Biofouling of reverse osmosis membranes: Positively contributing factors of Sphingomonas

Environmental Science and Technology

Volumn 48, Issue 23, 2014, Pages 13941-13950

  Gutman, Jenia ^a   Herzberg, Moshe ^a   Walker, Sharon L ^b  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b University of California Riverside   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; BIOFILMS; BIOFOULING; CRYSTALS; ESCHERICHIA COLI; QUARTZ CRYSTAL MICROBALANCES; REVERSE OSMOSIS;

CONTRIBUTING FACTOR; CROSSFLOW MEMBRANES; CUMULATIVE IMPACTS; ESCHERICHIA COLI CELLS; EXTRACELLULAR POLYMERIC SUBSTANCES; PSEUDOMONAS AERUGINOSA; QUARTZ CRYSTAL MICROBALANCE WITH DISSIPATION; REAR STAGNATION POINT;

OSMOSIS MEMBRANES;

GLYCOSPHINGOLIPID; POLYAMIDE; ARTIFICIAL MEMBRANE;

ADHESION; BIOFILM; BIOFOULING; COLONIZATION; MEMBRANE; MICROBIAL ACTIVITY; OSMOSIS; POLYMER;

ADHESION; ARTICLE; ARTIFICIAL MEMBRANE; ATOMIC FORCE MICROSCOPY; BACTERIAL COLONIZATION; BACTERIAL OUTER MEMBRANE; BACTERIUM ADHERENCE; BIOFOULING; CARBOHYDRATE ANALYSIS; CELL SURFACE; CHEMICAL COMPOSITION; CONTACT ANGLE; CONTROLLED STUDY; DESALINATION; DESORPTION; ESCHERICHIA COLI; HYDROPHOBICITY; LIPID VESICLE; MEMBRANE REACTOR; NONHUMAN; POLYMERIZATION; PSEUDOMONAS AERUGINOSA; QUARTZ CRYSTAL MICROBALANCE; REVERSE OSMOSIS; SHEAR STRESS; SPHINGOMONAS; SURFACE CHARGE; SURFACE PROPERTY; WATER TREATMENT; BIOFILM; DEVICES; FILTRATION; GROWTH, DEVELOPMENT AND AGING; OSMOSIS; PHYSIOLOGY; PROCEDURES; WATER MANAGEMENT;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA; SPHINGOMONAS; SPHINGOMONAS SP.; SPHINGOMONAS WITTICHII;

BIOFILMS; BIOFOULING; FILTRATION; MEMBRANES, ARTIFICIAL; OSMOSIS; SPHINGOMONAS; WATER PURIFICATION;

EID: 84918790975     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es503680s     Document Type: Article

References (83)

1. LeChevallier, M. W.; Babcock, T. M.; Lee, R. G. Examination and characterization of distribution system biofilms Appl. Environ. Microbiol. 1987, 53 (12) 2714-2724
2. Matin, A.; Khan, Z.; Zaidi, S.; Boyce, M. Biofouling in reverse osmosis membranes for seawater desalination: Phenomena and prevention Desalination 2011, 281, 1-16
3. Ivnitsky, H.; Minz, D.; Kautsky, L.; Preis, A.; Ostfeld, A.; Semiat, R.; Dosoretz, C. G. Biofouling formation and modeling in nanofiltration membranes applied to wastewater treatment J. Membr. Sci. 2010, 360 (1) 165-173
4. Herzberg, M.; Berry, D.; Raskin, L. Impact of microfiltration treatment of secondary wastewater effluent on biofouling of reverse osmosis membranes Water Res. 2010, 44 (1) 167-176
5. Baker, J. S.; Dudley, L. Y. Biofouling in membrane systems - A review∗ 1 Desalination 1998, 118 (1-3) 81-89
6. Ridgway, H. F.; Safarik, J.; District, O. C. W. Biofouling of reverse osmosis membranes. Biofouling and Biocorrosion in Industrial Water Systems; Springer: Berlin, Heidelberg, 1991; pp 81-111.
7. Van Loosdrecht, M.; Lyklema, J.; Norde, W.; Schraa, G.; Zehnder, A. Electrophoretic mobility and hydrophobicity as a measured to predict the initial steps of bacterial adhesion Appl. Environ. Microbiol. 1987, 53 (8) 1898-1901
8. Van Loosdrecht, M.; Lyklema, J.; Norde, W.; Schraa, G.; Zehnder, A. The role of bacterial cell wall hydrophobicity in adhesion Appl. Environ. Microbiol. 1987, 53 (8) 1893-1897
9. Marcus, I. M.; Herzberg, M.; Walker, S. L.; Freger, V. Pseudomonas aeruginosa attachment on QCM-D sensors: The role of cell and surface hydrophobicities Langmuir 2012, 28 (15) 6396-6402
10. Shellenberger, K.; Logan, B. E. Effect of molecular scale roughness of glass beads on colloidal and bacterial deposition Environ. Sci. Technol. 2002, 36 (2) 184-189
11. Yee, N.; Fein, J. B.; Daughney, C. J. Experimental study of the pH, ionic strength, and reversibility behavior of bacteria-mineral adsorption Geochim. Cosmochim. Acta 2000, 64 (4) 609-617
12. Simoni, S. F.; Bosma, T. N.; Harms, H.; Zehnder, A. J. Bivalent cations increase both the subpopulation of adhering bacteria and their adhesion efficiency in sand columns Environ. Sci. Technol. 2000, 34 (6) 1011-1017
13. de Kerchove, A. J.; Elimelech, M. Bacterial swimming motility enhances cell deposition and surface coverage Environ. Sci. Technol. 2008, 42 (12) 4371-4377
14. O'Toole, G. A.; Kolter, R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development Mol. Microbiol. 2002, 30 (2) 295-304
15. Pratt, L. A.; Kolter, R. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili Mol. Microbiol. 1998, 30 (2) 285-293
16. Walker, S. L.; Redman, J. A.; Elimelech, M. Role of cell surface lipopolysaccharides in Escherichia coli K12 adhesion and transport Langmuir 2004, 20 (18) 7736-7746
17. Herzberg, M.; Kang, S.; Elimelech, M. Role of extracellular polymeric substances (EPS) in biofouling of reverse osmosis membranes Environ. Sci. Technol. 2009, 43 (12) 4393-4398
18. Li, B.; Logan, B. E. Bacterial adhesion to glass and metal-oxide surfaces Colloids Surf., B 2004, 36 (2) 81-90
19. Lau, P. C. Y.; Lindhout, T.; Beveridge, T. J.; Dutcher, J. R.; Lam, J. S. Differential lipopolysaccharide core capping leads to quantitative and correlated modifications of mechanical and structural properties in Pseudomonas aeruginosa biofilms J. Bacteriol. 2009, 191 (21) 6618-6631
20. Rietschel, E. T.; Brade, H.; Holst, O.; Brade, L.; Müller-Loennies, S.; Mamat, U.; Zähringer, U.; Beckmann, F.; Seydel, U.; Brandenburg, K. Bacterial endotoxin: chemical constitution, biological recognition, host response, and immunological detoxification. Pathology of septic shock; Springer: 1996; pp 39-81.
21. Flemming, H. C.; Wingender, J. The biofilm matrix Nat. Rev. Microbiol. 2010, 8 (9) 623-633
22. Arbel, R. The effect of biofouling on mineral scaling in reverse osmosis operation. Master Thesis, Environmental Engineering; Ben Gurion University of the Negev, 2010.
23. Subramani, A.; Hoek, E. Direct observation of initial microbial deposition onto reverse osmosis and nanofiltration membranes J. Membr. Sci. 2008, 319 (1-2) 111-125
24. Vigeant, M. A. S.; Ford, R. M.; Wagner, M.; Tamm, L. K. Reversible and irreversible adhesion of motile Escherichia coli cells analyzed by total internal reflection aqueous fluorescence microscopy Appl. Environ. Microbiol. 2002, 68 (6) 2794
25. Koskinen, R.; Ali-Vehmas, T.; Kämpfer, P.; Laurikkala, M.; Tsitko, I.; Kostyal, E.; Atroshi, F.; Salkinoja-Salonen, M. Characterization of Sphingomonas isolates from Finnish and Swedish drinking water distribution systems J. Appl. Microbiol. 2001, 89 (4) 687-696
26. Bereschenko, L.; Stams, A.; Euverink, G.; van Loosdrecht, M. Biofilm formation on reverse osmosis membranes is initiated and dominated by Sphingomonas spp Appl. Environ. Microbiol. 2010, 76 (8) 2623-2632
27. Ivnitsky, H.; Katz, I.; Minz, D.; Volvovic, G.; Shimoni, E.; Kesselman, E.; Semiat, R.; Dosoretz, C. G. Bacterial community composition and structure of biofilms developing on nanofiltration membranes applied to wastewater treatment Water Res. 2007, 41 (17) 3924-3935
28. Khambhaty, Y.; Plumb, J. Characterization of bacterial population associated with a brackish water desalination membrane Desalination 2011, 269 (1) 35-40
29. Huang, L. N.; De Wever, H.; Diels, L. Diverse and distinct bacterial communities induced biofilm fouling in membrane bioreactors operated under different conditions Environ. Sci. Technol. 2008, 42 (22) 8360-8366
30. Neef, A.; Witzenberger, R.; Kämpfer, P. Detection of sphingomonads and in situ identification in activated sludge using 16S rRNA-targeted oligonucleotide probes J. Indust. Microbiol. Biotechnol. 1999, 23 (4) 261-267
31. Bereschenko, L.; Heilig, G.; Nederlof, M.; van Loosdrecht, M.; Stams, A.; Euverink, G. Molecular characterization of the bacterial communities in the different compartments of a full-scale reverse-osmosis water purification plant Appl. Environ. Microbiol. 2008, 74 (17) 5297-5304
32. Al Ashhab, A.; Herzberg, M.; Gillor, O. Biofouling of reverse-osmosis membranes during tertiary wastewater desalination: microbial community composition Water Res. 2013, 50, 341-349
33. Fujioka, T.; Khan, S. J.; Poussade, Y.; Drewes, J. E.; Nghiem, L. D. N-nitrosamine removal by reverse osmosis for indirect potable water reuse-A critical review based on observations from laboratory-, pilot-and full-scale studies Sep. Purif. Technol. 2012, 98, 503-515
34. Kawahara, K.; Kuraishi, H.; Zähringer, U. Chemical structure and function of glycosphingolipids of Sphingomonas spp and their distribution among members of the α-4 subclass of proteobacteria J. Indust. Microbiol. Biotechnol. 1999, 23 (4-5) 408-413
35. Kawahara, K.; Seydel, U.; Matsuura, M.; Danbara, H.; Rietschel, E. T. Chemical structure of glycosphingolipids isolated from Sphingomonas paucimobilis FEBS Lett. 1991, 292 (1) 107-110
36. Wiese, A.; Seydel, U. Interaction of peptides and proteins with bacterial surface glycolipids: a comparison of glycosphingolipids and lipopolysaccharides J. Ind. Microbiol. Biotechnol. 1999, 23 (4) 414-424
37. Wiese, A.; Reiners, J. O.; Brandenburg, K.; Kawahara, K.; Zähringer, U.; Seydel, U. Planar asymmetric lipid bilayers of glycosphingolipid or lipopolysaccharide on one side and phospholipids on the other: membrane potential, porin function, and complement activation Biophys. J. 1996, 70 (1) 321-329
38. Yin, A. B.; Hawke, D.; Zhou, D. Mass spectrometric analysis of glycosphingolipid antigens JoVE (Journal of Visualized Experiments) 2013, 74, e4224-e4224
39. Gutman, J.; Kaufman, Y.; Kawahara, K.; Walker, S. L.; Freger, V.; Herzberg, M. The interactions of glycosphingolipids and lipopolysaccharides with silica and polyamide surfaces: Adsorption and viscoelastic properties Biomacromolecules 2014, 15 (6) 2128-2137
40. Gutsmann, T.; Seydel, U. Impact of the glycostructure of amphiphilic membrane components on the function of the outer membrane of Gram-negative bacteria as a matrix for incorporated channels and a target for antimicrobial peptides or proteins Eur. J. Cell Biol. 2010, 89 (1) 11-23
41. Pang, C. M.; Hong, P.; Guo, H.; Liu, W. T. Biofilm formation characteristics of bacterial isolates retrieved from a reverse osmosis membrane Environ. Sci. Technol. 2005, 39 (19) 7541-7550
42. Rodahl, M.; Höök, F.; Fredriksson, C.; Keller, C. A.; Krozer, A.; Brzezinski, P.; Voinova, M.; Kasemo, B. Simultaneous frequency and dissipation factor QCM measurements of biomolecular adsorption and cell adhesion Faraday Discuss. 1997, 107, 229-246
43. Walker, S. L. The role of nutrient presence on the adhesion kinetics of Burkholderia cepacia G4g and ENV435g Colloid Surface B 2005, 45 (3-4) 181-188
44. Ying, W.; Gitis, V.; Herzberg, M. Effects of shear rate on biofouling of reverse osmosis membrane during tertiary wastewater desalination J. Membr. Sci. 2012, 427, 390-398
45. Durfee, T.; Nelson, R.; Baldwin, S.; Plunkett, G.; Burland, V.; Mau, B.; Petrosino, J. F.; Qin, X.; Muzny, D. M.; Ayele, M. The complete genome sequence of Escherichia coli DH10B: insights into the biology of a laboratory workhorse J. Bacteriol. 2008, 190 (7) 2597-2606
46. Davies, D. G.; Parsek, M. R.; Pearson, J. P.; Iglewski, B. H.; Costerton, J.; Greenberg, E. The involvement of cell-to-cell signals in the development of a bacterial biofilm Science 1998, 280 (5361) 295-298
47. Kirby, B. J.; Hasselbrink, E. F. Zeta potential of microfluidic substrates: 2. Data for polymers Electrophoresis 2004, 25 (2) 203-213
48. Ying, W.; Gitis, V.; Lee, J.; Herzberg, M. Effects of shear rate on biofouling of reverse osmosis membrane during tertiary wastewater desalination J. Membr. Sci. 2013, 427, 390-398
49. Orgad, O.; Oren, Y.; Walker, S. L.; Herzberg, M. The role of alginate in Pseudomonas aeruginosa EPS adherence, viscoelastic properties and cell attachment Biofouling 2011, 27 (7) 787-798
50. Liu, H.; Fang, H. H. P. Extraction of extracellular polymeric substances (EPS) of sludges J. Biotechnol. 2002, 95 (3) 249-256
51. Redman, J. A.; Walker, S. L.; Elimelech, M. Bacterial adhesion and transport in porous media: Role of the secondary energy minimum Environ. Sci. Technol. 2004, 38 (6) 1777-1785
52. Tong, J.; McIntosh, T. J. Structure of supported bilayers composed of lipopolysaccharides and bacterial phospholipids: raft formation and implications for bacterial resistance Biophys. J. 2004, 86 (6) 3759-3771
53. de Kerchove, A. J.; Weronski, P.; Elimelech, M. Adhesion of nonmotile Pseudomonas aeruginosa on "soft" polyelectrolyte layer in a radial stagnation point flow system: Measurements and model predictions Langmuir 2007, 23 (24) 12301-12308
54. Rijnaarts, H. H.; Norde, W.; Lyklema, J.; Zehnder, A. J. The isoelectric point of bacteria as an indicator for the presence of cell surface polymers that inhibit adhesion Colloid Surface B 1995, 4 (4) 191-197
55. Lee, S.; Ang, W. S.; Elimelech, M. Fouling of reverse osmosis membranes by hydrophilic organic matter: implications for water reuse Desalination 2006, 187 (1) 313-321
56. Herzberg, M.; Elimelech, M. Biofouling of reverse osmosis membranes: role of biofilm-enhanced osmotic pressure J. Membr. Sci. 2007, 295 (1-2) 11-20
57. Ying, W.; Yang, F.; Bick, A.; Oron, G.; Herzberg, M. Extracellular polymeric substances (EPS) in a hybrid growth membrane bioreactor (HG-MBR): viscoelastic and adherence characteristics Environ. Sci. Technol. 2010, 44 (22) 8636-8643
58. Sweity, A.; Ying, W.; Belfer, S.; Oron, G.; Herzberg, M. pH effects on the adherence and fouling propensity of extracellular polymeric substances in a membrane bioreactor J. Membr. Sci. 2011, 378 (1) 186-193
59. Raaijmakers, J. M.; Weller, D. M.; Thomashow, L. S. Frequency of antibiotic-producing Pseudomonas spp. in natural environments Appl. Environ. Microbiol. 1997, 63 (3) 881-887
60. Wolfgang, M. C.; Kulasekara, B. R.; Liang, X.; Boyd, D.; Wu, K.; Yang, Q.; Miyada, C. G.; Lory, S. Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (14) 8484-8489
61. Gómez-Suárez, C.; Pasma, J.; van der Borden, A. J.; Wingender, J.; Flemming, H.; Busscher, H. J.; van der Mei, H. C. Influence of extracellular polymeric substances on deposition and redeposition of Pseudomonas aeruginosa to surfaces Microbiology 2002, 148 (4) 1161-1169
62. Hentzer, M.; Teitzel, G. M.; Balzer, G. J.; Heydorn, A.; Molin, S.; Givskov, M.; Parsek, M. R. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function J. Bacteriol. 2001, 183 (18) 5395-5401
63. Govan, J. R.; Deretic, V. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia Microbiol. Rev. 1996, 60 (3) 539-574
64. Kawahara, K.; Moll, H.; Knirel, Y. A.; Seydel, U.; Zähringer, U. Structural analysis of two glycosphingolipids from the lipopolysaccharide-lacking bacterium Sphingomonas capsulata Eur. J. Biochem. 2000, 267 (6) 1837-1846
65. Schultheis, E.; Dreger, M. A.; Nimtz, M.; Wray, V.; Hempel, D. C.; Nörtemann, B. Structural characterization of the exopolysaccharide PS-EDIV from Sphingomonas pituitosa strain DSM 13101 Appl. Microbiol. Biotechnol. 2008, 78 (6) 1017-1024
66. Sutherland, I. W. Biofilm exopolysaccharides: a strong and sticky framework Microbiology 2001, 147 (1) 3-9
67. Williams, V.; Fletcher, M. Pseudomonas fluorescens adhesion and transport through porous media are affected by lipopolysaccharide composition Appl. Environ. Microbiol. 1996, 62 (1) 100-104
68. Hermansson, M.; Kjelleberg, S.; Korhonen, T. K.; Stenström, T. Hydrophobic and electrostatic characterization of surface structures of bacteria and its relationship to adhesion to an air-water interface Arch. Microbiol. 1982, 131 (4) 308-312
69. Magnusson, K.; Johansson, G. Probing the surface of Salmonella typhimurium and Salmonella minnesota SR and R bacteria by aqueous biphasic partitioning in systems containing hydrophobic and charged polymers FEMS Microbiol. Lett. 1977, 2 (4) 225-228
70. Azeredo, J.; Oliveira, R. The role of exopolymers in the attachment of Sphingomonas paucimobilis Biofouling 2000, 16 (1) 59-67
71. Wozniak, D. J.; Wyckoff, T. J.; Starkey, M.; Keyser, R.; Azadi, P.; O'Toole, G. A.; Parsek, M. R. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (13) 7907-7912
72. Ashtaputre, A. A.; Shah, A. K. Studies on a Viscous, Gel-forming exopolysaccharide from Sphingomonas paucimobilis GS1 Appl. Environ. Microbiol. 1995, 61 (3) 1159-1162
73. Pollock, T. J.; van Workum, W. A.; Thorne, L.; Mikolajczak, M. J.; Yamazaki, M.; Kijne, J. W.; Armentrout, R. W. Assignment of biochemical functions to glycosyl transferase genes which are essential for biosynthesis of exopolysaccharides in Sphingomonas strain S88 and Rhizobium leguminosarum J. Bacteriol. 1998, 180 (3) 586-593
74. Nivens, D. E.; Ohman, D. E.; Williams, J.; Franklin, M. J. Role of alginate and its O acetylation in formation of Pseudomonas aeruginosa microcolonies and biofilms J. Bacteriol. 2001, 183 (3) 1047-1057
75. Nanci, A.; Wuest, J.; Peru, L.; Brunet, P.; Sharma, V.; Zalzal, S.; McKee, M. Chemical modification of titanium surfaces for covalent attachment of biological molecules J. Biomed. Mater. Res. 1998, 40 (2) 324-335
76. Parak, W. J.; Gerion, D.; Zanchet, D.; Woerz, A. S.; Pellegrino, T.; Micheel, C.; Williams, S. C.; Seitz, M.; Bruehl, R. E.; Bryant, Z. Conjugation of DNA to silanized colloidal semiconductor nanocrystalline quantum dots Chem. Mater. 2002, 14 (5) 2113-2119
77. Nohynek, L. J.; Suhonen, E. L.; Nurmiaho-Lassila, E.; Hantula, J.; Salkinoja-Salonen, M. Description of four pentachlorophenol-degrading bacterial strains as Sphingomonas chlorophenolica sp. nov Syst. Appl. Microbiol. 1995, 18 (4) 527-538
78. Gutman, J.; Walker, S. L.; Freger, V.; Herzberg, M. Bacterial attachment and viscoelasticity: Physicochemical and motility effects analyzed with QCM-D Environ. Sci. Technol. 2012, 47 (1) 398-404
79. Heydorn, A.; Ersbøll, B.; Kato, J.; Hentzer, M.; Parsek, M. R.; Tolker-Nielsen, T.; Givskov, M.; Molin, S. Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression Appl. Environ. Microbiol. 2002, 68 (4) 2008-2017
80. Varela, R. P. A.; Gonçalves da Silva, M. P. S.; Amélia; Fedorov, A.; Futerman, H. A.; Prieto, M.; Silva, C. L. Effect of glucosylceramide on the biophysical properties of fluid membranes Biochim. Biophys. Acta 2013, 1828, 1122-1300
81. Silva, L. C.; Futerman, A. H.; Prieto, M. Lipid raft composition modulates sphingomyelinase activity and ceramide-induced membrane physical alterations Biophys. J. 2009, 96 (8) 3210-3222
82. James, G.; Beaudette, L.; Costerton, J. Interspecies bacterial interactions in biofilms J. Ind. Microbiol. 1995, 15 (4) 257-262
83. Skillman, L.; Sutherland, I.; Jones, M. The role of exopolysaccharides in dual species biofilm development J. Appl. Microbiol. 1998, 85 (S1) 13S-18S