Extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms: Characterization by infrared spectroscopy and proteomics

Environmental Microbiology

Volumn 13, Issue 4, 2011, Pages 1018-1031

  Cao, Bin ^a   Shi, Liang ^b   Brown, Roslyn N ^b   Xiong, Yijia ^b   Fredrickson, Jim K ^b   Romine, Margaret F ^b   Marshall, Matthew J ^b   Lipton, Mary S ^b   Beyenal, Haluk ^a  

^a Washington State University   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYTOCHROME C; MEMBRANE PROTEIN; POLYMER;

ARTICLE; BIOFILM; BIOREACTOR; CHEMISTRY; ELECTRON TRANSPORT; EXTRACELLULAR SPACE; INFRARED SPECTROSCOPY; LIQUID CHROMATOGRAPHY; OXIDATION REDUCTION REACTION; PROTEOMICS; SHEWANELLA; TANDEM MASS SPECTROMETRY;

BACTERIAL PROTEINS; BIOFILMS; BIOREACTORS; CHROMATOGRAPHY, LIQUID; CYTOCHROME C GROUP; ELECTRON TRANSPORT; EXTRACELLULAR SPACE; MEMBRANE PROTEINS; OXIDATION-REDUCTION; POLYMERS; PROTEOMICS; SHEWANELLA; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TANDEM MASS SPECTROMETRY;

SHEWANELLA; SHEWANELLA ONEIDENSIS; SHEWANELLA ONEIDENSIS MR-1; SHEWANELLA SP.;

EID: 79953277727     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02407.x     Document Type: Article

References (98)

1. Adkins, J., Mottaz, H., Norbeck, A., Gustin, J., Rue, J., Clauss, T., etal. (2006) Analysis of the Salmonella typhimurium proteome through environmental response toward infectious conditions. Mol Cell Proteomics 5: 1450-1461.
2. Aguilera, A., Souza-Egipsy, V., San Martin-Uriz, P., and Amils, R. (2008) Extraction of extracellular polymeric substances from extreme acidic microbial biofilms. Appl Microbiol Biotechnol 78: 1079-1088.
3. Allensen-Holm, M., Barken, K., Yang, L., Klausen, M., Webb, J., Kjelleberg, S., etal. (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59: 1114-1128.
4. Badireddy, A., Korpol, B., Chellam, S., Gassman, P., Engelhard, M., Lea, A., and Rosso, K. (2008) Spectroscopic characterization of extracellular polymeric substances from Escherichia coli and Serratia marcescens: suppression using subinhibitory concentrations of bismuth thiols. Biomacromolecules 9: 3079-3089.
5. Baker, M., Lalonde, S., Konhauser, K., and Foght, J. (2010) Role of extracellular polymeric substances in the surface chemical reactivity of Hymenobacter aerophilus, a psychrotolerant bacterium. Appl Environ Microbiol 76: 102-109.
6. Battin, T., Wille, A., Sattler, B., and Psenner, R. (2001) Phylogenetic and functional heterogeneity of sediment biofilms along environmental gradients in a glacial stream. Appl Environ Microbiol 67: 799-807.
7. Beliaev, A., and Saffarini, D. (1998) Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J Bacteriol 180: 6292-6297.
8. Beliaev, A., Saffarini, D., McLaughlin, J., and Hunnicutt, D. (2001) MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol Microbiol 39: 722-730.
9. Brown, R., Romine, M., Schepmoes, A., Smith, R., and Lipton, M. (2010) Mapping the subcellular proteome of Shewanella oneidensis MR-1 using Sarkosyl-based fractionation and LC-MS/MS protein identification. J Proteome Res 9: 4454-4463.
10. Burgos, W., McDonough, J., Senko, J., Zhang, G., Dohnalkova, A., Kelly, S., etal. (2008) Characterization of uraninite nanoparticles produced by Shewanella oneidensis MR-1. Geochim Cosmochim Acta 72: 4901-4915.
11. Burns, J., Ginn, B., Bates, D., Dublin, S., Taylor, J., Apkarian, R., etal. (2010) Outer membrane-associated serine protease involved in adhesion of Shewanella oneidensis to Fe(III) oxides. Environ Sci Technol 44: 68-73.
12. von Canstein, H., Ogawa, J., Shimizu, S., and Lloyd, J. (2008) Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 74: 615-623.
13. Comte, S., Guibaud, G., and Baudu, M. (2006a) 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.
14. Comte, S., Guibaud, G., and Baudu, M. (2006b) Biosorption properties of extracellular polymeric substances (EPS) resulting from activated sludge according to their type: soluble or bound. Process Biochem 41: 815-823.
15. Coursolle, D., Baron, D., Bond, D., and Gralnick, J. (2010) The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. J Bacteriol 192: 467-474.
16. Cucarella, C., Solano, C., Valle, J., Amorena, B., Lasa, I., and Penades, J. (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183: 2888-2896.
17. D'Abzac, P., Bordas, F., Joussein, E., Hullebusch, E., Lens, P., and Guibaud, G. (2010) Characterization of the mineral fraction associated to extracellular polymeric substances (EPS) in anaerobic granular sludges. Environ Sci Technol 44: 412-418.
18. Davies, D. (1999) Regulation of matrix polymer in biofilm formation and dispersion. In Microbial Extracellular Polymeric Substances: Characterization, Structure and Function. Wingender, J., Neu, T., and Flemming, H. (eds). Berlin, Germany: Springer, pp. 93-117.
19. Eboigbodin, K.E., and Biggs, C.A. (2008) Characterization of the extracellular polymeric substances produced by Escherichia coli using infrared spectroscopic, proteomic, and aggregation studies. Biomacromolecules 9: 686-695.
20. Eggleston, C., Voros, J., Shi, L., Lower, B., Droubay, T., and Colberg, P. (2008) Binding and direct electrochemistry of OmcA, an outer-membrane cytochrome from an iron reducing bacterium, with oxide electrode: a candidate biofuel cell system. Inorg Chim Acta 361: 769-777.
21. Flemming, H. (1995) Sorption sites in biofilms. Water Sci Technol 32: 27-33.
22. Flemming, H., and Wingender, J. (2001) Relevance of microbial extracellular polymeric substances (EPSs): part I. Structural and ecological aspects. Water Sci Technol 43: 1-8.
23. Flemming, H., and Wingender, J. (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
24. Fournier, E. (2001) Colorimetric quantification of carbohydrates. In Current Protocols in Food Analytical Chemistry. Wrolstad, R.E. (ed.). Hoboken, NJ, USA: John Wiley and Sons, E1.1.1-E1.1.8.
25. Fredrickson, J., and Zachara, J. (2008) Electron transfer at the microbe-mineral interface: a grand challenge in biogeochemistry. Geobiology 6: 245-253.
26. Fredrickson, J., Zachara, J., Kennedy, D., Liu, C., Duff, M., Hunter, D., and Dohnalkova, A. (2002) Influence of Mn oxides on the reduction of uranium(VI) by the metal-reducing bacterium Shewanella putrefaciens. Geochim Cosmochim Acta 66: 3247-3262.
27. Freitas, F., Alves, V., Pais, J., Costa, N., Oliveira, C., Mafra, L., etal. (2009) Characterization of an extracellular polymeric polysaccharide produced by a Pseudomonas strain grown on glycerol. Bioresour Technol 100: 859-865.
28. Gong, A.S., Bolster, C.H., Benavides, M., and Walker, S.L. (2009) Extraction and analysis of extracellular polymeric substances: comparison of methods and extracellular polymeric substance levels in Salmonella pullorum SA1685. Environ Eng Sci 26: 1523-1532.
29. Ha, J., Gelabert, A., Spormann, A.M., and Brown, G.E. (2010) Role of extracellular polymeric substances in metal ion complexation on Shewanella oneidensis: batch uptake, thermodynamic modeling, ATR-FTIR, and EXAFS study. Geochim Cosmochim Acta 74: 1-15.
30. Hartshorne, R., Reardon, C., Ross, D., Nuester, J., Clarke, T., Gates, A., etal. (2009) Characterization of an electron conduit between bacteria and the extracellular environment. Proc Natl Acad Sci USA 106: 22169-22174.
31. Heidelberg, J.F., Paulsen, I.T., Nelson, K.E., Gaidos, E.J., Nelson, W.C., Read, T.D., etal. (2002) Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol 20: 1118-1123.
32. Hinsa, S., Espinosa-Urgel, M., Ramos, J., and O'Toole, G. (2003) Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49: 905-918.
33. Huber, B., Riedel, K., Kothe, M., Givskov, M., Molin, S., and Eberl, L. (2002) Genetic analysis of functions involved in the late stages of biofilm development in Burkholderia cepacia H111. Mol Microbiol 46: 411-426.
34. Inoue, K., Leang, C., Franks, A., Woodard, T., Nevin, K., and Lovley, D. (2010) Specific localization of the c-type cytochrome OmcZ at the anode surface in current-producing biofilms of Geobacter sulfurreducens. Environ Microbiol Rep (in press): doi: 10.1111/j.1758-2229.2010.00210.x.
35. Jiao, Y., Cody, G., Harding, A., Wilmes, P., Schrenk, M., Wheeler, K., etal. (2010) Characterization of extracellular polymeric substances from Acidophilic microbial biofilms. Appl Environ Microbiol 76: 2916-2922.
36. Jones, D., Tobler, D., Schaperdoth, T., Mainiero, M., and Macalady, J. (2010) Community structure of subsurface biofilms in the thermal sulfidic caves of Acquasanta Terme, Italy. Appl Environ Microbiol 76: 5902-5910.
37. Joshi, P., and Juwarkar, A. (2009) In vivo studies to elucidate the role of extracellular polymeric substances from Azotobacter in immobilization of heavy metals. Environ Sci Technol 43: 5884-5889.
38. Kachlany, S., Levery, S., Kim, J., Reuhs, B., Lion, L., and Ghiorse, W. (2001) Structure and carbohydrate analysis of the exopolysaccharide capsule of Pseudomonas putida G7. Environ Microbiol 3: 774-784.
39. Kerisit, S., Rosso, K., Dupuis, M., and Valiev, M. (2007) Molecular computational investigation of electron-transfer kinetics across cytochrome-iron oxide interfaces. J Phys Chem C 111: 11363-11375.
40. Kieft, T., Fredrickson, J., Onstott, T., Gorby, Y., Kostandarithes, H., Bailey, T., etal. (1999) Dissimilatory reduction of Fe(III) and other electron acceptors by a Thermus isolate. Appl Environ Microbiol 65: 1214-1221.
41. Laspidou, C., and Rittmann, B. (2002) A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass. Water Res 36: 2711-2720.
42. Latasa, C., Roux, A., Toledo-Arana, A., Ghigo, J., Gamazo, C., Penades, J., and Lasa, I. (2005) BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58: 1322-1339.
43. Leang, C., Qian, X., Mester, T., and Lovley, D. (2010) Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl Environ Microbiol 76: 4080-4084.
44. Lee, H.-K., Ahn, M.-J., Kwak, S.-H., Song, W.-H., and Jeong, B.-C. (2003) Purification and characterization of cold active lipase from psychrotropic Aeromonas sp. LPB 4. J Microbiol 41: 22-27.
45. Liu, C., Zachara, J., Gorby, Y., Szecsody, J., and Brown, C. (2001) Microbial reduction of Fe(III) and sorption/precipitation of Fe(II) on Shewanella putrefaciens strain CN32. Environ Sci Technol 35: 1385-1393.
46. Liu, C., Gorby, Y., Zachara, J., Fredrickson, J., and Brown, C. (2002) Reduction kinetics of Fe(III), Co(III), U(VI), Cr(VI), and Tc(VII) in cultures of dissimilatory metal-reducing bacteria. Biotechnol Bioeng 80: 637-649.
47. Liu, H., and Fang, H. (2002) Extraction of extracellular polymeric substances (EPS) of sludges. J Biotechnol 95: 249-256.
48. Lower, B., Shi, L., Yongsunthon, R., Droubay, T., McCready, D., and Lower, S. (2007) Specific bonds between an iron oxide surface and outer membrane cytochromes MtrC and OmcA from Shewanella oneidensis MR-1. J Bacteriol 189: 4944-4952.
49. Lower, B., Lins, R., Oestreicher, Z., Straatsma, T., Hochella, M., Shi, L., and Lower, S. (2008) In vitro evolution of a peptide with a hematite binding motif that may constitute a natural metal-oxide binding archetype. Environ Sci Technol 42: 3821-3827.
50. Lower, B., Youngsunthon, R., Shi, L., Wildling, L., Gruber, H., Wigginton, N., etal. (2009) Antibody recognition force microscopy shows that outer membrane cytochromes OmcA and MtrC are expressed on the exterior surface of Shewanella oneidensis MR-1. Appl Environ Microbiol 75: 2931-2935.
51. McLean, J., Pinchuk, G., Geydebrekht, O., Bilskis, C., Zakrajsek, B., Hill, E., etal. (2008a) Oxygen-dependent autoaggregation in Shewanella oneidensis MR-1. Environ Microbiol 10: 1861-1876.
52. McLean, J., Ona, O., and Majors, P. (2008b) Correlated biofilm imaging, transport and metabolism measurements via combined nuclear magnetic resonance and confocal microscopy. ISME J 2: 121-131.
53. Marshall, M., Beliaev, A., Dohnalkova, A., Kennedy, D., Shi, L., Wang, Z., etal. (2006) c-Type cytochrome-dependent formation of U(IV) nanoparticles by Shewanella oneidensis. PLoS Biol 4: 1324-1333.
54. Marsili, E., Baron, D., Shikhare, I., Coursolle, D., Gralnick, J., and Bond, D. (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Nat Acad Sci USA 105: 3968-3973.
55. 13C CPMAS NMR spectroscopy. Appl Microbiol Biotechnol 85: 197-206.
56. Myers, C., and Myers, J. (1997) Outer membrane cytochromes of Shewanella putrefaciens MR-1: spectral analysis, and purification of the 83-kDa c-type cytochrome. Biochim Biophys Acta 1326: 307-318.
57. Myers, C., and Myers, J. (2003) Cell surface exposure of the outer membrane cytochromes of Shewanella oneidensis MR-1. Lett Appl Microbiol 37: 254-258.
58. Myers, J., and Myers, C. (1998) Isolation and sequence of omcA, a gene encoding a decaheme outer membrane cytochrome c of Shewanella putrefaciens MR-1, and detection of omcA homologs in other strains of S. putrefaciens. Biochim Biophys Acta 1371: 237-251.
59. Myszka, K., and Czaczyk, K. (2009) Characterization of adhesive exopolysaccaride (EPS) produced by Pseudomonas aeruginosa under starvation conditions. Curr Microbiol 58: 541-546.
60. Ni, B.J., Fang, F., Xie, W.M., Sun, M., Sheng, G.P., Li, W.H., and Yu, H.Q. (2009) Characterization of extracellular polymeric substances produced by mixed microorganisms in activated sludge with gel-permeating chromatography, excitation-emission matrix fluorescence spectroscopy measurement and kinetic modeling. Water Res 43: 1350-1358.
61. Nielsen, P., Jahn, A., and Palmgren, R. (1997) Conceptual model for production of exopolymers in biofilms. Water Sci Technol 36: 11-19.
62. Peng, J., Elias, J., Thoreen, C., Licklider, L., and Gygi, S. (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2: 43-50.
63. Pinchuk, G., Ammons, C., Culley, D., Li, S.-M., McLean, J., Romine, M., etal. (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.
64. Reardon, C., Dohnalkova, A., Nachimuthu, P., Kennedy, D., Saffarini, D., Arey, B., etal. (2010) Role of outer-membrane cytochromes MtrC and OmcA in the biomineralization of ferrihydrite by Shewanella oneidensis MR-1. Geobiology 8: 56-68.
65. Reguera, G., McCarthy, K., Mehta, T., Nicoll, J., Touminen, M., and Lovley, D. (2005) Extracellular electron transfer via microbial nanowires. Nature 435: 1098-1101.
66. Reguera, G., Nevin, K., Nicoll, J., Covalla, S., Woodard, T., and Lovley, D. (2006) Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl Environ Microbiol 72: 7345-7348.
67. Reguera, G., Pollina, R., Nicoll, J., and Lovley, D. (2007) Possible nonconductive role of Geobacter sulfurreducens pilus nanowires in biofilm formation. J Bacteriol 189: 2125-2127.
68. Ross, D., Ruebush, S., Brantley, S., Hartshorne, R., Clarke, T., Richardson, D., and Tien, M. (2007) Characterization of protein-protein interactions involved in iron reduction by Shewanella oneidensis MR-1. Appl Environ Microbiol 73: 5797-5808.
69. Roux, A., Beloin, C., and Ghigo, J. (2005) Combined inactivation and expression strategy to study gene function under physiological conditions: application to identification of new Escherichia coli adhesins. J Bacteriol 187: 1001-1013.
70. Saville, R., Dieckmann, N., and Spormann, A. (2010) Spatiotemporal activity of the mshA gene system in Shewanella oneidensis MR-1 biofilms. FEMS Microbiol Lett 308: 76-83.
71. van Schaik, E., Giltner, C., Audette, G., Keizer, D., Bautista, D., Slupsky, C., etal. (2005) DNA binding: a novel function of Pseudomonas aeruginosa type IV pili. J Bacteriol 187: 1455-1464.
72. Schmitt, J., and Flemming, H. (1998) FTIR-spectroscopy in microbial and material analysis. Int Biodeterior Biodegradation 41: 1-11.
73. Sheng, G.-P., Yu, H.-Q., and Yu, Z. (2005) Extraction of extracellular polymeric substances from the photosynthetic bacterium Rhodopseudomonas acidophila. Appl Microbiol Biotechnol 67: 125-130.
74. Sheng, G.-P., Yu, H.-Q., and Li, X.-Y. (2010) Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnol Adv 28: 882-894.
75. Shi, L., Squier, T., Zachara, J., and Fredrickson, J. (2007) Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol Microbiol 65: 12-20.
76. Shi, L., Deng, S., Marshall, M., Wang, Z., Kennedy, D., Dohnalkova, A., etal. (2008) Direct involvement of type II secretion system in extracellular translocation of Shewanella oneidensis outer membrane cytochromes MtrC and OmcA. J Bacteriol 190: 5512-5516.
77. Shi, L., Richardson, D., Wang, Z., Kerisit, S., Rosso, K., Zachara, J., and Fredrickson, J. (2009) The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ Microbiol Rep 1: 220-227.
78. Siezen, R., Renchens, B., and Boekhorst, J. (2007) Evolution of prokaryotic subtilases: genome-wide analysis reveals novel subfamilies with different catalytic residues. Proteins 67: 681-694.
79. Suzuki, Y., Kitatsuji, Y., Ohnuki, T., and Tsujimura, S. (2010) Flavin mononucleotide mediated electron pathway for microbial U(VI) reduction. Phys Chem Chem Phys 12: 10081-10087.
80. Tapia, J., Munoz, J., Gonzalez, F., Blazquez, M., Malki, M., and Ballester, A. (2009) Extraction of extracellular polymeric substances from the acidophilic bacterium Acidiphilium 3.2Sup(5). Water Sci Technol 59: 1959-1967.
81. Theunissen, S., De Smet, L., Dansercoer, A., Motte, B., Coenye, T., Van Beeumen, J., etal. (2010) The 285kDa Bap/RTX hybrid cell surface protein (SO4317) of Shewanella oneidensis MR-1 is a key mediator of biofilm formation. Res Microbiol 161: 144-152.
82. Thomas, P., Ryan, D., and Levin, W. (1976) An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal Biochem 75: 168-176.
83. Thormann, K., Saville, R., Shukla, S., and Pelletier, D. (2004) Initial phases of biofilm formation in Shewanella oneidensis MR-1. Appl Environ Microbiol 186: 8096-8104.
84. Toledo-Arana, A., Valle, J., Solano, C., Arrizubieta, M., Cucarella, C., Lamata, M., etal. (2001) The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl Environ Microbiol 67: 4538-4545.
85. Tormo, M., Knecht, E., Gotz, F., Lasa, I., and Penades, J. (2005) Bap-dependent biofilm formation by pathogenic species of Staphylococcus: evidence of horizontal gene transfer? Microbiology 151: 2465-2475.
86. Turse, J., Marshall, M., Fredrickson, J., Lipton, M., and Callister, S. (2010) An empirical strategy for characterizing bacterial proteomes across species in the absence of genomic sequences. PLoS ONE 5: e13968.
87. Ueshima, M., Ginn, B., Haack, E., Szymanowski, J., and Fein, J. (2008) Cd adsorption onto Pseudomonas putida in the presence and absence of extracellular polymeric substances. Geochim Cosmochim Acta 72: 5885-5898.
88. Urrutia, M., Roden, E., Fredrickson, J., and Zachara, J. (1998) Microbial and surface chemistry controls on reduction of synthetic Fe(III) oxide minerals by the dissimilatory iron-reducing bacterium Shewanella alga. Geomicrobiol J 15: 269-291.
89. Washburn, M., Wolters, D., and Yates, J., III (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19: 242-247.
90. Weidler, G., Dornmayr-Pfaffenhuemer, M., Gerbl, F., Heinen, W., and Stan-Lotter, H. (2007) Communities of archaea and bacteria in a subsurface radioactive thermal spring in the Autrian Central Alps, and evidence of ammonia-oxidizing Crenarchaeota. Appl Environ Microbiol 73: 259-270.
91. Welch, S., Barker, W., and Banfield, J. (1999) Microbial extracellular polysaccharides and plagioclase dissolution. Geochim Cosmochim Acta 63: 1405-1419.
92. Wingender, J., Neu, T., and Flemming, H. (1999) Microbial Extracellular Polymeric Substances: Characterization, Structure and Fuction. Berlin, Germany: Springer.
93. Xiong, Y., Shi, L., Chen, B., Mayer, M., Lower, B., Londer, Y., etal. (2006) High-affinity binding and direct electron transfer to solid metals by the Shewanella oneidensis MR-1 outer membrane c-type cytochrome OmcA. J Am Chem Soc 128: 13978-13979.
94. Yen, Y., Kostakioti, M., Henderson, I., and Stathopoulos, C. (2008) Common themes and variations in serine protease autotransporters. Trends Microbiol 16: 370-379.
95. 3+ oxides in single phase suspensions and subsurface minerals. Am Mineral 83: 1426-1443.
96. Zhang, D., Pan, X., Mostofa, K., Chen, X., Mu, G., Wu, F., etal. (2010) Complexation between Hg(II) and biofilm extracellular polymeric substances: an application of fluorescence spectroscopy. J Hazard Mater 175: 359-365.
97. Zhang, T., and Fang, H. (2001) Quantification of extracellular polymeric substances in biofilms by confocal laser scanning microscopy. Biotechnol Lett 23: 405-409.
98. Zhang, X., Bishop, P., and Kinkle, B. (1999) Comparison of extraction methods for quantifying extracellular polymers in biofilms. Water Sci Technol 39: 211-218.