Critical Review pubs.acs.org/est
Transparent Exopolymer Particles: From Aquatic Environments and Engineered Systems to Membrane Biofouling Edo Bar-Zeev,*,† Uta Passow,‡ Santiago Romero-Vargas Castrillón,† and Menachem Elimelech† †
Department of Chemical and Environmental Engineering, Yale University, P. O. Box 208286, New Haven, Connecticut 06520, United States ‡ Marine Science Institute, University of California, Santa Barbara, California 93106, United States ABSTRACT: Transparent exopolymer particles (TEP) are ubiquitous in marine and freshwater environments. For the past two decades, the distribution and ecological roles of these polysaccharide microgels in aquatic systems were extensively investigated. More recent studies have implicated TEP as an active agent in biofilm formation and membrane fouling. Since biofouling is one of the main hurdles for efficient operation of membranebased technologies, there is a heightened interest in understanding the role of TEP in engineered water systems. In this review, we describe relevant TEP terminologies while critically discussing TEP biological origin, biochemical and physical characteristics, and occurrence and distributions in aquatic systems. Moreover, we examine the contribution of TEP to biofouling of various membrane technologies used in the desalination and water/wastewater treatment industry. Emphasis is given to the link between TEP physicochemical and biological properties and the underlying biofouling mechanisms. We highlight that thorough understanding of TEP dynamics in feedwater sources, pretreatment challenges, and biofouling mechanisms will lead to better management of fouling/biofouling in membrane technologies. Growing shortages of global freshwater supplies21,22 have stimulated a growth in the application of membranes for water purification systems.23,24 Examples of such technologies include desalination or advanced wastewater reuse by reverse osmosis (RO), pretreatment of feed waters with microfiltration (MF) or ultrafiltration (UF), and wastewater treatment by membrane bioreactors (MBR). These technologies use a wide spectrum of feedwater sources ranging from coastal, estuarine, and brackish aquifers to wastewater effluents, all with markedly different fouling propensities. In this article, we critically review the dynamic nature of TEP and their intricate interactions with bacterial communities in various aqueous systems, while attempting to bridge TEP terminologies used in the environmental/marine sciences and engineering communities. Concurrently, we identify and discuss key features of TEP that promote biofouling in various membrane systems. Finally, we assess current and future challenges in managing TEP at the growing membrane field.
1. INTRODUCTION Transparent exopolymer particles (TEP) are clear, gel-like polysaccharides that are ubiquitous in marine and freshwater environments, where they play diverse biochemical roles.1 TEP promote aggregate formation2,3 by providing the scaffold/matrix for marine or lake “snow”,3−6 thereby significantly impacting particle sedimentation processes in aquatic environments. TEP also serve as substrates for microbes that form protobiofilms, which consist of complex microbial communities embedded in TEP.7 Protobiofilms, similarly to marine snow, are likely to act as microbial hotspots,8,9 thus fueling the microbial loop and impacting food web structure by providing bacteria as a food source to zooplankton that feed on particles greater than ∼10 μm.10 In estuaries and coastal systems, TEP can also act as a vector for pathogens.11,12 Berman and Holenberg (2005) were first to suggest TEP as potential agents for membrane fouling in various engineered systems.13 Specifically, they proposed that during wastewater treatment or desalination TEP in feedwater form the initial conditioning film, thus enhancing biofilm formation and reinforcing biofilm structure. TEP readily adsorb to surfaces,7,14 such as membranes,15−17 and change their physicochemical properties by forming a hydrogel layer. To date, ample evidence has been accumulated on the role of TEP in biofilm formation and membrane biofouling.7,13−15,17−20 Hence, TEP might directly (by organic fouling) and indirectly (by expediting biofouling) reduce membrane performance, which results in a significant rise in the overall cost and energy use. © 2014 American Chemical Society
2. OVERVIEW OF TRANSPARENT EXOPOLYMER PARTICLES (TEP) TEP and Related Particles. Many types of microscale organic particles have been described in marine, freshwater, and other aqueous environments.25−29 The most extensively Received: Revised: Accepted: Published: 691
August 25, 2014 December 8, 2014 December 12, 2014 December 12, 2014 DOI: 10.1021/es5041738 Environ. Sci. Technol. 2015, 49, 691−707
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Figure 1. (A) Abiotic and (B) biotic pathways of TEP formation (TEP stained with Alcian blue). Abiotic TEP formation, which is presumably similar to self-assembled gel (SAG) formation, commences with organic fibrillar polymers (∼5−50 nm) that assemble to form colloidal nanogels (100−200 nm) by diffusion and electrostatic interaction. These nanogels could continue annealing by fibrillar tangles and Ca2+ bridging to form larger (0.4−300 μm) microgels. The abiotic pathway was in part adapted from ref 55 (copyright 2010 Elsevier). The biotic formation pathway is characterized by the direct shedding of mucus (0.4−300 μm) into the aquatic environment.1 Shown are three examples of microplanktonic organisms that directly secrete/shed TEP: diatom Nitzchia sp., the cyanobacteria Trichodesmium erythraeum, and heterotrophic bacteria. Nitzchia sp. and the heterotrophic bacteria (visualized with DAPI) were collected from the surface and at 250 m depth, respectively, of the Mediterranean Sea. Trichodesmium erythraeum was sampled from a monoculture.
of characterization, although the potential overlap between TEP and these different classes is often uncertain. TEP and their dissolved precursors exist along a size continuum (Figure 1), ranging from dissolved fibrillar polymers, hereafter termed as TEP precursors (5−400 nm), to gelatinous sheets and/or cobweb-like networks (0.4−300 μm), defined hereafter as TEP.46,48 The dissolved organic fraction and nanometer-scale colloidal gels47,53,54 might be considered as precursors to TEP, yet this has not been unambiguously shown.29,55 Recently, extracellular Alcian blue stainable material in water has been further specified as particulate TEP (pTEP, particle size > 0.4 μm) and colloidal TEP (cTEP, 0.05 μm < particle size < 0.4 μm) in the membrane field.15,16 As defined earlier, cTEP might, in part, be classified as TEP precursors, thus potentially forming larger particles spontaneously. Differentiation between Sessile EPS and Planktonic TEP. The term EPS is very broad and refers to any extracellular dissolved organic matter (DOM) released by prokaryotes or eukaryotes.49,56−58 The released material usually includes a mixture of polysaccharides, proteins, lipids, and nucleic acids.49,58−61 Divalent cations (mainly Ca2+) initiate multiple cross-links between the dissolved polysaccharide chains to form the semistable gelatinous network characteristic of EPS.58,59,62,63 Hydrophobic interactions, which drive the spontaneous association of apolar hydrophobic solutes in water,64 may also be involved in the formation of these gels.46,54 The term EPS is frequently ascribed to sessile microbial biofilms.56,61,65,66 In that context, EPS is defined as a self-produced, biopolymeric network that provides the three-dimensional (3-D) architecture.56,58 The main role of biofilm EPS is to provide cell-to-cell scaffolding, while securing irreversible attachment of the entire consortium to the surface as “bio-anchorage”.56,58,61,66
studied type of nonliving, planktonic particles are transparent exopolymer particles.1,4,27,30,31 The term TEP was first coined two decades ago by Alldredge et al. in 1993 to describe pelagic transparent exopolymer particles (0.4 μm to hundreds of micrometers) that stain with acidic Alcian blue (AB).27,32 TEP were defined operationally as pelagic, acidic polysaccharide particles (retained on 0.4 μm filters) that are made visible with AB stain.27 Accordingly, the term TEP does not define these particles based on their source or chemical composition but rather their staining capacity by low pH, AB solution.33 TEP originate from extracellular polysaccharides released by various organisms, such as planktonic bacteria,34,35 microalgae,31,34,36−39 benthic macroalgae,40,41 bivalves,42 coral reefs, and other benthic suspension feeders.43,44 However, while attached to organisms as envelopes or capsules, AB stained material is not considered as TEP, and hence may introduce a bias when detected by various spectrometric methods. Moreover, it was shown that intact phytoplankton colonies (such as Chaetoceros socialis and Phaeocystis spp.) do not stain as TEP, but colony disintegration results in detectable TEP formation.45 TEP can be also recognized as hydrogels since they share several key features with marine gels. Specifically, TEP (i) are composed mainly of acidic polysaccharides,27 (ii) disperse in the presence of different chelators,27,46,47 (iii) pass through 0.2 μm filters,15,33 and (iv) spontaneously reassemble.1,29,48 As free-floating particles, TEP are considered a subgroup of “extracellular polymeric substances” (EPS).49,50 Additional subclasses of EPS/hydrogels such “self-assembled gels (SAG)”,47 “biopolymer clusters (BPC)”,51 and “soluble microbial products (SMP)”52 have been recently named depending on the method 692
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*
Should be measured in liquid to avoid gel deformation.
of data from different AB batches. Hence, the units describing TEP concentrations are often expressed as GX equivalents. It was further highlighted that, in the presence of salt, TEP precursors could only be quantified after dialysis.67 However, in freshwater samples TEP and TEP precursors may be determined jointly by direct addition of the dye to the sample, although the method is less sensitive.68 Other colorimetric and microscopic techniques have been developed since (Table 1), with further details reviewed by Discart et al.69 Because the chemical composition of TEP is unknown, all of the methods developed to date are only semiquantitative; the amount of AB bound per carbon depends on the number of binding sites per carbon content. Hence, to estimate the carbon content in TEP, various conversion factors from TEP to carbon have been empirically determined using different monocultures.30,70 However, conversion factors for natural samples have yet to be developed. From Extracellular Release to TEP Formation. TEP form either abiotically from dissolved TEP precursors29,48,55,71 or via biotic pathways.34,38,72−74 Abiotic formation constitutes the predominant pathway for TEP formation and is thought to result in the formation of “physical gels”, presumably in a similar fashion as self-assembled gels (SAG).29 These are polymer networks embedded in an aqueous solvent. These newly formed gels are characterized by weak hydrophobic and ion bridging interactions, and can easily tangle, assemble, and disperse.29,55 The less common, biotic pathway usually leads to “chemical gels”, which are characterized by covalently crosslinked, irreversibly attached biopolymers.29,72 It is suggested that the abiotic pathway (Figure 1A) commences with the release of dissolved fibrillar polysaccharides from various planktonic organisms as extracellular release,34,74−76 as well as lysis and/or breakage of cells through viral infections.29,34,48,55,71 A hitherto unknown fraction of these fibrillar polymers are TEP precursors, a few to tens ( τ the chains disentangle. The relaxation time depends principally on the third power of the molecular weight, N, as τ ∼ N3.82 Longer polymer chains have a higher probability of establishing networkforming contacts, while shorter polymers engage in fewer such contacts and face a smaller energetic barrier for disentanglement and diffusion.29 Colloidal TEP precursors might interlock through axial reptational diffusion and anneal to form microgels and eventually larger (few to hundred micrometers) TEP.29,34,71,83 Hydrogels are dynamic entities and hence undergo reversible conformational transitions between the different precursors and microgels in short time scales (hours to few days) to reach an assembly/dispersion equilibrium.29,46,55 However, high concentrations and molecular attributes (Table 2) including polymer charge density, gel architecture, flexibility, and polymer chain
3. TEP PHYSICOCHEMICAL PROPERTIES RELEVANT TO BIOFOULING TEP Sticky Character. TEP sticky properties have been previously studied in various environmental1,31,85,86 and biofouling7,13,15,17,20,87 contexts. Based on the constituents of the bacterial cell wall and polysaccharide extracellular coating, the physicochemical interactions driving bacterial attachment to TEP are likely to be the same as those that result in TEP selfassembly. The cell wall of Gram-positive bacteria comprises a thick (up to 80 nm), cross-linked peptidoglycan (murein) layer, with embedded teichoic acids. Gram-negative bacteria are usually covered by a thin (∼10 nm) peptidoglycan layer with an additional outer envelope composed of mainly phospholipids and lipopolysaccharides.88 Thus, the surfaces of most bacteria are rich in amphiphilic moieties that can participate in hydrophobic interactions, hydroxyl and amine groups that form hydrogen bonds, and carboxylates than can engage in bridging interactions mediated by divalent ions such as Ca2+. Physicochemical Forces of Bacterial Attachment. A common first approach to understand bacteria−surface interactions regards bacterial cells as negatively charged, hydrophobic particles. For such simple systems, the theory due to Derjaguin, Landau, Verwey, and Overbeek (DLVO) can provide quantitative description of particle−particle and particle− surface interactions. DLVO theory describes the free energy of 694
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and surface charge), and the hydrodynamic conditions (initial permeate flux and cross-flow velocity) in the membrane module.107,108 As a first approximation, macromolecule−surface interactions can be described by an extended DLVO theory accounting for Lifshitz−van der Waals, electrostatic double layer, and acid−base interactions combined with permeation drag forces.109−111 Given the relative hydrophobicity of membrane materials, such as polyamide,23 hydrophobic interactions also bolster macromolecule adsorption on the membrane surface. The nanoscale roughness of thin-film composite (TFC) membranes for seawater desalination and wastewater reclamation, with RMS roughness ∼100−200 nm,23 has been shown to increase the fouling propensity by lowering the energetic barrier for particle deposition.109 Membrane surface charge also plays a key role in membrane fouling. Thin-film composite RO and NF membranes are amphoteric, exhibiting a positive ζ potential (or surface charge) at low pH, an isoelectric point at pH 3−5, and negative ζ potential at near-neutral and basic pH due to deprotonation of surface carboxylic acid groups.108,112 At near-neutral pH, characteristic of natural waters and wastewaters, RO and NF membrane surfaces are thus negatively charged. Similar to the intermolecular TEP interactions, the ubiquitous Ca2+ ion bolsters the adsorption of carboxylate-rich polysaccharides on the membrane surface through the formation of calcium bridges with the membrane surface carboxylic groups.60,113 The adsorption of polysaccharides (likely also TEP) on the membrane surface forms a gel layer that drastically alters the membrane surface characteristics108,112,114,115 and hence may change the membrane fouling propensity.
adhesion of a colloidal particle to an extended solid surface as the sum of van der Waals and electrostatic double-layer interactions.89,90 However, in reality bacterial attachment is more complex. Short-range phenomena, such as hydrogen bonding and hydrophobic interactions, which act at cell−surface separations less than ∼5−10 nm,91 need to be explicitly accounted for. The standard DLVO theory has been supplemented to include contributions arising from Born repulsion,92 electron donor− electron acceptor interactions,93,94 and steric interactions between surfaces containing grafted polymers.95 These theories have only been marginally successful in describing bacterial interactions with model hydrophobic and hydrophilic surfaces96 and polymeric membrane surfaces.97 The description of the electrostatic double-layer interaction of bacterial cells also requires additional considerations beyond DLVO theory. The biopolymers on the outer cell wall constitute a “soft”, charged, ion-permeable layer; hence, electrokinetic theories using the ζ potential to approximate the surface potential are inadequate for bacteria, because they regard cells as rigid and ion-impenetrable.98 The electrokinetic theory by Ohshima99 considers a spherical particle coated with an ionpermeable polyelectrolyte layer, and therefore provides a closer approximation of the charging behavior of bacterial cells.98 Electrostatic surface potentials calculated using the theory by Ohshima have been used in conjunction with DLVO theory to determine the interactions between bacteria and quartz surfaces.98 For bacteria−surface interactions, the presence of macromolecules, polyelectrolytes, and their aggregates, such as TEP and TEP precursors, may bolster bacterial attachment. This is commonly referred to as a conditioning film,7,100−102 which significantly affects the roughness, hydrophobicity, and charge of the interface7,17,103 and typically promotes bacterial adhesion. However, studies reporting antagonistic effects of the conditioning film have also been reported, and it is unclear whether a conditioning film bolsters bacterial attachment when it occurs concurrently with other fouling processes, such as organic fouling or scaling.104 Recent work has focused on the effect of surface conditioning on bacterial adhesion using adsorbed layers of alginate (as polysaccharide substance) and other components such as humic substances and proteins.103,105 The results have shown that bacterial adhesion rate depends on factors such as solution chemistry, principally ionic strength and composition, which regulates the viscoelastic properties and structure of the conditioning film.62,103 The effect of surface conditioning with polysaccharides on bacterial adhesion to RO membranes showed that cell surface abundance was two orders of magnitude higher in conditioned membrane surfaces compared to nonconditioned.104,106 While the conditioning film is generally thought to promote bacterial adhesion and membrane biofouling, the general synergies between the conditioning film and long-term biofouling remain to be clarified.104 Interactions of TEP with Membrane Surfaces. TEP and TEP precursors are present in the feedwater of most desalination and wastewater treatment facilities at varying concentrations, depending on the pretreatment technology used (Table 3). The factors governing the adsorption of organic molecules, such as TEP and TEP precursors, on membrane surfaces are macromolecule−surface interactions. These associations are determined by the water chemistry (pH, ionic strength, and concentration of divalent cations), membrane physicochemical properties (nanoscale roughness, hydrophobicity,
4. UBIQUITY OF TEP IN FEEDWATERS FOR MEMBRANE SYSTEMS Since first described, the ubiquity of TEP in marine and freshwater ecosystems has been extensively documented.1 TEP concentrations are spatially, temporally, and species-dependent, thus highly variable across the aqueous environment, ranging from micrograms to a few milligrams GX equivalent per liter (Table 3). Open ocean ecosystems tend to be less productive than coastal systems. Correspondingly, TEP concentrations usually range between a few micrograms to 1 mg of GX equiv L−1 and follow phytoplankton−bacterial dynamics as indicated by chlorophyll a (Chl a) as algal proxy.34,35,38,116−118 Coastal waters and estuaries are exposed to larger environmental changes compared to open ocean systems and are drastically influenced by various physiochemical parameters as well as anthropogenic eutrophication due to runoff or river input.119,120 Nutrient-rich coastal ecosystems (excluding lightlimited regions) result in phytoplankton blooms followed by abrupt demise.121−124 These blooms fuel intense microbial activity.125−127 Additionally, large-scale jellyfish swarms periodically accumulate in near-shore environments and might also enhance microbial activity by extensive organic matter release.128 TEP concentrations are tightly linked to these various changes, resulting in large variations (Table 3). Extreme mucilage events such as large (meters long) underwater gelatinous clouds129,130 and massive foam-like matter131−133 occasionally appear in costal environments concurrently with abrupt phytoplankton blooms resulting in distinct polysaccharide signature. Although localized, in such events TEP concentrations were observed to reach up to 15 mg of GX equiv L−1.130 Feedwater sources for RO desalination are usually pumped from estuary and/or coastal environments. Intake pipes are 695
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Table 3. TEP Concentrations in Different Ecosystems and Engineered Systems (unless Specified Otherwise, All Concentrations Refer to TEP)a
a Pretreatment prior to reverse osmosis desalination: rapid sand filtration (RSF), cartridge filters (CF), reverse osmosis membrane (RO), microfiltration (MF), ultrafiltration (UF), and in-line coagulation (IC). Feedwater origin: (#) seawater, ($) estuary, and (‡) wastewater secondary effluent (sec. eff.). NA, data were not available. Removal efficiencies (%) were calculated by regarding the feedwater as 100%.
between 10 and 100 mg of GX equiv L−1 in untreated municipal wastewater and up to 4 mg of GX equiv L−1 in secondary effluents (Table 3). Currently, the sources of TEP in these effluents are unclear. However, similarly to the aquatic environment, TEP could be generated through abiotic assembly of precursors and/or via microbial mediated release of mucosal matter.20,139
often located around 1 km from the shore and a few meters beneath the surface.134,135 Hence, spatial and annual variations in TEP concentrations, in the overall size spectrum, and in the ratio between TEP precursors and TEP in near-shore environments will be reflected in the desalination facility feedwater and, consequently, at the RO stage inlet.14,15,136 Currently, various pretreatment configurations, such as granular (sand) filtration or UF/MF, are located upstream of the RO stage to improve the quality of water passing through the RO modules and improve the system performance over time. Wastewater purification through MBR is becoming increasingly popular, since they result in effluents with low TOC and total suspended solids (TSS) concentration.137 However, high organic loadings at the MBR feedwater are one of the main hurdles for this approach.20,137,138 TEP concentrations can range
5. TEP FOULING PROPENSITY IN MEMBRANE PROCESSES Emergence of TEP as Active Agents in MembraneBased Technologies. Reverse osmosis desalination and wastewater reuse represent key technologies for sustainable global water supply. RO currently comprises over 63.7% (>41 million m3 d−1) of the global desalination industry.140−143 In RO desalination, hydraulic pressure drives permeation of 696
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Figure 2. Superimposing (illustrative) “classic” biofilm pathway65 emphasizing the contribution of TEP species in the revised biofilm development paradigm. (A) Nanocolloidal TEP precursors as conditioning film were imaged using in situ atomic force microscopy (AFM). The z-scale in the inset is 33 nm. (B) TEP sheets or comb-like matter were visualized after staining with Alcian blue (blue) with bright-field microscopy. (C) Floating protobiofilm micrographs (as complex microbial shuttles) were taken in situ with bright-field and epifluorescence microscopy after staining bacteria with SYTO 9 (green) and TEP with Alcian blue (blue). Note, Alcian blue stain may have partly precipitated due to the saline character of the seawater, hence causing some bias and deformation of the microgel morphology. Protobiofilms’ 3-D micrographs were taken using in situ confocal laser scanning microscope (CLSM) after double staining the sample with concanvalin A (blue) and SYTO 9 (bacteria, green). For further details see Bar-Zeev et al.7
(stage i, Figure 2) organic polymers and colloids present in water adhere to the surface, forming a nanometer-thin “conditioning film” composed of polysaccharides, proteins, lipids, nucleic acids, and humic and fulvic acids.7,100,153,154 Bacterial cells in the overlying water undergo reversible attachment to this conditioning layer via van der Waals, hydrophobic, and hydrogen bonding interactions that overcome electrostatic repulsive forces (stage ii).88,155 In this stage, bacteria attachment is reversible and can easily be removed by application of mild shear forces.104,156 After a few hours, most of the bacteria become irreversibly attached to the surface by self-produced EPS secretions (stage iii); the polysaccharides in the EPS interact with the surface through hydrophobic interactions, strong dipole−dipole forces, and hydrogen bonding.88,156 Hours to days later (stages iv and v), bacterial proliferation and constant EPS secretion result in an organized, multilayered mature biofilm structure.65,157 Recently, Bar-Zeev et al. proposed a revised paradigm for accelerated aquatic biofilm formation that takes into account the roles of TEP precursors, TEP, and protobiofilms.7 This paradigm occurs in tandem with the currently accepted stage-wise process and is likely to have considerable implications for membrane-based technologies. Immediately upon surface exposure to any aqueous system, TEP precursors (Figure 2A) will adsorb to the surface, resulting in a thin (∼5−100 nm), negatively charged and patchy conditioning layer.7,102,105,154 The morphology of the thin-film conditioning layer, as observed with atomic force microscopy, is
water across a selective membrane. Since their introduction over 30 years ago, TFC polyamide membranes have become the standard of the RO desalination industry.23,144 Nonetheless, owing the physicochemical properties of the polyamide selective layer (i.e., roughness, hydrophobicity, and surface charge), thin-film composite membranes are prone to organic and bio-fouling, requiring extensive pretreatment that increases the energy use and cost of the process.23,135,140 Pretreatment is implemented upstream to reduce fouling, maintain membrane selectivity and flux, and hence extend membrane lifetime.23,135 Concurrently, growing interest in wastewater (WW) reuse as a source of renewable water for industry, agriculture, and even fresh drinking water145 has pushed this ancient process (1700 BC) to 21st century membrane technology.146 The traditional activated sludge bioreactors are now combined with membranes (typically UF) to form new hybridized membrane bioreactors, MBRs.147,148 However, similarly to RO, one of the main technological obstacles for MBR technology is membrane fouling.137 Berman was the first to point out that TEP might act as a potential agent in biofilm formation, highlighting the possible negative implications for the water sector.13,18 Since then the role of TEP was discussed in expediting biofilm formation,7,14 as well as TEP’s possible effects on membrane properties and performance.15,17,20,149−151 TEP Contribution to Biofilm Formation. The traditional, classic concept of biofilm formation follows a complex pathway involving several sequential stages (Figure 2).56,65,152 Initially 697
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Figure 3. Measured TEP and chlorophyll a (Chl a) concentrations with corresponding removal percentage by traditional pretreatment from two large-scale desalination facilities located on the Israeli coastline. Samples were collected from (A) the desalination facility feedwater, (B) the rapid sand filter (RSF) effluent, and (C) cartridge filter filtrate (CF; nominal pore size of ∼15 μm) prior to the reverse osmosis (RO) module. Removal efficiencies (%) were calculated by regarding the feedwater as a 100%. Data were modified from refs 14, 164, and 180, while averages and their standard deviations were calculated from samples (n) collected over 3 years.
characterized by rough bubble and/or fiber-like structures.7,46,154 Despite being negatively charged, these organic films significantly increase bacterial attachment by hydrophobic interactions and hydrogen bonding with overlying cell flagellates of planktonic bacteria.103,105 Concurrently (Figure 2B), highly sticky (i.e., characterized by adhesive forces up to 8.5 nN determined by AFM), carbon-rich, thick (up to 250 nm) microgel-TEP patches attach and cover extremely large (up to 1 mm2) surfaces.7,14 Once adsorbed to a surface, TEP become part of the EPS layer that mediates bacterial attachment and reinforces the biofilm structure (Figure 2). A detailed study showed that TEP attach to pristine glass slides forming the first conditioning layer.14 It was proposed that in the early stages (minutes to hours) of biofilm development, most of captured “EPS” areas originate from TEP present in the feedwater.14 This EPS (formerly TEP) layer significantly increases the elasticity, roughness, and organic content of the surface, resulting in a favorable substrate for the attachment of bacteria and additional microgel particles.7 Following attachment, these organic TEP-like fouling layers were also shown to reduce the performance of different types of membranes, such as UF17,20 and RO.154,158,159 The term “protobiofilm” has recently been proposed to designate free-floating, marine microgel clusters with extensive microbial outgrowth.7 This planktonic microbial consortium is firmly attached to AB-stainable organic polymers and exhibits a wide range of particle sizes, from several μm2 to more than 1 mm2 in upper surface area (Figure 2). Protobiofilms display most of the characteristics of early biofilm development, with the exception of being attached to a fixed surface. It was suggested that within the confines of these heavily colonized microgel particles, diffusion of signaling molecules released by prokaryote cells should be greatly restricted, thereby enhancing the efficiency of quorum sensing and other forms of microbial communication.160 Although only documented in coastal ecosystems, it is likely that protobiofilms will also be present in various marine and freshwater systems. Fundamental questions regarding protobiofilms still remain: (i) What are the genetic fingerprints of the bacterial species that form these planktonic colonies? (ii) Will bacteria follow the classical biofilm formation paradigm aboard these gel-like platforms? (iii) Does quorum sensing play any role in the congregation of these consortiums? (iv) Which
bacterial species that comprise the protobiofilm consortium flourish as biofilm once attached to a surface? Protobiofilms can also adhere to various, immersed surfaces (Figure 2C), simultaneously with TEP precursors and TEP, to instantly form large (up to 210 μm thick) primary biofilm colonies.7 The 3-D complexity of these attached protobiofilms has all of the characteristics of mature biofilms, namely, large bacterial clusters separated by channel-like structures and encapsulated in a polysaccharide matrix. Adsorption of these “prefabricated” floating consortiums bridge over the reversible cell attachment phase, while forming a nutrient-rich substratum.7 Once attached (∼30 min), protobiofilms were reported to exhibit up to a 12.8-fold increase in biovolume than prefiltered samples (excluding protobiofilms), resulting in expedited biofilm development.7 Protobiofilms, unless removed by the pretreatment stage, might have serious implications for membrane biofouling. Removal of TEP and TEP precursors in Pretreatment Systems for Seawater Desalination. All reverse osmosis desalination facilities pretreat the feedwater to minimize fouling and biofouling.23,135,140 In most large-scale desalination facilities, pretreatment systems are based on conventional coagulation/ flocculation steps, followed by rapid sand filtration (RSF) and cartridge filtration (CF).140,161,162 Chemically induced coagulation and flocculation prior to the RSF are used to destabilize and aggregate suspended and colloidal particles. RSF are granular filtration systems with flow rates (approach velocities) ranging between 5 and 30 m h−1.135 This technology is designed to remove suspended and fine colloidal particles by physicochemical filtration.89,135 Backwashing is a common procedure to clean the granular media for a subsequent filtration run. CF units with nominal pore sizes of 1−20 μm are commonly installed downstream of the RSF to minimize particle concentration at the RO feed.134 These dead-end filters usually have a plate or mesh design and operate in a bundle of pressurized (
