Abstract
Biogranulation is a promising biotechnology developed for wastewater treatment. Biogranules exhibit a matrix microbial structure, and intensive research has shown that extracellular polymeric substances (EPS) are a major component of the biogranule matrix material in both anaerobic and aerobic granules. This paper aims to review the role of EPS in biogranulation, factors influencing EPS production, the effect of EPS on cell surface properties of biogranules, and the relationship of EPS to the structural stability of biogranules. EPS production is substantially enhanced when the microbial community is subject to stressful culture conditions, and the stimulated EPS production in the microbial matrix in turn favours the formation of anaerobic and aerobic granules. EPS can also play an essential role in maintaining the integrity and stability of spatial structure in mature biogranules. It is expected that this paper can provide deep insights into the functions of EPS in the biogranulation process.
Similar content being viewed by others
References
Andreadakis AD (1993) Physical and chemical properties of activated sludge flocs. Water Res 27:1701–1714
Azeredo J, Lazarova V, Oliverira R (1999) Methods to extract the exopolymeric matrix from biofilms: a comparative study. Water Sci Technol 39:243–250
Babcock GT, Wikstrom M (1992) Oxygen activation and the conservation of energy in cell respiration. Nature 356:301–309
Batstone DJ, Keller J (2001) Variation of bulk properties of anaerobic granules with wastewater type. Water Res 35:1723–1729
Beer D de, Flaharty VO, Thareesri J, Lens P, Verstraete W (1996) Distribution of extracellular polysaccharides and flotation of anaerobic sludge. Appl Microbiol Biotechnol 46:197–201
Cammarota MC, Sant’Anna GL (1998) Metabolic blocking of exopolysaccharides synthesis: effects on microbial adhesion and biofilm accumulation. Biotechnol Lett 20:1–4
Chan CS, De Stasio G, Welch SA, Girasole M, Frazer BH, Nesterova MV, Fakra S, Banfield JF (2004) Microbial polysaccharides template assembly of nanocrystal fibers. Science 303:1656–1658
Costerton JW, Irvin RT, Cheng KJ (1981) The bacterial glycocalyx in nature and disease. Annu Rev Microbiol 35:299–324
Daffochio D, Thaveesri J, Verstraete W (1995) Contact angle measurement and cell hydrophobicity of granular sludge from upflow anaerobic sludge bed reactors. Biotechnol Lett 61:3676–3680
Dignac MF, Urbain V, Rybacki D, Bruchet A, Snidaro D, Scribe P (1998) Chemical description of extracellular polymers: implication on activated sludge floc structure. Water Sci Technol 38:45–53
Durmaz B, Sanin FD (2001) Effect of carbon to nitrogen ratio on the composition of microbial extracellular polymers in activated sludge. Water Sci Technol 44:221–229
El-Mamouni R, Leduc R, Costerton JW, Guiot SR (1995) Influence of the microbial content of different precursory nuclei on the anaerobic granulation dynamics. Water Sci Technol 32:173–177
Etchebehere C, Cabezas A, Dabert P, Muxi L (2003) Evolution of the bacterial community during granules formation in denitrifying reactors followed by molecular, culture-independent techniques. Water Sci Technol 48:75–79
Fang HHP (2000) Microbial distribution in UASB granules and its resulting effects. Water Sci Technol 42:201–208
Fang HHP, Liu H, Zhang T (2002) Characterization of a hydrogen-producing granular sludge. Biotechnol Bioeng 78:44–52
Forster CF (1992) Anaerobic upflow sludge blanket reactors: aspects of their microbiology and chemistry. J Biotechnol 17:221–232
Frolund B, Palmgren R, Keiding K, Nielsen P (1996) Extraction of extracellular polymers from activated sludge using a cation exchange resin. Water Res 30:1749–1758
Fukuzaki S, Nishio N, Nagai S (1995) High rate performance and characterisation of granular methanogenic sludges in upflow anaerobic sludge blanket reactors fed with various defined substrates. J Ferment Bioeng 79:354–359
Ghigo JM (2003) Are there biofilm-specific physiological pathways beyond a reasonable doubt? Res Microbiol 154:1–8
Goodwin JAS, Forster CF (1985) A further examination into the composition of activated sludge surfaces in relation to their settlement characteristics. Water Res 19:527–533
Grotenhuis JTC, Smith M, van Lammeran AAM, Stams AJM, Zehnder AJB (1991) Localization and quantification of extracellular polymers in methanogenic granular sludge. Appl Microbiol Biotechnol 36:115–119
Horan NJ, Eccles CR (1986) Purification and characterization of extracellular polysaccharide from activated sludge. Water Res 20:1427–1432
Jiang HL, Tay JH, Tay STL (2002) Aggregation of immobilized activated sludge into aerobically grown microbial granule for the aerobic biodegradation of phenol. Lett Appl Microbiol 35:439–445
Jiang HL, Tay JH, Tay STL (2003) Changes in structure, activity and metabolism of aerobic granules as a microbial response to high phenol loading. Appl Microbiol Biotechnol 63:602–608
Jorand F, Guicherd P, Urbain V, Manem J, Block JC (1994) Hydrophobicity of activated sludge flocs and laboratory-growth bacteria. Water Sci Technol 30:211–218
Jorand F, Zartarian F, Thomas F, Block JC, Bottero JY, Villemin G, Urbain V, Manem J (1995) Chemical and structural (2D) linkage between bacteria within activated sludge flocs. Water Res 29:1639–1647
Jorand F, Boue-Bigne F, Block JC, Urbain V (1998) Hydrophobic/hydrophilic properties of activated sludge exopolymeric substances. Water Sci Technol 37:307–315
Liao BQ, Allen DG, Droppo IG, Leppard GG, Liss SN (2001) Surface properties of sludge and their role in bioflocculation and settleability. Water Res 35:339–350
Liu H, Fang HHP (2002) Characterization of electrostatic binding sites of extracellular polymers by linear programming analysis of titration data. Biotechnol Bioeng 80:806–811
Liu Y, Xu HL, Show KY, Tay JH (2002) Anaerobic granulation technology for wastewater treatment. World J Microbiol Biotechnol 18:99–113
Liu QS, Tay JH, Liu Y (2003) Substrate concentration-independent aerobic granulation in sequential aerobic sludge blanket reactor. Environ Technol 24:1235–1242
Liu Y, Yang SF, Tay JH (2004a) Improved stability of aerobic granules by selecting slow-growing nitrifying bacteria. J Biotechnol 108:161–169
Liu Y, Yang SF, Tay JH, Liu QS, Qin Lei, Li Y (2004b) Cell hydrophobicity is a triggering force of biogranulation. Enzyme Microb Technol 34:371–379
Lopez JM, Koopman B, Bitton G (1986) INT-dehydrogenase test for activated sludge process control. Biotechnol Bioeng 28:1080–1085
Macleod FA, Guiot SR, Costerton JW (1995) Electron-microscopic examination of the extracellular polymeric substances in anaerobic granular biofilms. World J Microbiol Biotechnol 11:481–485
Mahmoud N, Zeeman G, Gijzen H, Lettinga G (2003) Solids removal in upflow anaerobic reactors, a review. Bioresour Technol 90:1–9
Martinez FO, Lema J, Mendez R, Cuervo-Lopez F, Gomez J (2004) Role of exopolymeric protein on the settleability of nitrifying sludges. Bioresour Technol 94:43–48
Mcnab R, Forbes H, Handley P, Loach DM, Tannock GW, Jenkison HF (1999) Cell wall-anchored CshA polypeptide (259 kilodaltons) in Streptococcus gordonii forms surface fibrils that confer hydrophobic and adhesive properties. J Bacteriol 181:3087–3095
Morgan JW, Forster CF, Evison L (1990) A comparative study of the nature of biopolymers extracted from anaerobic and activated sludges. Water Res 24:743–750
Nichols CAM, Garon S, Bowman JP, Raguenes G, Guezennec J (2004) Production of exopolysaccharides by Antarctic marine bacterial isolates. J Appl Microbiol 96:1057–1066
Nielsen PH, Jahn A, Palmgren R (1997) Conceptual model for production and composition of exopolymers in biofilms. Water Sci Technol 36:11–19
Pavoni JL, Tenney MW, Echelberger JWF (1972) Bacterial extracellular polymers and biological flocculation. J Water Pollut Control Fed 44:414–431
Punal A, Trevisan M, Rozzi A, Lema JM (2000) Influence of C:N ratio on the start-up of up-flow anaerobic filter reactors. Water Res 34:2614–2619
Punal A, Brauchi S, Rdyes JG, Chamy R (2003) Dynamics of extracellular polymeric substances in UASB and EGSB reactors treating medium and low concentrated wastewaters. Water Sci Technol 48:41–49
Qin L, Liu QS, Yang SF, Tay JH, Liu Y (2004a) Stressful conditions-induced production of extracellular polysaccharides in aerobic granulation process. Civil Eng Res 17:49–51
Qin L, Tay JH, Liu Y (2004b) Selection pressure is a driving force of aerobic granulation in sequencing batch reactors. Process Biochem 39:579–584
Quarmby J, Forster CF (1995) An examination of the structure of UASB granules. Water Res 29:2449–2454
Ross WR (1984) The phenomenon of sludge pelletization in the anaerobic treatment of a maize processing waste. Water SA 10:197–204
Rouxhet PG, Mozes N (1990) Physical chemistry of the interaction between attached microorganisms and their support. Water Sci Technol 22:1–16
Schmidt JE, Ahring BK (1994) Extracellular polymers in granular sludge from different upflow anaerobic sludge blanket (UASB) reactors. Appl Microbiol Biotechnol 42:457–462
Schmidt JE, Ahring BK (1996) Granular sludge formation in upflow anaerobic sludge blanket (UASB) reactors. Biotechnol Bioeng 49:229–246
Shen CF, Kosaric N, Blaszczyk R (1993) The effect of selected heavy metals (Ni, Co and Fe) on anaerobic granules and their extracellular polymeric substance (EPS). Water Res 27:25–33
Singh KK, Vincent WS (1987) Clumping characteristics and hydrophobic behavior of an isolated bacterial strain from sewage sludge. Appl Microbiol Biotechnol 25:396–398
Singleton DR, Masuoka J, Hazen KC (2001) Cloning and analysis of a Candida albicans gene that affects cell surface hydrophobicity. J Bacteriol 183:3582–3588
Sponza DT (2002) Extracellular polymer substances and physicochemical properties of flocs in steady- and unsteady-state activated sludge systems. Process Biochem 37:983–998
Strand SP, Varum KM, Ostgaard K (2003) Interactions between chitosans and bacterial suspensions: adsorption and flocculation. Colloids Surf B 27:71–81
Tay JH, Liu QS, Liu Y (2001a) The role of cellular polysaccharides in the formation and stability of aerobic granules. Lett Appl Microbiol 33:222–226
Tay JH, Liu QS, Liu Y (2001b) The effects of shear force on the formation, structure and metabolism of aerobic granules. Appl Microbiol Biotechnol 57:227–233
Tay JH, Liu QS, Liu Y (2001c) Microscopic observation of aerobic granulation in sequential aerobic sludge blanket reactor. J Appl Microbiol 91:168–175
Tay JH, Yang SF, Liu Y (2002) Hydraulic selection pressure-induced nitrifying granulation in sequencing batch reactors. Appl Microbiol Biotechnol 59:332–337
Trevors JT (1984) The measurement of electron transport system (ETS) activity in freshwater sediment. Water Res 18:581–584
Tsuneda S, Jung J, Hayashi H, Aikawa H, Hirata A, Sasaki H (2003a) Influence of extracellular polymers on electrokinetic properties of heterotrophic bacterial cells examined by soft particle electrophoresis theory. Colloids Surf B 29:181–188
Tsuneda S, Aikawa H, Hayashi H, Yuasa A, Hirata A (2003b) Extracellular polymeric substances responsible for bacterial adhesion onto solid surface. FEMS Microbiol Lett 223:287–292
Urbain V, Block JC, Manem J (1993) Bioflocculation in activated sludge, an analytic approach. Water Res 27:829–838
Veiga MC, Jain MK, Wu WM, Hollingsworth RI, Zeikus JG (1997) Composition and role of extracellular polymers in methanogenic granules. Appl Environ Microbiol 63:403–407
Yang SF, Tay JH, Liu Y (2003) A novel granular sludge sequencing-batch reactor for organic and nitrogen removal from wastewater. J Biotechnol 106:77–86
Yang SF, Tay JH, Liu Y (2004) Inhibition of free ammonia to the formation of aerobic granules. Biochem Eng J 17:41–48
Yi S, Tay JH, Maszenan AM, Tay STL (2003) A culture-independent approach for studying microbial diversity in aerobic granules. Water Sci Technol 47:283–290
Yu HQ, Tay JH, Fang HHP (2001) The roles of calcium in sludge granulation during UASB reactor start-up. Water Res 35:1052–1060
Zhang XQ, Bishop PL (2001) Spatial distribution of extracellular polymeric substances in biofilms. J Environ Eng 127:850–856
Zhang XQ, Bishop PL, Kinkle BK (1999) Comparison of extraction methods for quantifying extracellular polymers in biofilms. Water Sci Technol 39:211–218
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liu, YQ., Liu, Y. & Tay, JH. The effects of extracellular polymeric substances on the formation and stability of biogranules. Appl Microbiol Biotechnol 65, 143–148 (2004). https://doi.org/10.1007/s00253-004-1657-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-004-1657-8