Advanced techniques for in situ analysis of the biofilm matrix (Structure, Composition, Dynamics) by means of laser scanning microscopy

Methods in Molecular Biology

Volumn 1147, Issue , 2014, Pages 43-64

  Neu, Thomas R ^a   Lawrence, John R ^a  

^a NONE

Author keywords

Bioaggregate; Biofilm; Biofilm matrix; Confocal laser scanning microscopy (CLSM); Extracellular polymeric substances (EPS); Fluorescence; Fluorescence lectin binding analysis (FLBA); Laser scanning microscopy (LSM)

Indexed keywords

AMYLOID; GLYCOCONJUGATE; NUCLEIC ACID; POLYSACCHARIDE; THIOFLAVINE;

ARTICLE; BIOFILM; CELL SURFACE; CHEMICAL COMPOSITION; CHEMICAL STRUCTURE; CONFOCAL LASER MICROSCOPY; ENZYME ACTIVITY; EPIFLUORESCENCE MICROSCOPY; EXTRACELLULAR MATRIX; FLUIDIZED BED REACTOR; FLUORESCENCE ANALYSIS; FLUORESCENCE IN SITU HYBRIDIZATION; FLUORESCENCE LECTIN BINDING ANALYSIS; LASER MICROSCOPY; LECTIN BINDING; LIPID VESICLE; MEMBRANE VESICLE; MICROBIAL COMMUNITY; MICROHABITAT; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; BACTERIAL PHENOMENA AND FUNCTIONS; CHEMISTRY; CONFOCAL MICROSCOPY; MICROBIOLOGICAL EXAMINATION;

BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIOLOGICAL TECHNIQUES; BIOFILMS; EXTRACELLULAR MATRIX; MICROSCOPY, CONFOCAL;

EID: 84910115923     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4939-0467-9_4     Document Type: Article

References (119)

1. Wingender J, Neu TR, Flemming H-C (1999) Microbial extracellular polymeric substances. Springer, Heidelberg
2. Neu TR, Lawrence JR (2009) Extracellular polymeric substances in microbial biofilms. In: Moran A, Brenan P, Holst O, von Itzstein M (eds) Microbial glycobiology: structures, relevance and applications. Elsevier, San Diego, pp 735-758
3. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623-633
4. Allison DG, Sutherland IW, Neu TR (2003) EPS: what’s in an acronym? In: Mc Bain A, Allison DG, Brading M, Rickard A, Verran J, Walker J (eds) Biofilm communities: order from chaos? BioLine, Cardiff, pp 381-387
5. Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41-55
6. Schermelleh L, Heintzmann R, Leonhardt H (2010) A guide to super-resolution fluorescence microscopy. J Cell Biol 190:165-175
7. Lawrence JR, Swerhone GDW, Leppard GG et al (2003) Scanning transmission x-ray, laser scanning, and transmission electron microscopy mapping of the exopolymeric matrix of microbial biofilms. Appl Environ Microbiol 69:5543-5554
8. Liu X, Eusterhues K, Thieme J et al (2013) STXM and NanoSIMS investigations on EPS fractions before and after adsorption to goethite. Environ Sci Technol 47:3158-3166
9. Behrens S, Kappler A, Obst M (2012) Linking environmental processes to the in situ functioning of microorganisms by highresolution secondary ion mass spectrometry (NanoSIMS) and scanning transmission X-ray microscopy (STXM). Environ Microbiol 14: 2851-2869
10. Remusat L, Hatton PJ, Nico PS et al (2012) NanoSIMS study of organic matter associated with soil aggregates: advantages, limitations, and combination with STXM. Environ Sci Technol 46:3943-3949
11. Rasconi S, Jobard M, Jouve L, Sime-Ngando T (2009) Use of calcofluor white for detection, identification, and quantification of phytoplanktonic fungal parasites. Appl Environ Microbiol 75:2545-2553 Biofilm Matrix Analysis 60
12. Neu TR, Marshall KC (1991) Microbial “footprints”: a new approach to adhesive polymers. Biofouling 3:101-112
13. Neu TR (1992) Microbial “footprints” and the general ability of microorganisms to label interfaces. Can J Microbiol 38:1005-1008
14. Sharon N, Lis H (2003) Lectins. Kluwer Academic Publishers, Dordrecht
15. Schloter M, Borlinghaus R, Bode W, Hartmann A (1993) Direct identification, and localization of Azospirillum in the rhizosphere of wheat using fluorescence-labelled monoclonal antibodies and confocal scanning laser microscopy. J Microsc 171:173-177
16. Assmus B, Schloter M, Kirchhof G et al (1997) Improved in situ tracking of rhizosphere bacteria using dual staining with fluorescencelabeled antibodies and rRNA- targeted oligonucleotides. Microb Ecol 33:32-40
17. Schloter M, Wiehe W, Assmus B et al (1997) Root colonization of different plants by plantgrowth- promoting Rhizobium leguminosarum bv. trifolii R39 studied with monospecific polyclonal antisera. Appl Environ Microbiol 63:2038-2046
18. Gilbert B, Assmus B, Hartmann A, Frenzel P (1998) In situ localization of two methanotrophic strains in the rhizosphere of rice plants. FEMS Microbiol Ecol 25:117-128
19. Palmer RJ Jr, Gordon SM, Cisar JO, Kolenbrander PE (2003) Coaggregationmediated interactions of Streptococci and Actinomyces detected in initial human dental plague. J Bacteriol 185:3400-3409
20. Chalmers NI, Palmer RJ Jr, Du-Thumm L et al (2007) Use of quantum dot luminescent probes to achieve single: cell resolution of human oral bacteria in biofilms. Appl Environ Microbiol 73:630-636
21. Periasamy S, Chalmers NI, Du-Thumm L, Kolenbrander PE (2009) Fusobacterium nucleatum ATCC 10953 requires Actinomyces naeslundii ATCC 43146 for growth on saliva in a three-species community that includes Streptococcus oralis 34. Appl Environ Microbiol 75:3250-3257
22. Periasamy S, Kolenbrander PE (2009) Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early and late colonizers of enamel. J Bacteriol 191:6804-6811
23. Periasamy S, Kolenbrander PE (2010) Central role of the early colonizer Veillonella sp . in establishing multispecies biofilm communities with initial, middle, and late colonizers of enamel. J Bacteriol 192:2965-2972
24. Neu TR, Lawrence JR (1999) Lectinbinding- analysis in biofilm systems. Methods Enzymol 310:145-152
25. Neu TR, Swerhone GDW, Lawrence JR (2001) Assessment of lectin-binding analysis for in situ detection of glycoconjugates in biofilm systems. Microbiology 147:299-313
26. Staudt C, Horn H, Hempel DC, Neu TR (2003) Screening of lectins for staining lectinspecific glycoconjugates in the EPS of biofilms. In: Lens P, Moran AP, Mahony T, Stoodley P, O’Flaherty V (eds) Biofilms in medicine, industry and environmental technology. IWA Publishing, UK, pp 308-327
27. Zippel B, Neu TR (2011) Characterization of glycoconjugates of extracellular polymeric substances in tufa-associated biofilms by using fluorescence lectin-binding analysis. Appl Environ Microbiol 77:505-516
28. Lu S, Chourey K, Reiche M et al (2013) Insights into the structure and metabolic function of microbes that shape pelagic ironrich aggregates (“iron snow”). Appl Environ Microbiol 79:4272-4281
29. Bennke CM, Neu TR, Fuchs BM, Amann R (2013) Mapping glycoconjugate-mediated interactions of marine Bacteroidetes with diatoms. Syst Appl Microbiol 36:417-425
30. Lawrence JR, Swerhone GDW, Kuhlicke U, Neu TR (2007) In situ evidence for microdomains in the polymer matrix of bacterial microcolonies. Can J Microbiol 53: 450-458
31. Saarima C, Peltola M, Raulio M et al (2006) Characterisation of adhesion threads of Deinococcus geothermalis as Type IV pili. J Bacteriol 188:7016-7021
32. Peltola M, Neu TR, Kanto-Oqvist L et al (2008) Architecture of Deinococcus geothermalis biofilms on glass and steel: a lectin study. Environ Microbiol 10:1752-1759
33. Zubkov MV, Fuchs BM, Eilers H et al (1999) Determination of total protein content of bacterial cells by SYPRO staining and flow cytometry. Appl Environ Microbiol 65: 3251-3257
34. Hinck S, Mußmann M, Salman V et al (2011) Vacuolated Beggiatoa -like filaments from different hypersaline environments form a novel genus. Environ Microbiol 13: 3194-3205
35. Rusznyak A, Akob DM, Nietzsche S et al (2012) Calcite biomineralization by bacterial isolates from the recently discovered pristine karstic Herrenberg cave. Appl Environ Microbiol 78:1157-1167
36. DePas WH, Chapman MR (2012) Microbial manipulation of the amyloid fold. Res Microbiol 163:592-606
37. Schwartz K, Boles BR (2013) Microbial amyloids − functions and interactions within the host. Curr Opin Microbiol 16:93-99
38. Larsen P, Nielsen JL, Dueholm MS et al (2007) Amyloid adhesins are abundant in natural biofilms. Environ Microbiol 9: 3077-3090
39. Gebbink MFBG, Claessen D, Bouma B et al (2005) Amyloids: a functional coat for microorganisms. Nat Rev Microbiol 3:333-341
40. Jordal PB, Dueholm MS, Larsen P et al (2009) Widespread abundance of functional bacterial amyloid in mycolata and other grampositive bacteria. Appl Environ Microbiol 75:4101-4110
41. Dueholm MS, Petersen SV, Soenderkaer M et al (2010) Functional amyloid in Pseudomonas. Mol Microbiol 77:1009-1020
42. Blanco LP, Evans ML, Smith DR et al (2012) Diversity, biogenesis and function of microbial amyloids. Trends Microbiol 20:66-73
43. Oli MW, Otoo HN, Crowley PJ et al (2012) Functional amyloid formation by Streptococcus mutans . Microbiology 158:2903-2916
44. Krebs MRH, Bromley EHC, Donald AM (2005) The binding of thioflavin-T to amyloid fibrils: localisation and implications. J Struct Biol 149:30-37
45. O’Nuallain B, Wetzel R (2002) Conformational Abs recognizing a generic amyloid fibril epitope. Proc Natl Acad Sci U S A 99: 1485-1490
46. Kloecke FO, Geesey GG (1999) Localization and identification of populations of phosphatase: active bacterial cells associated with activated sludge flocs. Microb Ecol 38:201-214
47. Espeland EM, Wetzel RG (2001) Effects of photosynthesis on bacterial phosphatase production in biofilms. Microb Ecol 42: 328-337
48. Gonzalez-Gil S, Kaefer BA, Jovine RVM et al (1998) Detection and quantification of alkaline phosphatase in single cells of phosphorousstarved marine phytoplankton. Mar Ecol Prog Ser 164:21-35
49. Rengefors K, Pettersson K, Blenckner T, Anderson DM (2001) Species-specific alkaline phosphatase activity in freshwater spring phytoplankton: application of a novel method. J Plankton Res 23:435-443
50. Nedoma J, Strojsova A, Vrba J et al (2003) Extracellular phosphatase activity of natural plankton studied with ELF97 phosphate: fluorescence quantification and labelling kits. Environ Microbiol 5:462-472
51. Strojsova A, Vrba J, Nedoma J, Komarkova J, Znachor P (2003) Seasonal study of extracellular phosphatase expression in the phytoplankton of a eutrophic reservoir. Eur J Phycol 38:295-306
52. van Aarle IM, Olsson PA, Söderström B (2001) Microscopic detection of phosphatase activity of saprophytic and arbuscular mycorrhizal fungi using a fluorogenic substrate. Mycologia 93:17-24
53. Murakawa T (1973) Slime production by Pseudomonas aeruginosa IV. Chemical analysis of two varieties of slime produced by Pseudomonas aeruginosa . Jpn J Microbiol 17:513-520
54. Palmgren R, Nielsen PH (1996) Accumulation of DNA in the extracellular matrix of activated sludge and bacterial cultures. Water Sci Technol 34:233-240
55. Whitchurch CB, Tolker-Nielsen T, Ragas P, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487
56. Allesen-Holm M, Bundvik Barken K, Yang L et al (2006) A characterisation of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114-1128
57. Yang L, Barken KB, Skindersoe ME et al (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa . Microbiology 153:1318-1328
58. Neu TR (1996) Significance of bacterial surface- active compounds in interaction of bacteria with interfaces. Microbiol Rev 60: 151-166
59. Rosenberg E, Ron EZ (1999) High- and lowmolecular- mass microbial surfactants. Appl Microbiol Biotechnol 52:154-162
60. Schooling SR, Beveridge TJ (2006) Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188:5945-5957
61. Tashiro Y, Ichikawa S, Shimizu M et al (2010) Variation of physiochemical properties and cell association activity of membrane vesicles with growth phase in Pseudomonas aeruginosa . Appl Environ Microbiol 76:3732-3739
62. Brooks SA, Leathem AJC, Schumacher U (1997) Lectin histochemistry. A concise practical handbook. Bios Scientific Publishers, Oxford
63. Lawrence JR, Wolfaardt GM, Korber DR (1994) Determination of diffusion coefficients in biofilms by confocal laser microscopy. Appl Environ Microbiol 60:1166-1173
64. Hidalgo G, Burns A, Herz E et al (2009) Functional tomographic fluorescence imaging of pH microenvironments in microbial biofilms by use of silica nanoparticle sensors. Appl Environ Microbiol 75:7426-7435
65. Acosta MA, Velasquez M, Williams K et al (2012) Fluorescent silica particles for monitoring oxygen levels in three-dimensional heterogeneous cellular structures. Biotechnol Bioeng 109:2663-2670
66. Aldeek F, Mustin C, Balan L et al (2011) Surface-engineered quantum dots for the labeling of hydrophobic microdomains in bacterial biofilms. Biomaterials 32:5459-5470
67. Aldeek F, Schneider R, Fontaine-Aupart MP et al (2013) Patterned hydrophobic domains in the exopolymer matrix of Shewanella oneidensis MR-1 biofilms. Appl Environ Microbiol 79:1400-1402
68. Epstein AK, Pokroy B, Seminara A, Aizenberg J (2011) Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration. Proc Natl Acad Sci U S A 108: 995-1000
69. Kobayashi K, Iwano M (2012) BslA(YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol Microbiol 85:51-66
70. Nielsen PH, Jahn A (1999) Extraction of EPS. In: Wingender J, Neu TR, Flemming H-C (eds) Microbial extracellular polymeric substances. Springer, Berlin, pp 49-72
71. Gallaher TK, Wu S, Webster P, Aguilera R (2006) Identification of biofilm proteins in non-typeable Haemophilus influenzae . BMC Microbiol 6:1-9
72. Curtis PD, Atwood J III, Orlando R, Shimkets LJ (2007) Proteins associated with the Myxococcus xanthus extracellular matrix. J Bacteriol 189:7634-7642
73. Dumas E, Meunier B, Berdague J-L et al (2008) Comparative analysis of extracellular and intracellular proteomes of Listeria monocytogenes strains reveals a correlation between protein expression and serovar. Appl Environ Microbiol 74:7399-7409
74. Paes Leme AF, Bellato CM, Bedi G et al (2008) Effects of Sucrose on the extracellular matrix of plaque-like biofilm formed in vivo, studied by proteomic analysis. Caries Res 42: 435-443
75. Cao B, Shi L, Brown RN et al (2011) Extracellular polymeric substances from Shewanella sp . HRCR-1 biofilms: characterization by infrared spectroscopy and proteomics. Environ Microbiol 13:1018-1031
76. Ivleva N, Wagner M, Horn H, Niessner R, Haisch C (2009) Towards a nondestructive chemical characterization of biofilm matrix by Raman microscopy. Anal Bioanal Chem 393: 197-206
77. Wagner M, Ivleva NP, Haisch C et al (2009) Combined use of confocal laser scanning microscopy (CLSM) and Raman microscopy (RM): investigations on EPS-matrix. Water Res 43:63-76
78. Böckelmann U, Janke A, Kuhn R et al (2006) Bacterial extracellular DNA forming a defined network like structure. FEMS Microbiol Lett 262:31-38
79. Guiton PS, Hung CS, Kline KA et al (2009) Contribution of autolysin and sortase A during Enterococcus faecalis DNA-dependent biofilm development. Infect Immun 77:3626-3638
80. Jurcisek JA, Bakaletz LO (2007) Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J Bacteriol 189:3868-3875
81. Vilain S, Pretorius JM, Theron J, Brözel VS (2009) DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75:2861-2868
82. Mann EE, Rice KC, Boles BR et al (2009) Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 4:e5822
83. Lappmann M, Claus H, van Alen T et al (2010) A dual role of extracellular DNA during biofilm formation of Neisseria meningitis . Mol Microbiol 75:1355-1371
84. Seper A, Fengler VHI, Roier S et al (2011) Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Mol Microbiol 82:1015-1037
85. Goedeke J, Paul K, Lassak J, Thormann KM (2011) Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1. ISME J 5:613-626
86. Goedeke J, Heun M, Bubendorfer S et al (2011) Roles of two Shewanella oneidensis MR-1 extracellular endonucleases. Appl Environ Microbiol 77:5342-5351
87. Pinchuk GE, Ammons C, Culley DE et al (2008) Utilization of DNA as a sole source of phosphorus, carbon, and energy by Shewanella spp: ecological and physiological implications for dissimilatory metal reduction. Appl Environ Microbiol 74:1198-1208
88. Caldwell DE, Korber DR, Lawrence JR (1992) Confocal laser scanning microscopy and digital image analysis in microbial ecology. Adv Microb Ecol 12:1-67
89. Gorman SP, Mawhinney WM, Adair CG (1993) Confocal laser scanning microscopy ofadherent microorganisms, biofilms and surfaces. In: Denyer SP, Gorman SP, Sussman M (eds) Microbial biofilms: formation and control. Blackwell, London, pp 95-107
90. Manning PA (1995) Use of confocal microscopy in studying bacterial adhesion and invasion. Methods Enzymol 253:159-167
91. Lawrence JR, Korber DR, Wolfaardt GM, Caldwell DE (1996) Analytical imaging and microscopy techniques. In: Hurst CJ, Knudsen GR, McInerney MJ, Stetzenbach LD, Walter MV (eds) Manual of environmental microbiology. ASM, Washington, pp 29-51
92. Lawrence JR, Wolfaardt G, Neu TR (1998) The study of microbial biofilms by confocal laser scanning microscopy. In: Wilkinson MHF, Shut F (eds) Digital image analysis of microbes. Wiley, Chichester, pp 431-465
93. Lawrence JR, Neu TR (1999) Confocal laser scanning microscopy for analysis of microbial biofilms. Methods Enzymol 310:131-144
94. Palmer RJ Jr, Sternberg C (1999) Modern microcopy in biofilm research: confocal microscopy and other approaches. Curr Opin Biotechnol 10:263-268
95. Adair CG, Gorman SP, Byers LB et al (2000) Confocal laser scanning microscopy for examination of microbial biofilms. In: An YH, Friedman RJ (eds) Handbook of bacterial adhesion. Humana, Totowa, pp 249-256
96. Neu TR, Kuhlicke U, Lawrence JR (2002) Assessment of fluorochromes for two-photon laser scanning microscopy biofilms. Appl Environ Microbiol 68:901-909
97. Lawrence JR, Korber DR, Wolfaardt GM et al (2002) Analytical imaging and microscopy techniques. In: Hurst CJ, Crawford RL, Knudsen GR, McInerney MJ, Stetzenbach LD (eds) Manual of environmental microbiology. ASM, Washington, pp 39-61
98. Li Y, Dick WA, Tuovinen OH (2004) Fluorescence microscopy for visualisation of soil microorganisms: a review. Biol Fertil Soils 39:301-311
99. Schmid M, Rothballer M, Assmus B et al (2004) Detection of microbes by scanning confocal laser microscopy (SCLM). In: Kowalchuk GA, Bruijn FJ, Head IM, Akkermans ADL, Elsas JD (eds) Molecular microbial ecology manual. Kluwer Academic Publishers, Dordrecht, pp 875-910
100. Neu TR, Lawrence JR (2005) One-photon versus two-photon laser scanning microscopy and digital image analysis of microbial biofilms. Methods Microbiol 34:87-134
101. Palmer RJ Jr, Haagensen J, Neu TR, Sternberg C (2006) Confocal microscopy of biofilms: spatiotemporal approaches. In: Pawley JB (ed) Handbook of biological confocal microscopy. Springer, New York, pp 882-900
102. Lawrence JR, Korber D, Neu TR (2007) Analytical imaging and microscopy techniques. In: Hurst CJ, Crawford RL, Garland JL, Lipson DA, Mills AL, Stetzenbach LD (eds) Manual of environmental microbiology. ASM, Washington, DC, pp 40-68
103. Lawrence JR, Neu TR (2007) Laser scanning microscopy. In: Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM, Snyder LR (eds) Methods for general and molecular microbiology. ASM, Washington DC, pp 34-53
104. Lawrence JR, Neu TR (2007) Laser scanning microscopy for microbial flocs and particles. In: Wilkinson KJ, Lead JR (eds) Environmental colloids: behavior, structure and characterisation. John Wiley, Chichester, pp 469-505
105. Neu TR, Lawrence JR (2010) Examination of microbial communities on hydrocarbons by means of laser scanning microscopy. In: Timmis KN (ed) Microbiology of hydrocarbons, oils, lipids and derived compounds. Springer, Heidelberg, pp 4073-4084
106. Neu TR, Manz B, Volke F et al (2010) Advanced imaging techniques for assessment of structure, composition and function in biofilm systems. FEMS Microbiol Ecol 72:1-21
107. Brown MJ, Lester JN (1980) Comparison of bacterial extracellular polymer extraction methods. Appl Environ Microbiol 40:179-185
108. Jahn A, Nielsen PH (1995) Extraction of extracellular polymeric substances (EPS) from biofilms using a cation exchange resin. Water Sci Technol 32:157-164
109. Zhang X, Bishop PL, Kinkle BK (1999) Comparison of extraction methods for quantifying extracellular polymers in biofilms. Water Sci Technol 39:211-218
110. Liu H, Fang HHP (2002) Extraction of extracellular polymeric substances (EPS) of sludges. J Biotechnol 95:249-256
111. Comte S, Guibaud G, Baudu M (2006) Relations between extraction protocols for activated sludge extracellular polymeric substances (EPS) and EPS complexation properties: part I. Comparison of the efficiency of eight EPS extraction methods. Enzyme Microb Technol 38:237-245
112. Klock J-H, Wieland A, Seifert R, Michaelis W (2007) Extracellular polymeric substances (EPS) from cyanobacterial mats: characterisation and isolation method optimisation. Marine Biol 152:1077-1085
113. Ras M, Girbal-Neuhauser E, Paul E et al (2008) Protein extraction from activated sludge: an analytical approach. Water Res 42:1867-1878
114. Aguilera A, Souza-Egipsy V, San Martin-Uriz P, Amils R (2008) Extraction of extracellular polymeric substances from extreme acidic microbial biofilms. Appl Microbiol Biotechnol 78:1079-1088
115. Wu J, Xi C (2009) Evaluation of different methods for extracting extracellular DNA from the biofilm matrix. Appl Environ Microbiol 75:5390-5395
116. D’Abzac P, Bordas F, van Hullebusch E et al (2010) Extraction of extracellular polymeric substances (EPS) from anaerobic granular sludge: comparison of chemical and physical extraction protocols. Appl Microbiol Biotechnol 85:1589-1599
117. Wei LL, Wang K, Zhao QL et al (2012) Fractional, biodegradable and spectral characteristics of extracted and fractionated sludge extracellular polymeric substances. Water Res 46:4387-4396
118. Sun M, Li WW, Yu HQ, Harada H (2012) A novel integrated approach to quantitatively evaluate the efficiency of extracellular polymeric substances (EPS) extraction process. Appl Microbiol Biotechnol 96:1577-1585
119. Zhang L, Ren H, Ding L (2012) Comparison of extracellular polymeric substances (EPS) extraction from two different activated sludges. Water Sci Technol 66:1558-1564