Vibrio cholerae Strains Possess Multiple Strategies for Abiotic and Biotic Surface Colonization
10.1128/jb.01867-06
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACT Despite its notoriety as a human pathogen, Vibrio cholerae is an aquatic microbe suited to live in freshwater, estuarine, and marine environments where biofilm formation may provide a selective advantage. Here we report characterization of biofilms formed on abiotic and biotic surfaces by two non-O1/O139 V. cholerae strains, TP and SIO, and by the O1 V. cholerae strain N16961 in addition to the isolation of 44 transposon mutants of SIO and TP impaired in biofilm formation. During the course of characterizing the mutants, 30 loci which have not previously been associated with V. cholerae biofilms were identified. These loci code for proteins which perform a wide variety of functions, including amino acid metabolism, ion transport, and gene regulation. Also, when the plankton colonization abilities of strains N16961, SIO, and TP were examined, each strain showed increased colonization of dead plankton compared with colonization of live plankton (the dinoflagellate Lingulodinium polyedrum and the copepod Tigriopus californicus ). Surprisingly, most of the biofilm mutants were not impaired in plankton colonization. Only mutants impaired in motility or chemotaxis showed reduced colonization. These results indicate the presence of both conserved and variable genes which influence the surface colonization properties of different V. cholerae subspecies.

Bibliography

Mueller, R. S., McDougald, D., Cusumano, D., Sodhi, N., Kjelleberg, S., Azam, F., & Bartlett, D. H. (2007). Vibrio cholerae Strains Possess Multiple Strategies for Abiotic and Biotic Surface Colonization. Journal of Bacteriology, 189(14), 5348–5360.

Authors 7
  1. Ryan S. Mueller (first)
  2. Diane McDougald (additional)
  3. Danielle Cusumano (additional)
  4. Nidhi Sodhi (additional)
  5. Staffan Kjelleberg (additional)
  6. Farooq Azam (additional)
  7. Douglas H. Bartlett (additional)
References 72 Referenced 72
  1. Alexeyev, M. F., and I. N. Shokolenko. 1995. Mini-Tn10 transposon derivatives for insertion mutagenesis and gene delivery into the chromosome of Gram-negative bacteria. Gene 160 : 59-62. (10.1016/0378-1119(95)00141-R) / Gene (1995)
  2. 10.1016/S0022-2836(05)80360-2
  3. 10.1128/jb.169.3.1061-1070.1987
  4. Atsumi, T., L. McCarter, and Y. Imae. 1992. Polar and lateral flagellar motors of marine Vibrio are driven by different ion-motive forces. Nature 355 : 182-184. (10.1038/355182a0) / Nature (1992)
  5. 10.1128/JB.185.19.5685-5696.2003
  6. 10.1128/JB.186.5.1574-1578.2004
  7. Chen, X., and P. S. Stewart. 2002. Role of electrostatic interactions in cohesion of bacterial biofilms. Appl. Microbiol. Biotechnol. 59 : 718-720. (10.1007/s00253-002-1044-2) / Appl. Microbiol. Biotechnol. (2002)
  8. 10.1128/AEM.67.7.3220-3225.2001
  9. Collet, A., S. Vilain, P. Cosette, G. A. Junter, T. T. Jouenne, R. S. Phillips, and P. D. Martino. 2007. Protein expression in Escherichia coli S17-1 biofilms: impact of indole. Antonie Leeuwenhoek 91 : 71-85. / Antonie Leeuwenhoek (2007)
  10. Colwell, R. R. 1996. Global climate and infectious disease: the cholera paradigm. Science 274 : 2025-2031. (10.1126/science.274.5295.2025) / Science (1996)
  11. Colwell, R. R., A. Huq, M. S. Islam, K. M. A. Aziz, M. Yunus, N. H. Khan, A. Mahmud, R. B. Sack, G. B. Nair, J. Chakraborty, D. A. Sack, and E. Russek-Cohen. 2003. Reduction of cholera in Bangladeshi villages by simple filtration. Proc. Natl. Acad. Sci. USA 100 : 1051-1055. (10.1073/pnas.0237386100) / Proc. Natl. Acad. Sci. USA (2003)
  12. D'Andrea, L. D., and L. Regan. 2003. TPR proteins: the versatile helix. Trends Biochem. Sci. 28 : 655. (10.1016/j.tibs.2003.10.007) / Trends Biochem. Sci. (2003)
  13. 10.1128/AEM.65.10.4594-4600.1999
  14. Epstein, P. 1993. Algal blooms in the spread and persistence of cholera. Biosystems 31 : 209-221. (10.1016/0303-2647(93)90050-M) / Biosystems (1993)
  15. Espeland, E. M., and R. G. Wetzel. 2001. Complexation, stabilization, and UV photolysis of extracellular and surface-bound glucosidase and alkaline phosphatase: implications for biofilm microbiota. Microb. Ecol. 42 : 572-585. (10.1007/s00248-001-1023-7) / Microb. Ecol. (2001)
  16. 10.1128/JB.185.9.2700-2710.2003
  17. Finkelstein, R. A., and S. Mukerjee. 1963. Hemagglutination: a rapid method for differentiating Vibrio cholerae and El Tor vibrios. Proc. Soc. Exp. Biol. Med. 112 : 355-359. (10.3181/00379727-112-28043) / Proc. Soc. Exp. Biol. Med. (1963)
  18. Culture of phytoplankton for feeding marine invertebrates. 1975
  19. 10.1128/AEM.70.4.2146-2153.2004
  20. Halpern, M., Y. B. Broza, S. Mittler, E. Arakawa, and M. Broza. 2004. Chironomid egg masses as a natural reservoir of Vibrio cholerae non-O1 and non-O139 in freshwater habitats. Microb. Ecol. 47 : 341-349. / Microb. Ecol. (2004)
  21. Haugo, A. J., and P. I. Watnick. 2002. Vibrio cholerae CytR is a repressor of biofilm development. Mol. Microbiol. 45 : 471-483. (10.1046/j.1365-2958.2002.03023.x) / Mol. Microbiol. (2002)
  22. 10.1038/35020000
  23. Horton, R. 1997. In vitro recombination and mutagenesis of DNA. SOEing together tailor-made genes. Methods Mol. Biol. 67 : 141-149. / Methods Mol. Biol. (1997)
  24. 10.1128/AEM.71.8.4645-4654.2005
  25. 10.1128/aem.45.1.275-283.1983
  26. Islam, M. S., B. S. Drasar, and D. J. Bradley. 1990. Long-term persistence of toxigenic Vibrio cholerae 01 in the mucilaginous sheath of a blue-green alga, Anabaena variabilis. J. Trop. Med. Hyg. 93 : 133-139. / J. Trop. Med. Hyg. (1990)
  27. Islam, M. S., S. Mahmuda, M. G. Morshed, H. B. Bakht, M. N. Khan, R. B. Sack, and D. A. Sack. 2004. Role of cyanobacteria in the persistence of Vibrio cholerae O139 in saline microcosms. Can. J. Microbiol. 50 : 127-131. (10.1139/w03-114) / Can. J. Microbiol. (2004)
  28. Jones, D. H., and S. C. Winistorfer. 1992. Sequence specific generation of a DNA panhandle permits PCR amplification of unknown flanking DNA. Nucleic Acids Res. 20 : 595-600. (10.1093/nar/20.3.595) / Nucleic Acids Res. (1992)
  29. 10.1093/nar/28.1.27
  30. 10.1128/AEM.69.9.5079-5088.2003
  31. Kirn, T. J., B. A. Jude, and R. K. Taylor. 2005. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438 : 863-866. (10.1038/nature04249) / Nature (2005)
  32. 10.1007/s00203-002-0442-2
  33. Lauro, F. M., E. A. Eloe, N. Liverani, G. Bertoloni, and D. H. Bartlett. 2005. Conjugal vectors for cloning, expression, and insertional mutagenesis in gram-negative bacteria. BioTechniques 38 : 708, 710, 712. (10.2144/05385BM06) / BioTechniques (2005)
  34. Lehmann, V., G. Hammerling, M. Nurminen, I. Minner, E. Ruschmann, O. Luderitz, T.-T. Kuo, and B. A. D. Stocker. 1973. A new class of heptose-defective mutant of Salmonella typhimurium. Eur. J. Biochem. 32 : 268-275. (10.1111/j.1432-1033.1973.tb02607.x) / Eur. J. Biochem. (1973)
  35. Lim, B., S. Beyhan, J. Meir, and F. H. Yildiz. 2006. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol. Microbiol. 60 : 331-348. (10.1111/j.1365-2958.2006.05106.x) / Mol. Microbiol. (2006)
  36. Lobitz, B., L. Beck, A. Huq, B. Wood, G. Fuchs, A. S. G. Faruque, and R. Colwell. 2000. Climate and infectious disease: use of remote sensing for detection of Vibrio cholerae by indirect measurement. Proc. Natl. Acad. Sci. USA 97 : 1438-1443. (10.1073/pnas.97.4.1438) / Proc. Natl. Acad. Sci. USA (2000)
  37. 10.1128/JB.185.9.2887-2900.2003
  38. Martino, P. D., R. Fursy, L. Bret, B. Sundararaju, and R. S. Phillips. 2003. Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. Can. J. Microbiol. 49 : 443-449. (10.1139/w03-056) / Can. J. Microbiol. (2003)
  39. Matthysse, A. G., S. Stretton, C. Dandie, N. C. McClure, and A. E. Goodman. 1996. Construction of GFP vectors for use in Gram-negative bacteria other than Escherichia coli. FEMS Microbiol. Lett. 145 : 87-94. (10.1111/j.1574-6968.1996.tb08561.x) / FEMS Microbiol. Lett. (1996)
  40. Matz, C., D. McDougald, A. M. Moreno, P. Y. Yung, F. H. Yildiz, and S. Kjelleberg. 2005. Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 102 : 16819-16824. (10.1073/pnas.0505350102) / Proc. Natl. Acad. Sci. USA (2005)
  41. Meibom, K. L., X. B. Li, A. T. Nielsen, C. Y. Wu, S. Roseman, and G. K. Schoolnik. 2004. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. USA 101 : 2524-2529. (10.1073/pnas.0308707101) / Proc. Natl. Acad. Sci. USA (2004)
  42. Merino, S., R. Gavin, M. Altarriba, L. Izquierdo, M. E. Maguire, and J. M. Tomas. 2001. The MgtE Mg2+ transport protein is involved in Aeromonas hydrophila adherence. FEMS Microbiol. Lett. 198 : 189-195. (10.1111/j.1574-6968.2001.tb10641.x) / FEMS Microbiol. Lett. (2001)
  43. Experiments in molecular genetics. 1972
  44. Miller, T. R., and R. Belas. 2006. Motility is involved in Silicibacter sp. TM1040 interaction with dinoflagellates. Environ. Microbiol. 8 : 1648-1659. (10.1111/j.1462-2920.2006.01071.x) / Environ. Microbiol. (2006)
  45. 10.1128/IAI.67.2.958-963.1999
  46. 10.1128/AEM.64.2.721-732.1998
  47. Moorthy, S., and P. I. Watnick. 2004. Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Mol. Microbiol. 52 : 573-587. (10.1111/j.1365-2958.2004.04000.x) / Mol. Microbiol. (2004)
  48. Moorthy, S., and P. I. Watnick. 2005. Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol. Microbiol. 57 : 1623-1635. (10.1111/j.1365-2958.2005.04797.x) / Mol. Microbiol. (2005)
  49. Muramoto, K., Y. Magariyama, M. Homma, I. Kawagishi, S. Sugiyama, Y. Imae, and S. Kudo. 1996. Rotational fluctuation of the sodium-driven flagellar motor of Vibrio alginolyticus is induced by binding of inhibitors. J. Mol. Biol. 259 : 687-695. (10.1006/jmbi.1996.0350) / J. Mol. Biol. (1996)
  50. 10.1016/S0076-6879(99)10008-9
  51. Paludan-Muller, C., D. Weichart, D. McDougald, and S. Kjelleberg. 1996. Analysis of starvation conditions that allow for prolonged culturability of Vibrio vulnificus at low temperature. Microbiology 142 : 1675-1684. (10.1099/13500872-142-7-1675) / Microbiology (1996)
  52. Pukatzki, S., A. T. Ma, D. Sturtevant, B. Krastins, D. Sarracino, W. C. Nelson, J. F. Heidelberg, and J. J. Mekalanos. 2006. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. USA 103 : 1528-1533. (10.1073/pnas.0510322103) / Proc. Natl. Acad. Sci. USA (2006)
  53. 10.1128/JB.187.9.2992-3001.2005
  54. 10.1128/JB.183.22.6579-6589.2001
  55. Schembri, M. A., K. Kjaergaard, and P. Klemm. 2003. Global gene expression in Escherichia coli biofilms. Mol. Microbiol. 48 : 253-267. (10.1046/j.1365-2958.2003.03432.x) / Mol. Microbiol. (2003)
  56. Shukla, B. N., D. C. Singh, and S. C. Sanyal. 1995. Attachment of non-culturable toxigenic Vibrio cholerae O1 and non-O1 and Aeromonas spp. to the aquatic arthropod Gerris spinolae and plants in the River Ganga, Varanasi. FEMS Immun. Med. Microbiol. 12 : 113-120. (10.1111/j.1574-695X.1995.tb00182.x) / FEMS Immun. Med. Microbiol. (1995)
  57. 10.1038/nbt1183-784
  58. Singh, P. K., M. R. Parsek, E. P. Greenberg, and M. J. Welsh. 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417 : 552. (10.1038/417552a) / Nature (2002)
  59. On the mode of communication of cholera 1855
  60. 10.1128/AEM.69.4.2313-2320.2003
  61. Tischler, A. D., and A. Camilli. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53 : 857-869. (10.1111/j.1365-2958.2004.04155.x) / Mol. Microbiol. (2004)
  62. Toner, B., A. Manceau, M. A. Marcus, D. B. Millet, and G. Sposito. 2005. Zinc sorption by a bacterial biofilm. Environ. Sci. Technol. 39 : 8288-8294. (10.1021/es050528+) / Environ. Sci. Technol. (2005)
  63. 10.1128/AEM.64.10.3648-3655.1998
  64. 10.1128/JB.183.14.4210-4216.2001
  65. Watnick, P. I., and R. Kolter. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34 : 586-595. (10.1046/j.1365-2958.1999.01624.x) / Mol. Microbiol. (1999)
  66. 10.1128/JB.186.23.8066-8073.2004
  67. Whiteley, M., M. G. Bangera, R. E. Bumgarner, M. R. Parsek, G. M. Teitzel, S. Lory, and E. P. Greenberg. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413 : 860-864. (10.1038/35101627) / Nature (2001)
  68. Worden, A. Z., M. Seidel, S. Smriga, A. Wick, F. Malfatti, D. Bartlett, and F. Azam. 2006. Trophic regulation of Vibrio cholerae in coastal marine waters. Environ. Microbiol. 8 : 21-29. (10.1111/j.1462-2920.2005.00863.x) / Environ. Microbiol. (2006)
  69. 10.1128/JB.183.5.1716-1726.2001
  70. Yildiz, F. H., X. S. Liu, A. Heydorn, and G. K. Schoolnik. 2004. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol. Microbiol. 53 : 497-515. (10.1111/j.1365-2958.2004.04154.x) / Mol. Microbiol. (2004)
  71. Yildiz, F. H., and G. K. Schoolnik. 1999. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc. Natl. Acad. Sci. USA 96 : 4028-4033. (10.1073/pnas.96.7.4028) / Proc. Natl. Acad. Sci. USA (1999)
  72. Zhu, J., M. B. Miller, R. E. Vance, M. Dziejman, B. L. Bassler, and J. J. Mekalanos. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99 : 3129-3134. (10.1073/pnas.052694299) / Proc. Natl. Acad. Sci. USA (2002)
Dates
Type When
Created 18 years, 3 months ago (May 11, 2007, 8:48 p.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:34 p.m.)
Indexed 1 month, 2 weeks ago (July 14, 2025, 11:19 p.m.)
Issued 18 years, 1 month ago (July 15, 2007)
Published 18 years, 1 month ago (July 15, 2007)
Published Print 18 years, 1 month ago (July 15, 2007)
Funders 0

None

@article{Mueller_2007, title={Vibrio cholerae Strains Possess Multiple Strategies for Abiotic and Biotic Surface Colonization}, volume={189}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.01867-06}, DOI={10.1128/jb.01867-06}, number={14}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Mueller, Ryan S. and McDougald, Diane and Cusumano, Danielle and Sodhi, Nidhi and Kjelleberg, Staffan and Azam, Farooq and Bartlett, Douglas H.}, year={2007}, month=jul, pages={5348–5360} }