Skip to main content
SpringerLink
Log in

Role of extracellular polymeric substances (EPS) production in bioaggregation: application to wastewater treatment

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

This paper reviews the formation, structure, and stability of bioaggregates with an emphasis on the composition and distribution of extracellular polymeric substances (EPS) and their role in bioaggregation. Bioaggregation is ubiquitous in natural environment and is of great importance in biological wastewater treatment processes. It greatly influences the flocculability, settleability, and dewaterability for flocs and sludge retention and shear resistance for biofilms. The physico-chemical and microbial structures of bioaggregates are dependent on operational conditions as well as microbial diversity and spatial distribution. The formation of bioaggregates is mediated by the physico-chemical interactions as well as the microbial interactions such as EPS production and quorum sensing. EPS are composed of a mixture of macromolecules including proteins, polysaccharides, humic-like substances, and nucleic acids, which entrap the microbial cells in a three-dimensional matrix. The composition and physico-chemical characteristics of EPS have significant influence on the maintenance of the bioaggregate structure and the process performance of the wastewater treatment. However, the mechanisms of bioaggregation are still unclear and the conclusions on the role of EPS were mostly drawn from the established correlations and hypotheses. This paper expects to provide up-to-date knowledge on bioaggregation and insights for further studies and applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ab Halim MH, Nor Anuar A, Azmi SI, Jamal NSA, Wahab NA, Ujang Z, Shraim A, Bob MM (2015) Aerobic sludge granulation at high temperatures for domestic wastewater treatment. Bioresour technol 185:445–9

    Article  CAS  PubMed  Google Scholar 

  • Adav SS, Lee DJ, Tay JH (2008a) Extracellular polymeric substances and structural stability of aerobic granule. Water Res 42(6–7):1644–1650

    Article  CAS  PubMed  Google Scholar 

  • Adav SS, Lee DJ, Show KY, Tay JH (2008b) Aerobic granular sludge: recent advances. Biotechnol Adv 26(5):411–423

    Article  CAS  PubMed  Google Scholar 

  • Albertsen M, Stensballe A, Nielsen KL, Nielsen PH (2013) Digging into the extracellular matrix of a complex microbial community using a combined metagenomic and metaproteomic approach. Water Sci Technol 67(7):1650–1656

    Article  CAS  PubMed  Google Scholar 

  • Almstrand R, Persson F, Daims H, Ekenberg M, Christensson M, Wilen BM, Sorensson F, Hermansson M (2014) Three-dimensional stratification of bacterial biofilm populations in a moving bed biofilm reactor for nitritation-anammox. Int J Mol Sci 15(2):2191–2206

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Badireddy AR, Chellam S, Gassman PL, Engelhard MH, Lea AS, Rosso KM (2010) Role of extracellular polymeric substances in bioflocculation of activated sludge microorganisms under glucose-controlled conditions. Water Res 44(15):4505–4516

    Article  CAS  PubMed  Google Scholar 

  • Barr JJ, Cook AE, Bond PL (2010) Granule formation mechanisms within an aerobic wastewater system for phosphorus removal. Appl Environ Microbiol 76(22):7588–7597

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Batstone DJ, Keller J (2001) Variation of bulk properties of anaerobic granules with wastewater type. Water Res 35(7):1723–1729

    Article  CAS  PubMed  Google Scholar 

  • Beun JJ, Hendriks A, Van Loosdrecht MCM, Morgenroth E, Wilderer PA, Heijnen JJ (1999) Aerobic granulation in a sequencing batch reactor. Water Res 33(10):2283–2290

    Article  CAS  Google Scholar 

  • Boelee NC, Janssen M, Temmink H, Taparaviciute L, Khiewwijit R, Janoska A, Buisman CJN, Wijffels RH (2014) The effect of harvesting on biomass production and nutrient removal in phototrophic biofilm reactors for effluent polishing. J Appl Phycol 26(3):1439–1452

    Article  CAS  Google Scholar 

  • Bossier P, Verstraete W (1996) Triggers for microbial aggregation in activated sludge? Appl Microbiol Biotechnol 45(1–2):1–6

    Article  CAS  Google Scholar 

  • Bourven I, Simon S, Guibaud G (2013) Influence of extraction method on size exclusion chromatography fingerprints of EPS from wastewater sludges. Environ Technol (United Kingdom) 34(3):321–332

    CAS  Google Scholar 

  • Bourven I, Bachellerie G, Costa G, Guibaud G (2015) Evidence of glycoproteins and sulphated proteoglycan-like presence in extracellular polymeric substance from anaerobic granular sludge. Environ Technol 36(19):2428–2435

    Article  CAS  PubMed  Google Scholar 

  • Caudan C, Filali A, Sperandio M, Girbal-Neuhauser E (2014) Multiple EPS interactions involved in the cohesion and structure of aerobic granules. Chemosphere 117:262–270

    Article  PubMed  CAS  Google Scholar 

  • Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, Normark S, Hultgren SJ (2002) Role of Escherichia Coli curli operons in directing amyloid fiber formation. Science 295(5556):851–855

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen MY, Lee DJ, Tay JH (2007) Distribution of extracellular polymeric substances in aerobic granules. Appl Microbiol Biotechnol 73(6):1463–1469

    Article  CAS  PubMed  Google Scholar 

  • D’Abzac P, Bordas F, Van Hullebusch E, Lens PNL, Guibaud G (2010) Extraction of extracellular polymeric substances (EPS) from anaerobic granular sludges: comparison of chemical and physical extraction protocols. Appl Microbiol Biotechnol 85(5):1589–1599

    Article  PubMed  CAS  Google Scholar 

  • deBeer D, Oflaharty V, Thaveesri J, Lens P, Verstraete W (1996) Distribution of extracellular polysaccharides and flotation of anaerobic sludge. Appl Microbiol Biotechnol 46(2):197–201

    Article  CAS  Google Scholar 

  • Ding Z, Caliendo L, Panico A, Esposito G, van Hullebusch ED, Pirozzi F (2015) An innovative approach to remove nitrogen from wastewater using a biological anaerobic ammonium oxidation (anammox) process. Chem Eng Trans 43:2245–2250

    Google Scholar 

  • Doelle HW (1994) Microbial process development. World Scientific, Singapore

  • Dolfing J, Griffioen A, Vanneerven ARW, Zevenhuizen L (1985) Chemical and bacteriological composition of granular methanogenic sludge. Can J Microbiol 31(8):744–750

    Article  CAS  Google Scholar 

  • Felfoeldi T, Jurecska L, Vajna B, Barkacs K, Makk J, Cebe G, Szabo A, Zaray G, Marialigeti K (2015) Texture and type of polymer fiber carrier determine bacterial colonization and biofilm properties in wastewater treatment. Chem Eng J 264:824–834

    Article  CAS  Google Scholar 

  • Feng Q, Xue ZX, Chen LN, Li HY Effect of aeration induced shear stress on the settleability and activity of activated sludge. In: 3rd International conference on bioinformatics and biomedical engineering, iCBBE 2009, 2009.

  • Feng L, Wu Z, Yu X (2013) Quorum sensing in water and wastewater treatment biofilms. J Environ Biol 34(2):437–444

    CAS  PubMed  Google Scholar 

  • Ferrera I, Mas J, Taberna E, Sanz J, Sanchez O (2015) Biological support media influence the bacterial biofouling community in reverse osmosis water reclamation demonstration plants. Biofouling 31(2):173–180

    Article  PubMed  Google Scholar 

  • Frolund B, Palmgren R, Keiding K, Nielsen PH (1996) Extraction of extracellular polymers from activated sludge using a cation exchange resin. Water Res 30(8):1749–1758

    Article  Google Scholar 

  • Gao JF, Zhang Q, Wang JH, Wu XL, Wang SY, Peng YZ (2011) Contributions of functional groups and extracellular polymeric substances on the biosorption of dyes by aerobic granules. Bioresour Technol 102(2):805–813

    Article  CAS  PubMed  Google Scholar 

  • Garnier C, Görner T, Lartiges BS, Abdelouhab S, De Donato P (2005) Characterization of activated sludge exopolymers from various origins: a combined size-exclusion chromatography and infrared microscopy study. Water Res 39(13):3044–3054

    Article  CAS  PubMed  Google Scholar 

  • Ge L, Wang H, Ma L, Deng H (2006) Extraction of extracellular polymeric substances (EPS) from four kinds of activated sludge. Fresenius Environ Bull 15(10):1252–1255

    CAS  Google Scholar 

  • Gonzalez-Gil G, Holliger C (2014) Aerobic granules: microbial landscape and architecture, stages, and practical implications. Appl Environ Microbiol 80(11):3433–3441

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gonzalez-Gil G, Lens PNL, Van Aelst A, Van As H, Versprille AI, Lettinga G (2001) Cluster structure of anaerobic aggregates of an expanded granular sludge bed reactor. Appl Environ Microbiol 67(8):3683–3692

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gonzalez-Gil G, Sougrat R, Behzad AR, Lens PNL, Saikaly PE (2015) Microbial community composition and ultrastructure of granules from a full-scale anammox reactor. Microb Ecol 70(1):118–131

    Article  CAS  PubMed  Google Scholar 

  • Gorner T, de Donato P, Ameil MH, Montarges-Pelletier E, Lartiges BS (2003) Activated sludge exopolymers: separation and identification using size exclusion chromatography and infrared micro-spectroscopy. Water Res 37(10):2388–2393

    Article  CAS  PubMed  Google Scholar 

  • Gregory J (1997) The density of particle aggregates. Water Sci Technol 36(4):1–13

    Article  CAS  Google Scholar 

  • Guibaud G, van Hullebusch E, Bordas F (2006) Lead and cadmium biosorption by extracellular polymeric substances (EPS) extracted from activated sludges: pH-sorption edge tests and mathematical equilibrium modelling. Chemosphere 64(11):1955–1962

    Article  CAS  PubMed  Google Scholar 

  • Guibaud G, Bhatia D, d’Abzac P, Bourven I, Bordas F, van Hullebusch ED, Lens PNL (2012) Cd(II) and Pb(II) sorption by extracellular polymeric substances (EPS) extracted from anaerobic granular biofilms: evidence of a pH sorption-edge. J Taiwan Inst Chem E 43(3):444–449

    Article  CAS  Google Scholar 

  • Guo J, Peng Y, Wang S, Yang X, Yuan Z (2014) Filamentous and non-filamentous bulking of activated sludge encountered under nutrients limitation or deficiency conditions. Chem Eng J 255:453–461

    Article  CAS  Google Scholar 

  • Han Y, Liu J, Guo X, Li L (2012) Micro-environment characteristics and microbial communities in activated sludge flocs of different particle size. Bioresour Technol 124:252–258

    Article  CAS  PubMed  Google Scholar 

  • He YW, Zhang LH (2008) Quorum sensing and virulence regulation in Xanthomonas campestris. FEMS Microbiol Rev 32(5):842–857

    Article  CAS  PubMed  Google Scholar 

  • Hermansson M (1999) The DLVO theory in microbial adhesion. Colloid and Surface B 14(1–4):105–119

    Article  CAS  Google Scholar 

  • Higgins MJ, Novak JT (1997) Characterization of exocellular protein and its role in bioflocculation. J Environ Eng-Asce 123(5):479–485

    Article  CAS  Google Scholar 

  • Higgins MJ, Sobeck DC, Owens SJ, Szabo LM (2004a) Case study II: application of the divalent cation bridging theory to improve biofloc properties and industrial activated sludge system performance - using alternatives to sodium-based chemicals. Water Environ Res 76(4):353–359

    Article  CAS  PubMed  Google Scholar 

  • Higgins MJ, Tom LA, Sobeck DC (2004b) Case study I: application of the divalent cation bridging theory to improve biofloc properties and industrial activated sludge system performance - direct addition of divalent cations. Water Environ Res 76(4):344–352

    Article  CAS  PubMed  Google Scholar 

  • Hoa PT, Nair L, Visvanathan C (2003) The effect of nutrients on extracellular polymeric substance production and its influence on sludge properties. Water SA 29(4):437–442

    CAS  Google Scholar 

  • Hou X, Liu S, Zhang Z (2015) Role of extracellular polymeric substance in determining the high aggregation ability of anammox sludge. Water Res 75:51–62

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Wen Y, Cao A, Li H, Zhou Q (2012) The influence of temperature on bioflocculation and settling of activated sludge and their flocculation mechanisms involved. In: Iranpour R, Zhao J, Wang A, Yang FL, Li X (eds) Advances in environmental science and engineering, pts 1–6, vol 518–523, Adv Mater Res., pp 1817–1824

    Google Scholar 

  • Hulshoff Pol LW, de Castro Lopes SI, Lettinga G, Lens PNL (2004) Anaerobic sludge granulation. Water Res 38(6):1376–89

    Article  CAS  PubMed  Google Scholar 

  • Ivanov V, Nejad SR, Yi S, Wang XH (2008) Physiological heterogeneity of suspended microbial aggregates. Water Sci Technol 58(12):2435–2441

    Article  PubMed  Google Scholar 

  • Jiang W, Xia S, Duan L, Hermanowicz SW (2015) Biofilm architecture in a novel pressurized biofilm reactor. Biofouling 31(4):321–331

    Article  CAS  PubMed  Google Scholar 

  • Johnson CP, Li XY, Logan BE (1996) Settling velocities of fractal aggregates. Environ Sci Technol 30(6):1911–1918

    Article  CAS  Google Scholar 

  • Kalyuzhnyi S, De Los Santos LE, Martinez JR (1998) Anaerobic treatment of raw and preclarified potato-maize wastewaters in a UASB reactor. Bioresour Technol 66(3):195–199

    Article  CAS  Google Scholar 

  • Karadag D, Koroglu OE, Ozkaya B, Cakmakci M (2015) A review on anaerobic biofilm reactors for the treatment of dairy industry wastewater. Process Biochem 50(2):262–271

    Article  CAS  Google Scholar 

  • Khan MZ, Mondal PK, Sabir S (2013) Aerobic granulation for wastewater bioremediation: a review. Can J Chem Eng 91(6):1045–1058

    Article  CAS  Google Scholar 

  • Kjelleberg S, Hermansson M, Marden P (1987) The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine-environment. Annu Rev Microbiol 41:25–49

    Article  CAS  PubMed  Google Scholar 

  • Klausen MM, Thomsen TR, Nielsen JL, Mikkelsen LH, Nielsen PH (2004) Variations in microcolony strength of probe-defined bacteria in activated sludge flocs. FEMS Microbiol Ecol 50(2):123–132

    Article  CAS  PubMed  Google Scholar 

  • Langer S, Schropp D, Bengelsdorf FR, Othman M, Kazda M (2014) Dynamics of biofilm formation during anaerobic digestion of organic waste. Anaerobe 29:44–51

    Article  CAS  PubMed  Google Scholar 

  • Larsen P, Nielsen JL, Otzen D, Nielsen PH (2008) Amyloid-like adhesins produced by floc-forming and filamentous bacteria in activated sludge. Appl Environ Microbiol 74(5):1517–1526

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Legrand V, Hourdet D, Audebert R, Snidaro D (1998) Deswelling and flocculation of gel networks: application to sludge dewatering. Water Res 32(12):3662–3672

    Article  CAS  Google Scholar 

  • Lemaire R, Webb RI, Yuan Z (2008) Micro-scale observations of the structure of aerobic microbial granules used for the treatment of nutrient-rich industrial wastewater. ISME Journal 2(5):528–541

    Article  CAS  PubMed  Google Scholar 

  • Li XY, Yang SF (2007) Influence of loosely bound extracellular polymeric substances (EPS) on the flocculation, sedimentation and dewaterability of activated sludge. Water Res 41(5):1022–1030

    Article  CAS  PubMed  Google Scholar 

  • Li ZH, Wang XC, Kuba T, Kusuda T (2011) Porous structure and spatial characteristics of aerobic granules. Int J Environ Pollut 45(1–3):25–35

    Article  CAS  Google Scholar 

  • Li H, Wen Y, Cao A, Huang J, Zhou Q, Somasundaran P (2012) The influence of additives (Ca2+, Al3+, and Fe3+) on the interaction energy and loosely bound extracellular polymeric substances (EPS) of activated sludge and their flocculation mechanisms. Bioresour Technol 114:188–194

    Article  CAS  PubMed  Google Scholar 

  • Li J, Ding LB, Cai A, Huang GX, Horn H (2014a) Aerobic sludge granulation in a full-scale sequencing batch reactor. BioMed Res Int. 2014:268789. doi:10.1155/2014/268789

  • Li Y, Yang SF, Zhang JJ, Li XY (2014b) Formation of artificial granules for proving gelation as the main mechanism of aerobic granulation in biological wastewater treatment. Water Sci Technol 70(3):548–554

    Article  CAS  PubMed  Google Scholar 

  • Liang M, Wang T, Li Y, Yang P, Liu C, Li P, Zhao W (2013) Structural and fractal characteristics of biofilm attached on the surfaces of aquatic plants and gravels in the rivers and lakes reusing reclaimed wastewater. Environ Earth Sci 70(5):2319–2333

    Article  CAS  Google Scholar 

  • Liao BQ, Allen DG, Leppard GG, Droppo IG, Liss SN (2002) Interparticle interactions affecting the stability of sludge flocs. J Colloid Interface Sci 249(2):372–380

    Article  CAS  PubMed  Google Scholar 

  • Lin Y, de Kreuk M, van Loosdrecht MCM, Adin A (2010) Characterization of alginate-like exopolysaccharides isolated from aerobic granular sludge in pilot-plant. Water Res 44(11):3355–3364

    Article  CAS  PubMed  Google Scholar 

  • Lin YM, Sharma PK, van Loosdrecht MCM (2013) The chemical and mechanical differences between alginate-like exopolysaccharides isolated from aerobic flocculent sludge and aerobic granular sludge. Water Res 47(1):57–65

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Fang HHP (2003) Influences of extracellular polymeric substances (EPS) on flocculation, settling, and dewatering of activated sludge. Crit Rev Environ Sci Technol 33(3):237–273

    Article  CAS  Google Scholar 

  • Liu Y, Tay JH (2002) The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Res 36(7):1653–1665

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Xu HL, Yang SF, Tay JH (2003) Mechanisms and models for anaerobic granulation in upflow anaerobic sludge blanket reactor. Water Res 37(3):661–673

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Yang SF, Tay JH, Liu QS, Qin L, Li Y (2004a) Cell hydrophobicity is a triggering force of biogranulation. Enzyme Microb Technol 34(5):371–379

    Article  CAS  Google Scholar 

  • Liu YQ, Liu Y, Tay JH (2004b) The effects of extracellular polymeric substances on the formation and stability of biogranules. Appl Microbiol Biotechnol 65(2):143–148

    Article  CAS  PubMed  Google Scholar 

  • Liu XW, Sheng GP, Yu HQ (2009) Physicochemical characteristics of microbial granules. Biotechnol Adv 27(6):1061–1070

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Gao D-W, Zhang M, Fu Y (2010a) Comparison of Ca2+ and Mg2+ enhancing aerobic granulation in SBR. J Hazard Mater 181(1–3):382–387

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Li WW, Sheng GP, Liu ZF, Zeng RJ, Liu JX, Yu HQ, Lee DJ (2010b) Microscale hydrodynamic analysis of aerobic granules in the mass transfer process. Environ Sci Technol 44(19):7555–7560

    Article  CAS  PubMed  Google Scholar 

  • Liu XM, Sheng GP, Luo HW, Zhang F, Yuan SJ, Xu J, Zeng RJ, Wu JG, Yu HQ (2010c) Contribution of extracellular polymeric substances (EPS) to the sludge aggregation. Environ Sci Technol 44(11):4355–4360

    Article  CAS  PubMed  Google Scholar 

  • Liu YQ, Moy B, Kong YH, Tay JH (2010d) Formation, physical characteristics and microbial community structure of aerobic granules in a pilot-scale sequencing batch reactor for real wastewater treatment. Enzyme Microb Technol 46(6):520–525

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Zeng P, Song Y, Song C, Zhao L (2011) Short-term storage and subsequent reactivation of aerobic granules cultivated with phenol emissions. In: Hu J (ed) Advances in biomedical engineering. Advances in Biomedical Engineering. Proceedings of 2011 International Conference on Agricultural and Biosystems Engineering, pp 309–312

  • Lv J, Wang Y, Zhong C, Li Y, Hao W, Zhu J (2014a) The microbial attachment potential and quorum sensing measurement of aerobic granular activated sludge and flocculent activated sludge. Bioresour Technol 151:291–296

    Article  CAS  PubMed  Google Scholar 

  • Lv Y, Wan C, Lee DJ, Liu X, Tay JH (2014b) Microbial communities of aerobic granules: granulation mechanisms. Bioresour Technol 169:344–351

    Article  CAS  PubMed  Google Scholar 

  • Lynch MJ, Swift S, Kirke DF, Keevil CW, Dodd CE, Williams P (2002) The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ Microbiol 4(1):18–28

    Article  CAS  PubMed  Google Scholar 

  • Mahendran B, Lishman L, Liss SN (2012) Structural, physicochemical and microbial properties of flocs and biofilms in integrated fixed-film activated sludge (IFFAS) systems. Water Res 46(16):5085–5101

    Article  CAS  PubMed  Google Scholar 

  • Maksimova YG (2014) Microbial biofilms in biotechnological processes. Appl Biochem Microbiol 50(8):750–760

    Article  CAS  Google Scholar 

  • Martín-Cereceda M, Jorand F, Guinea A, Block JC (2001) Characterization of extracellular polymeric substances in rotating biological contactors and activated sludge flocs. Environ Technol 22(8):951–959

    Article  PubMed  Google Scholar 

  • Mascarenhas T, Mikkelsen LH, Nielsen PH (2004) Effects of chlorination on the adhesion strength and deflocculation of activated sludge flocs. Water Environ Res 76(4):327–333

    Article  CAS  PubMed  Google Scholar 

  • Mayer C, Moritz R, Kirschner C, Borchard W, Maibaum R, Wingender J, Flemming HC (1999) The role of intermolecular interactions: studies on model systems for bacterial biofilms. Int J Biol Macromol 26(1):3–16

    Article  CAS  PubMed  Google Scholar 

  • McSwain BS, Irvine RL, Hausner M, Wilderer PA (2005) Composition and distribution of extracellular polymeric substances in aerobic flocs and granular sludge. Appl Environ Microb 71(2):1051–1057

    Article  CAS  Google Scholar 

  • Metcalf L, Eddy HP, Tchobanoglous G (2010) Wastewater engineering: treatment, disposal, and reuse. McGraw-Hill, New York

  • Metivier R, Bourven I, Labanowski J, Guibaud G (2013) Interaction of erythromycin ethylsuccinate and acetaminophen with protein fraction of extracellular polymeric substances (EPS) from various bacterial aggregates. Environ Sci Pollut R 20(10):7275–7285

    Article  CAS  Google Scholar 

  • Mezger TG (2006) The rheology handbook: for users of rotational and oscillatory rheometers. Vincentz Network, Hannover

  • Miksch K, Konczak B (2012) Distribution of extracellular polymeric substances and their role in aerobic granule formation. Chem Process Eng -Inzynieria Chemiczna I Procesowa 33(4):679–688

    CAS  Google Scholar 

  • Mishima K, Nakamura M (1991) Self-immobilization of aerobic activated-sludge - a pilot-study of the aerobic upflow sludge blanket process in municipal sewage-treatment. Water Sci Technol 23(4–6):981–990

    CAS  Google Scholar 

  • Morgan-Sagastume F, Allen DG (2005) Activated sludge deflocculation under temperature upshifts from 30 to 45°C. Water Res 39(6):1061–1074

    Article  CAS  PubMed  Google Scholar 

  • Mu Y, Yu HQ, Wang G (2006) Permeabilities of anaerobic CH4-producing granules. Water Res 40(9):1811–1815

    Article  CAS  PubMed  Google Scholar 

  • Mu Y, Ren TT, Yu HQ (2008) Drag coefficient of porous and permeable microbial granules. Environ Sci Technol 42(5):1718–1723

    Article  CAS  PubMed  Google Scholar 

  • Mulder A, Vandegraaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16(3):177–183

    Article  CAS  Google Scholar 

  • Ni BJ, Yu HQ (2010) Mathematical modeling of aerobic granular sludge: a review. Biotechnol Adv 28(6):895–909

    Article  CAS  PubMed  Google Scholar 

  • Ni S-Q, Zhang J (2013) Anaerobic ammonium oxidation: from laboratory to full-scale application. BioMed research international 2013:469360–469360

    PubMed Central  PubMed  Google Scholar 

  • Ni BJ, Hu BL, Fang F, Xie WM, Kartal B, Liu XW, Sheng GP, Jetten M, Zheng P, Yu HQ (2010) Microbial and physicochemical characteristics of compact anaerobic ammonium-oxidizing granules in an upflow anaerobic sludge blanket reactor. Appl Environ Microbiol 76(8):2652–2656

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nicolella C, van Loosdrecht MCM, Heijnen JJ (2000) Wastewater treatment with particulate biofilm reactors. J Biotechnol 80(1):1–33

    Article  CAS  PubMed  Google Scholar 

  • Nielsen P, Jahn A (1999) Extraction of EPS. In: Neu T, Flemming HC (eds) Wingender J. Microbial extracellular polymeric substances, Springer Berlin Heidelberg, pp 49–72

    Google Scholar 

  • Nielsen PH, Keiding K (1998) Disintegration of activated sludge flocs in presence of sulfide. Water Res 32(2):313–320

    Article  CAS  Google Scholar 

  • Nielsen PH, Frølund B, Keiding K (1996) Changes in the composition of extracellular polymeric substances in activated sludge during anaerobic storage. Appl Microbiol Biotechnol 44(6):823–830

    Article  CAS  PubMed  Google Scholar 

  • Nielsen PH, Thomsen TR, Nielsen JL (2003) Bacterial composition of activated sludge - importance for floc and sludge properties. Water Sci Technol 49(10):51–58

    Google Scholar 

  • Ning YF, Chen YP, Shen Y, Zeng N, Liu SY, Guo JS, Fang F (2014) A new approach for estimating aerobic-anaerobic biofilm structure in wastewater treatment via dissolved oxygen microdistribution. Chem Eng J 255:171–177

    Article  CAS  Google Scholar 

  • Olofsson AC, Zita A, Hermansson M (1998) Floc stability and adhesion of green-fluorescent-protein-marked bacteria to flocs in activated sludge. Microbiology-Uk 144:519–528

    Article  CAS  Google Scholar 

  • Park C, Novak JT (2009) Characterization of lectins and bacterial adhesins in activated sludge flocs. Water Environ Res 81(8):755–764

    Article  CAS  PubMed  Google Scholar 

  • Pellicer-Nàcher C, Domingo-Félez C, Mutlu AG, Smets BF (2013) Critical assessment of extracellular polymeric substances extraction methods from mixed culture biomass. Water Res 47(15):5564–5574

    Article  PubMed  CAS  Google Scholar 

  • Peng DC, Bernet N, Delgenes JP, Moletta R (1999) Aerobic granular sludge–a case report. Water Res 33(3):890–893

    Article  CAS  Google Scholar 

  • Peng G, Ye F, Li Y (2012) Investigation of extracellular polymer substances (EPS) and physicochemical properties of activated sludge from different municipal and industrial wastewater treatment plants. Environ Technol 33(8):857–863

    Article  CAS  PubMed  Google Scholar 

  • Pradhan N, Dipasquale L, d’Ippolito G, Panico A, Lens PNL, Esposito G, Fontana A (2015) Hydrogen production by the thermophilic bacterium Thermotoga neapolitana. Int J Mol Sci 16:12578–12600

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raszka A, Chorvatova M, Wanner J (2006) The role and significance of extracellular polymers in activated sludge. Part I: literature review. Acta Hydrochim Hydrobiol 34(5):411–424

    Article  CAS  Google Scholar 

  • Ren TT, Yu HQ, Li XY (2010) The quorum-sensing effect of aerobic granules on bacterial adhesion, biofilm formation, and sludge granulation. Appl Microbiol Biotechnol 88(3):789–797

    Article  CAS  PubMed  Google Scholar 

  • Rittmann BE, Manem JA (1992) Development and experimental evaluation of a steady-state, multispecies biofilm model. Biotechnol Bioeng 39(9):914–922

    Article  CAS  PubMed  Google Scholar 

  • Serpell LC (2000) Alzheimer’s amyloid fibrils: structure and assembly. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease 1502(1):16–30

    Article  CAS  Google Scholar 

  • Seviour T, Pijuan M, Nicholson T, Keller J, Yuan Z (2009a) Gel-forming exopolysaccharides explain basic differences between structures of aerobic sludge granules and floccular sludges. Water Res 43(18):4469–4478

    Article  CAS  PubMed  Google Scholar 

  • Seviour T, Pijuan M, Nicholson T, Keller J, Yuan Z (2009b) Understanding the properties of aerobic sludge granules as hydrogels. Biotechnol Bioeng 102(5):1483–1493

    Article  CAS  PubMed  Google Scholar 

  • Seviour T, Donose BC, Pijuan M, Yuan Z (2010a) Purification and conformational analysis of a key exopolysaccharide component of mixed culture aerobic sludge granules. Environ Sci Technol 44(12):4729–4734

    Article  CAS  PubMed  Google Scholar 

  • Seviour T, Lambert LK, Pijuan M, Yuan Z (2010b) Structural determination of a key exopolysaccharide in mixed culture aerobic sludge granules using NMR spectroscopy. Environ Sci Technol 44(23):8964–8970

    Article  CAS  PubMed  Google Scholar 

  • Seviour TW, Lambert LK, Pijuan M, Yuan Z (2011) Selectively inducing the synthesis of a key structural exopolysaccharide in aerobic granules by enriching for Candidatus "Competibacter phosphatis". Appl Microbiol Biotechnol 92(6):1297–1305

    Article  CAS  PubMed  Google Scholar 

  • Seviour T, Yuan Z, van Loosdrecht MCM, Lin Y (2012) Aerobic sludge granulation: a tale of two polysaccharides? Water Res 46(15):4803–4813

    Article  CAS  PubMed  Google Scholar 

  • Sheng GP, Yu HQ, Li XY (2006) Stability of sludge flocs under shear conditions: roles of extracellular polymeric substances (EPS). Biotechnol Bioeng 93(6):1095–1102

    Article  CAS  PubMed  Google Scholar 

  • Sheng GP, Yu HQ, Li XY (2010) Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnol Adv 28(6):882–894

    Article  CAS  PubMed  Google Scholar 

  • Shrout JD, Nerenberg R (2012) Monitoring bacterial twitter: does quorum sensing determine the behavior of water and wastewater treatment biofilms? Environ Sci Technol 46(4):1995–2005

    Article  CAS  PubMed  Google Scholar 

  • Snidaro D, Zartarian F, Jorand F, Bottero JY, Block JC, Manem J (1997) Characterization of activated sludge flocs structure. Water Sci Technol 36(4):313–320

    Article  CAS  Google Scholar 

  • Sobeck DC, Higgins MJ (2002) Examination of three theories for mechanisms of cation-induced bioflocculation. Water Res 36(3):527–538

    Article  CAS  PubMed  Google Scholar 

  • Sponza DT (2002) Extracellular polymer substances and physicochemical properties of flocs in steady- and unsteady-state activated sludge systems. Process Biochem 37(9):983–998

    Article  CAS  Google Scholar 

  • Su KZ, Yu HQ (2006a) A generalized model for aerobic granule-based sequencing batch reactor. 1. Model development. Environ Sci Technol 40(15):4703–4708

    Article  CAS  PubMed  Google Scholar 

  • Su KZ, Yu HQ (2006b) A generalized model for aerobic granule-based sequencing batch reactor. 2. Parametric sensitivity and model verification. Environ Sci Technol 40(15):4709–4713

    Article  CAS  PubMed  Google Scholar 

  • Szalai AJ, VanCott J, McGhee JR, Volanakis JE, Benjamin WH (2000) Human C-reactive protein is protective against fatal Salmonella enterica serovar Typhimurium infection in transgenic mice. Infect Immun 68(10):5652–5656

  • Szilveszter S, Raduly B, Abraham B, Lanyi S (2013) In situ imaging of biopolymers and extracellular enzymes in activated sludge flocs of a municipal wastewater treatment plant. J Chem Technol Biotechnol 88(7):1295–1304

    Article  CAS  Google Scholar 

  • Tay JH, Xu HL, Teo KC (2000) Molecular mechanism of granulation. I: H+ trans location-dehydration theory. J Environ Eng-Asce 126(5):403–410

    Article  CAS  Google Scholar 

  • Tay JH, Ivanov V, Pan S, Tay STL (2002) Specific layers in aerobically grown microbial granules. Lett Appl Microbiol 34(4):254–257

    Article  CAS  PubMed  Google Scholar 

  • Teo KC, Xu HL, Tay JH (2000) Molecular mechanism of granulation. II: proton translocating activity. J Environ Eng-Asce 126(5):411–418

    Article  CAS  Google Scholar 

  • Tian Y, Zheng L, Sun DZ (2006) Functions and behaviors of activated sludge extracellular polymeric substances (EPS): a promising environmental interest. J Environ Sci-China 18(3):420–427

    CAS  PubMed  Google Scholar 

  • Vazquez-Padin J, Mosquera-Corral A, Luis Campos J, Mendez R, Revsbech NP (2010) Microbial community distribution and activity dynamics of granular biomass in a CANON reactor. Water Res 44(15):4359–4370

    Article  CAS  PubMed  Google Scholar 

  • Vlaeminck SE, Terada A, Smets BF, De Clippeleir H, Schaubroeck T, Bolca S, Demeestere L, Mast J, Boon N, Carballa M, Verstraete W (2010) Aggregate size and architecture determine microbial activity balance for one-stage partial nitritation and anammox. Appl Environ Microbiol 76(3):900–909

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Volcke EIP, Picioreanu C, De Baets B, van Loosdrecht MCM (2010) Effect of granule size on autotrophic nitrogen removal in a granular sludge reactor. Environ Technol 31(11):1271–1280

    Article  CAS  PubMed  Google Scholar 

  • von Sperling M (2007) Basic principles of wastewater treatment. IWA, London

  • Wan J, Mozo I, Filali A, Line A, Bessiere Y, Sperandio M (2011) Evolution of bioaggregate strength during aerobic granular sludge formation. Biochem Eng J 58–59:69–78

    Article  CAS  Google Scholar 

  • Wan C, Lee DJ, Yang X, Wang Y, Wang X, Liu X (2015) Calcium precipitate induced aerobic granulation. Bioresour Technol 176:32–37

    Article  CAS  PubMed  Google Scholar 

  • Wang ZW, Liu Y, Tay JH (2005) Distribution of EPS and cell surface hydrophobicity in aerobic granules. Appl Microbiol Biotechnol 69(4):469–473

    Article  CAS  PubMed  Google Scholar 

  • Wang HL, Yu GL, Liu GS, Pan F (2006) A new way to cultivate aerobic granules in the process of papermaking wastewater treatment. Biochem Eng J 28(1):99–103

    Article  CAS  Google Scholar 

  • Wang BB, Chang Q, Peng DC, Hou YP, Li HJ, Pei LY (2014a) A new classification paradigm of extracellular polymeric substances (EPS) in activated sludge: separation and characterization of exopolymers between floc level and microcolony level. Water Res 64:53–60

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Zheng P, Xing Y, Li W, Yang J, Abbas G, Liu S, He Z, Zhang J, Zhang H, Lu H (2014b) Effect of particle size on the performance of autotrophic nitrogen removal in the granular sludge bed reactor and microbiological mechanisms. Bioresour Technol 157:240–246

    Article  CAS  PubMed  Google Scholar 

  • Weissbrodt DG, Neu TR, Kuhlicke U, Rappaz Y, Holliger C (2013) Assessment of bacterial and structural dynamics in aerobic granular biofilms. Frontiers in Microbiology 4:175. doi:10.3389/fmicb.2013.00175

  • Wilén BM, Nielsen JL, Keiding K, Nielsen PH (2000) Influence of microbial activity on the stability of activated sludge flocs. Colloid Surface B 18(2):145–156

    Article  Google Scholar 

  • Wilén BM, Jin B, Lant P (2003) The influence of key chemical constituents in activated sludge on surface and flocculating properties. Water Res 37(9):2127–2139

    Article  PubMed  CAS  Google Scholar 

  • Wilén BM, Onuki M, Hermansson M, Lumley D, Mino T (2008) Microbial community structure in activated sludge floc analysed by fluorescence in situ hybridization and its relation to floc stability. Water Res 42(8–9):2300–2308

    Article  PubMed  CAS  Google Scholar 

  • Wilén BM, Lumley D, Mattsson A, Mino T (2010) Dynamics in flocculation and settling properties studied at a full-scale activated sludge plant. Water Environ Res 82(2):155–168

    Article  PubMed  CAS  Google Scholar 

  • Williams P, Cámara M (2009) Quorum sensing and environmental adaptation in pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12(2):182–191

  • Wingender J, Neu TR, Flemming HC (1999) Microbial extracellular polymeric substances: characterization, structure, and function. Springer Berlin Heidelberg

  • Yang SF, Li XY (2009) Influences of extracellular polymeric substances (EPS) on the characteristics of activated sludge under non-steady-state conditions. Process Biochem 44(1):91–96

    Article  CAS  Google Scholar 

  • Yin C, Meng F, Chen GH (2015) Spectroscopic characterization of extracellular polymeric substances from a mixed culture dominated by ammonia-oxidizing bacteria. Water Res 68:740–749

    Article  CAS  PubMed  Google Scholar 

  • Yu G-H, He PJ, Shao LM, Lee DJ (2007) Enzyme activities in activated sludge flocs. Appl Microbiol Biotechnol 77(3):605–612

    Article  CAS  PubMed  Google Scholar 

  • Yu G-H, He PJ, Shao LM, He P-P (2008) Stratification structure of sludge flocs with implications to dewaterability. Environ Sci Technol 42(21):7944–7949

    Article  CAS  PubMed  Google Scholar 

  • Yu G-H, He PJ, Shao LM (2009) Characteristics of extracellular polymeric substances (EPS) fractions from excess sludges and their effects on bioflocculability. Bioresour Technol 100(13):3193–3198

    Article  CAS  PubMed  Google Scholar 

  • Yuan DQ, Wang YL, Feng J (2014) Contribution of stratified extracellular polymeric substances to the gel-like and fractal structures of activated sludge. Water Res 56:56–65

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Feng X, Zhu N, Chen J (2007) Role of extracellular protein in the formation and stability of aerobic granules. Enzyme Microb Technol 41(5):551–557

    Article  CAS  Google Scholar 

  • Zhang ZJ, Wu WW, Wang JL (2010) Characteristics of autotrophic nitrifying granular sludge in sequencing batch reactor. Huanjing Kexue 31(5):1257–1262

    CAS  PubMed  Google Scholar 

  • Zhang SH, Yu X, Guo F, Wu ZY (2011) Effect of interspecies quorum sensing on the formation of aerobic granular sludge. Water Sci Technol 64(6):1284–1290

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Hendrickx TLG, Kampman C, Temmink H, Zeeman G (2013) Co-digestion to support low temperature anaerobic pretreatment of municipal sewage in a UASB-digester. Bioresour Technol 148:560–566

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Fang F, Chen YP, Shen Y, Zhang W, Yang JX, Li C, Guo JS, Liu SY, Huang Y, Li S, Gao X, Yan P (2014) Composition of EPS fractions from suspended sludge and biofilm and their roles in microbial cell aggregation. Chemosphere 117:59–65

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Guo JS, Shen Y, Yan P, Chen YP, Wang H, Yang JX, Fang F, Li C (2015a) Microbial communities, extracellular proteomics and polysaccharides: a comparative investigation on biofilm and suspended sludge. Bioresour Technol 190:21–28

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Shen Y, Guo JS, Li C, Wang H, Chen YP, Yan P, Yang JX, Fang F (2015b) Extracellular protein analysis of activated sludge and their functions in wastewater treatment plant by shotgun proteomics. Scientific Reports 5:12041

    Article  PubMed Central  PubMed  Google Scholar 

  • Zheng D, Angenent LT, Raskin L (2006) Monitoring granule formation in anaerobic upflow bioreactors using oligonucleotide hybridization probes. Biotechnol Bioeng 94(3):458–472

    Article  CAS  PubMed  Google Scholar 

  • Zhou D, Niu S, Xiong Y, Yang Y, Dong S (2014) Microbial selection pressure is not a prerequisite for granulation: dynamic granulation and microbial community study in a complete mixing bioreactor. Bioresour Technol 161:102–108

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was carried out in the framework of the Project “Modular photo-biologic reactor for bio-hydrogen: application to dairy waste–RE-MIDA” by the Agriculture Department of the Campania Region in the context of the “Programme of Rural Development 2007-2013, Measure 124.” The authors would also like to acknowledge the Erasmus Mundus Joint Doctorate Programme ETeCoS3 (Environmental Technologies for Contaminated Solids, Soils and Sediments) under the EU grant agreement FPA No 2010-0009.

Compliance with ethical standards

The authors declare that they have no conflict of interest, and the research involves neither human participants nor animal.

Author information

Authors and Affiliations

  1. Department of Civil and Mechanical Engineering, University of Cassino and Southern Lazio, via Di Biasio 43, 03043, Cassino, FR, Italy

    Zhiji Ding & Giovanni Esposito

  2. Groupement de Recherche Eau Sol Environnement, Université de Limoges, 123 Av. Albert Thomas, 87060, Limoges, France

    Isabelle Bourven & Gilles Guibaud

  3. Laboratoire Géomatériaux et Environnement (EA 4508), Université Paris-Est, UPEM, Marne la Vallée, 77454, Paris, France

    Eric D. van Hullebusch

  4. Telematic University Pegaso, Piazza Trieste e Trento 48, 80132, Naples, Italy

    Antonio Panico

  5. Department of Civil, Architectural and Environmental Engineering, University of Naples Federico II, via Claudio 21, 80125, Naples, Italy

    Francesco Pirozzi

Authors
  1. Zhiji Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabelle Bourven
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gilles Guibaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric D. van Hullebusch
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Antonio Panico
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Francesco Pirozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giovanni Esposito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhiji Ding.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ding, Z., Bourven, I., Guibaud, G. et al. Role of extracellular polymeric substances (EPS) production in bioaggregation: application to wastewater treatment. Appl Microbiol Biotechnol 99, 9883–9905 (2015). https://doi.org/10.1007/s00253-015-6964-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6964-8

Keywords

Search

Navigation