of function in engineered systemsknowledge of the bacterial species and metabolic properties of a system gives us a better understanding of the “working parts”. Another example comes from water distribution system corrosion; researchers have recently confirmed previous evidence that metal-resistant bacteria reside in corroding pipes.68,69 Because biofilms are increasingly associated with such corrosion, increased knowledge of the impacting bacteria is needed to find solutions to protect the water supply. Hao et al. used a combined genomic-analytical chemistry approach to study QS in an activated sludge system; an entirely new AHL signal was identified that still needs to be further characterized.25 These many new reports continue to suggest or directly show the presence of QS-dependent biofilm forming bacteria in environmental engineering systems. The role of QS in biofilm formation is best understood in pure-culture laboratory systems. In 1998, it was reported that P. aeruginosa AHL QS greatly influenced biofilm structure.18 Since this initial study, numerous links have been made between QS and biofilm formation. This includes direct demonstration of biofilm phenotypes or associated factors important to biofilm formation for species frequently observed in water treatment systems (see Table 2). It is known that the QS activity of Aeromonas, Pseudomonas, and Xanthomonas species can improve aspects of biofilm growth and matrix composition.18,60,63,70 However, it is important to realize that much remains to be learned about the universal role of QS to biofilm formation. Most of the species listed in Table 2 do not have clear functions associated with their documented QS circuitry. The importance of Nitrobacter and Nitrosomonas to biological nutrient removal (BNR) process certainly can be used to highlight the need for future research in this area. As more BNR processes are implemented to address nitrogen removal from waste streams, successful efficient design and operation of BNR systems depends critically upon the activity of species that oxidize reduced nitrogen compounds. Yet, the growth, physiology, and QS of species in the Nitrobacter, Nitrosomonas, and other genera are not well understood. Because growth conditions (i.e., fluid dynamics and nutrient composition) can also have a profound effect on when QS is important,71−75

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POTENTIAL QS SIGNALING IN WATER AND WASTEWATER TREATMENT SYSTEMS How do all these QS signals affect water and wastewater treatment biofilms? Currently, our understanding of QS and biofilms in mixed-culture systems is limited, but it is likely that QS influences attachment and EPS production for many bacteria in wastewater treatment. A recent investigation has also suggested that bacterial response to phospohorus limitation involves QS.64 A partial list of known QS bacteria routinely identified in municipal wastewater treatment systems, e.g. refs 65−67, is provided in Table 2. It is primarily within the past decade that we have known more than a select few of the bacteria present in biofilms that form in treatment systems. In addition to identifying some mixed community members, improvements to and use of multiple molecular techniques is allowing researchers to better assess the predominant species in these mixed biofilm communities. For example, Kong et al. identified species of Proteobacteria, Bacteroides, Actinobacteria, and Chlorof lexi in a 1999



Critical Review

(and biofilm formation) for multiple species. Xu and Liu have shown evidence of AI-2 signal disruption using 2,4dinitrophenol treatment to remove biofilm bacteria from membrane surfaces.90,91 The natural fimbrolide (5Z)-4bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone produced by the marine red algae Delisea pulchra has been shown to disrupt AI-2 signaling by inhibiting LuxS function; AI-2 disruption has been shown for this fimbrolide molecule in E. coli, P. aeruginosa, Pseudomonas putida, and select Vibrio species.92−94 Alternatively, Lowery et al. chemically modified the AI-2 DPD precursor to form synthetic molecules that effectively block AI-2 function, including hexyl-4,5-dihydroxy2,3-pentanedione (hexyl-DPD).95,96 While the hexyl-DPD compound provides significant inhibition of AI-2 signaling in Vibrio harveyi and Salmonella typhimurium, the shorter half-life, naturally occurring fimbrolide molecules may be more acceptable for use in engineering reactors due to the very stable nature of the synthetic hexyl-DPD disruptor compound. Certainly any one chemical agent or process modification is unlikely to solve all accumulation of undesired biofilm growth. This is apparent from inspection of the wealth of knowledge in industry, medicine, and fundamental laboratory research. The best biofilm control practices are likely to come in combination, as evidenced in several laboratory studies that use a combination of targets to control biofilm growth. For example, Hentzer et al. used a furanone inhibitor of P. aeruginosa QS to increase efficacy of detergent or antibiotic biofilm killing.97,98 Similarly, Lauderdale et al. used exogenous addition of autoinducer peptide (AIP) produced naturally by Staphylococcus aureus to induce dispersal and increase sensitivity of these biofilms to antibiotic(s).99 Barraud et al.86 found that chlorine treatment was 20 times more effective at removing multispecies biofilms from water systems after exposure to nitric oxide (NO). Anti-Biofilm Agents. Other recent research has targeted the ability to specifically disperse and disrupt biofilm formation. There are at least two agents that seem to disrupt intracellular signaling to prematurely cue biofilm dispersal, not necessarily through QS pathways. The fatty acid cis-2-decanoic acid induces dispersion of E. coli, Klebsiella pneumoniae, Proteus mirabilis, Streptococcus pyrogenes, Bacillus subtilis, Staphylococcus aureus, the yeast Candida albicans, and P. aeruginosa biofilms; this compound is produced in small quantities naturally by P. aeruginosa.87 Similarly, addition of NO induces dispersal of Serratia marcescens, Vibrio cholera, E. coli, Fusobacterium nucleatum, Bacillus licheniformis, Staphylococcus epidermidis, P. aeruginosa, and the yeast Candida albicans.86,98 There are multiple appealing factors about the use of either of these compounds, which includes their multispecies efficacy (including both Gram negative and Gram positive bacteria), natural synthesis, and readily biodegradable characteristics. The effect of NO appears to act specifically by disrupting the intracellular secondary messenger cyclic di-GMP.98 Many researchers are currently working to better describe the specifics of secondary messenger signaling, but we do understand that many bacteria use increases or decreases in intracellular cyclic di-GMP levels to control their actions in response to exogenous environmental cues. Additional work into cyclic di-GMP signaling disruption has shown that it is possible to induce biofilm dispersal using proteins such as BdcA that bind to cyclic diGMP;100−102 adding an innocuous organism that overexpresses BdcA may be effective at dispersing unwanted biofilms with no chemical addition. The ability to “trick” the bacteria into

there is a need to study biofilm formation and QS of BNR bacteria under various potential operating conditions. Lastly, even for the species with identified QS-biofilm correlations, the activity of QS by nitrogen-oxidizing species has only been investigated under mixed-culture conditions in a handful of studies (e.g., refs 17,76, and 77). There is a need, therefore, to understand both the QS genes regulated and the environmental conditions that promote regulation in both pure-culture and mixed-culture bacterial systems. EPS Production. A significant factor in biofilm development, and membrane biofouling, is the self-production of matrix material containing a mixture of EPS, proteins, and nucleic acids. This matrix provides structure to these assemblages of cells, and for many biofilms, EPS appears to be the dominant component of matrix material. Our current understanding is that EPS acts as a primary scaffolding that aids in the attachment of the bacterium to a surface and further acts as a strong matrix material to hold biofilm cells together.78−80 Table 3 includes a list of bacteria and their known EPS components that have been identified in select membrane systems. To date, only two of the species listed in Table 3 have been shown to have QS-regulated control of EPS regulation. Very little is known about EPS production for most fouling species, and QS control strategies may prove useful to limit EPS accumulation on membranes. The interaction of EPS with various membrane materials is an active area of research as it becomes clear that EPS is a main component in biofouling.81,82 Understanding how bacteria regulate EPS production, bacterial attachment, and biofilm development are inherently important to understand biofilms we wish to nurture or avoid in engineered reactors. Additionally, gaining a better understanding how bacteria regulate EPS production in mixed communities will be important for any improvements in design to be implemented. For some bacteria, their EPS production is directly linked with QS. For example, P. aeruginosa is known to produce three polysaccharides: alginate, Pel-polysaccharide, and Psl-polysaccharide; synthesis of both the Pel and Psl polysaccharides have QS dependence.83,84 Sinorhizobium meloti also produces two polysaccharides called EPS I and EPS II; production of EPS II and subsequent biofilm formation is controlled by AHL QS.85 Thus, it may be possible to affect EPS production and biofilm fouling by disrupting QS mechanisms in a directed manner. QS as a Target or Tool. Design of engineered reactors to promote certain conditions is standard practice. Currently this is accomplished with addition of chemicals, selective partitioning of a reactor, or manipulating reactor operation to achieve regions of oxygen depletion, desired pH, nutrient gradients, optimal growth conditions, etc. Promoting biofilm growth or detachment via QS mechanisms would likely employ similar strategies, where one might envision an addition of potassium (e.g., ref 59), sodium nitroprusside (SNP),86 or fatty acidcontaining waste (e.g., refs 87 and 88) to induce a desired biofilm adherence or release. Inhibiting the growth of certain biofilm-forming, “pioneer” species could also prevent biofouling.89 While laboratory studies have shown that QS disruption is possible, the above findings have yet to be employed in practice. In addition to the (NSM)-triggered potassium-leakage of B. subtilis described above,59 several other naturally occurring, QSdisrupting compounds have been identified. Several of these disruptors affect the interspecies AI-2 signal; it remains to be seen if these select examples are suited to disrupt AI-2 signaling 2000



Critical Review

dispersal from biofilms may significantly improve biofilm maintenance options as an alternative to antimicrobials that ultimately all promote growth of more resistant biofilms over time.

3) Continued research with mixed-culture systems is needed to document the effect of QS action(s) upon survival, growth, and function of species of relevance. Such work is likely to include both genomics and reductionist approaches to distinguish important species and actions on a temporal scale under the limited nutrient conditions observed in these treatment systems. Can biofilms in water treatment systems be controlled (or reduced) by adding more competition from soil or marine microbes?107−109 Can beneficial biofilms for wastewater treatment or bioremediation be enhanced and optimized by promoting the growth of QS bacteria or stimulating specific QS signaling pathways? There is a need to study cultures in batch and flow-through systems that combine enriched bacterial consortia with known QS-active species, enzymes, or molecular compounds. Additionally there will be a need to perform such experiments using specific materials; can biofilms forming on membranes or pipe material be disrupted given the surface attractive forces and local chemistry? 4) Bench and pilot-scale testing of QS-disruption strategies should be tested in pure-culture and mixed-culture systems. While some mechanisms that disrupt QS and/ or biofilm formation are now known for select species, it is not currently known how to apply this knowledge in mixed-culture systems on surfaces of engineering relevance. For example, can recently identified enzymatic and chemical biofilm dispersal strategies40,86,87,98,100,101 be applied broadly to mixed-cultures? Any potential QS-disruption strategy needs to work in practice and the mechanism needs to be understood. Industry is hungry for solutions to minimize fouling, minimize upsets, improve efficiency, and reduce maintenance costs.

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FUTURE RESEARCH NEEDS Consideration of the community-signaling aspects of bacterial biofilms that form in engineered systems has the potential to impact design and system operation. Biofouling of membranes with bacteria and associated EPS is among the top issues to be improved in membrane technology. When biological treatment is the goal, increased use of attached-growth treatment systems such as IFAS and MBBR can also be improved by design and maintenance of systems with robust, resilient biofilm communities. Such solutions are not a luxury but are critical for achieving the best design possible to meet our infrastructure needs. Improved understanding and potential exploitation of QS by engineers is an obvious intersection of fundamental science and engineering. While addressing QS within water technology systems is unlikely to fulfill a “silver bullet” role that solves all unanswered questions pertaining to biofilm growth, there is great potential to improve our current practices by considering QS-related functions. We know the application of singular chemical treatments differentially affects biofilms of distinct species;103 therefore, using a combined-approach of QS-related control with other measures may be the best solution. Clearly there are many research needs in this area that can be best answered by investigating QS important to water and wastewater bacteria in multiple ways. We propose these research needs include the following: 1) Pure-culture research using genetic isolation methods to identify the QS circuits and controlled processes of bacteria present in treatment systems; most research to date has addressed only a subset of the relevant bacterial species. While the QS mechanism(s) of “well-studied” systems continue to be investigated, there is a need to study the newly identified (or proposed) QS genes in the additional species relevant to these engineered systems. Multiple species of genera listed in Table 2 can be grown in pure culture, but few of these species have sequenced genomes and known protocols for bacterial genetic study. The limited library of sequence information will change dramatically in the next decade with the use of new pyro- and whole genome-sequencing technologies that will allow for description of whole genomes for multiple species (e.g., ref 104) Determination of the specific QS circuitry of these species will likely be more laborious to include genomic techniques and classical genetics approaches, which may require development of protocols for study of each specific organism. More immediately, experiments should be conducted with cocultures of known bacteria with more defined systems. Using an approach similar to An et al.,105 is it possible to isolate the effects of biofilm formation in defined cultures with 2−4 species? 2) There is a need to research the full capability of “quorum quenching”. Species such as Variovorax paradoxus that disrupt or degrade quorum sensing signal molecules have been identified.106 Can these populations be specifically nurtured in engineered systems to limit negative QSmediated actions (namely, biofilm formation)?

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AUTHOR INFORMATION

Corresponding Author

*Phone: 574-631-1726. E-mail: [email protected]. Address: University of Notre Dame, 156 Fitzpatrick Hall, Notre Dame, Indiana 46556, U.S.A. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was funded by the Department of Energy (DE SC0006642) to J.D.S. and the National Science Foundation (CBET-0954918) to R.N. Cover Art and Figure 2 were created by Matthew J. Sarna.

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