Environmental reservoirs and mechanisms of persistence of Vibrio cholerae

Frontiers in Microbiology

Volumn 4, Issue DEC, 2013, Pages

  Lutz, Carla ^a   Erken, Martina ^a,b   Noorian, Parisa ^a   Sun, Shuyang ^c   McDougald, Diane ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Biofilms; Chitin; Predation; Protozoa; Starvation adaptation; Stress; Viable but non culturable; Zooplankton

Indexed keywords

AQUATIC ENVIRONMENT; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; BACTERIAL TRANSMISSION; BACTERIOPLANKTON; BIOFILM; CHOLERA; COLONY FORMING UNIT; DISEASE ASSOCIATION; ENVIRONMENTAL DISEASE; ENVIRONMENTAL MANAGEMENT; ENVIRONMENTAL TEMPERATURE; GENE EXPRESSION REGULATION; HETEROTROPHY; NONHUMAN; ORGANISMAL INTERACTION; ORGANISMS BY GEOGRAPHICAL DISTRIBUTION; PROTOZOAL INFECTION; REVIEW; SALT STRESS; STARVATION; SURFACE PROPERTY; VIBRIO CHOLERAE;

EID: 84892160844     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00375     Document Type: Review

References (248)

1. Aagesen, A., and Häse, C. (2012). Sequence analyses of type IV pili from Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus. Microb. Ecol. 64, 509-524. doi: 10.1007/s00248-012-0021-2.
2. Abd, H., Saeed, A., Weintraub, A., Nair, G. B., and Sandström, G. (2007). Vibrio cholerae O1 strains are facultative intracellular bacteria, able to survive and multiply symbiotically inside the aquatic free-living amoeba Acanthamoeba castellanii. FEMS Microbiol. Ecol. 60, 33-39. doi: 10.1111/j.1574-6941.2006.00254.x.
3. Abd, H., Saeed, A., Weintraub, A., and Sandström, G. (2009). Vibrio cholerae O139 requires neither capsule nor LPS O side chain to grow inside Acanthamoeba castellanii. J. Med. Microbiol. 58, 125-131. doi: 10.1099/jmm.0.004721-0.
4. Abd, H., Shanan, S., Saeed, A., and Sandström, G. (2011). Survival of Vibrio cholerae inside Acanthamoeba and detection of both microorganisms from natural water samples may point out the amoeba as a protozoal host for V. cholerae. J. Bacteriol. Parasitol. 4, 109.
5. Abd, H., Weintraub, A., and Sandström, G. (2004). Interaction between Vibrio cholerae and Acanthamoeba castellanii. Microb. Ecol. Health Dis. 16, 51-57. doi: 10.1080/08910600410029190.
6. Abd, H., Weintraub, A., and Sandström, G. (2005). Intracellular survival and replication of Vibrio cholerae O139 in aquatic free-living amoebae. Environ. Microbiol. 7, 1003-1008. doi: 10.1111/j.1462-2920.2005.00771.x.
7. Absalon, C., Van Dellen, K., and Watnick, P. I. (2011). A communal bacterial adhesin anchors biofilm and bystander cells to surfaces. PLoS Pathog. 7:e1002210. doi:10.1371/journal.ppat.1002210.
8. Akselman, R., Jurquiza, V., Costagliola, M. C., Fraga, S. G., Pichel, M., Hozbor, C., et al. (2010). Vibrio cholerae O1 found attached to the dinoflagellate Noctiluca scintillans in Argentine shelf waters. Mar. Biodivers. Rec. 3, e120. doi:10.1017/S1755267210001077.
9. Alam, M., Sultana, M., Nair, G. B., Sack, R. B., Sack, D. A., Siddique, A. K., et al. (2006). Toxigenic Vibrio cholerae in the aquatic environment of Mathbaria, Bangladesh. Appl. Environ. Microbiol. 72, 2849-2855. doi: 10.1128/AEM.72.4.2849-2855.2006.
10. Alam, M., Sultana, M., Nair, G. B., Siddique, A. K., Hasan, N. A., Sack, R. B., et al. (2007). Viable but nonculturable Vibrio cholerae O1 in biofilms in the aquatic environment and their role in cholera transmission. Proc. Natl. Acad. Sci. U.S.A. 104, 17801-17806. doi: 10.1073/pnas.0705599104.
11. Albert, M., Ansaruzzaman, M., Bardhan, P., Faruque, A., Faruque, S., Islam, M., et al. (1993). Large epidemic of cholera-like disease in Bangladesh caused by Vibrio cholerae 0139 synonym Bengal. Lancet 342, 387-390. doi: 10.1016/0140-6736(93)92811-7.
12. Ali, A., Rashid, M. H., and Karaolis, D. K. (2002). High-frequency rugose exopolysaccharide production by Vibrio cholerae. Appl. Environ. Microbiol. 68, 5773-5778. doi: 10.1128/AEM.68.11.5773-5778.2002.
13. Andersson, Y., and Ekdahl, K. (2006). Wound infections due to Vibrio cholerae in Sweden after swimming in the Baltic Sea, summer 2006. Euro. Surveill. 11, E060803.2.
14. Arana, I., Muela, A., Iriberri, J., Egea, L., and Barcina, I. (1992). Role of hydrogen peroxide in loss of culturability mediated by visible light in Escherichia coli in a freshwater ecosystem. Appl. Environ. Microbiol. 58, 3903-3907.
15. Asakura, H., Ishiwa, A., Arakawa, E., Makino, S. I., Okada, Y., Yamamoto, S., et al. (2007). Gene expression profile of Vibrio cholerae in the cold stress-induced viable but non-culturable state. Environ. Microbiol. 9, 869-879. doi: 10.1111/j.1462-2920.2006.01206.x.
16. Asplund, M. E., Rehnstam-Holm, A. S., Atnur, V., Raghunath, P., Saravanan, V., Härnström, K., et al. (2011). Water column dynamics of Vibrio in relation to phytoplankton community composition and environmental conditions in a tropical coastal area. Environ. Microbiol. 13, 2738-2751. doi: 10.1111/j.1462-2920.2011.02545.x.
17. Bagg, A., and Neilands, J. B. (1987). Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry 26, 5471-5477. doi: 10.1021/bi00391a039.
18. Baker-Austin, C., Stockley, L., Rangdale, R., and Martinez-Urtaza, J. (2010). Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: a European perspective. Environ. Microbiol. Rep. 2, 7-18. doi: 10.1111/j.1758-2229.2009.00096.x.
19. Bakhshi, B., Barzelighi, H. M., Adabi, M., Lari, A. R., and Pourshafie, M. (2009). A molecular survey on virulence associated genotypes of non-O1 non-O139 Vibrio cholerae in aquatic environment of Tehran, Iran. Water Res. 43, 1441-1447. doi: 10.1016/j.watres.2008.12.025.
20. Bari, S. M. N., Roky, M. K., Mohiuddin, M., Kamruzzaman, M., Mekalanos, J. J., and Faruque, S. M. (2013). Quorum-sensing autoinducers resuscitate dormant Vibrio cholerae in environmental water samples. Proc. Natl. Acad. Sci. U.S.A. 110, 9926-9931. doi: 10.1073/pnas.1307697110.
21. Bauer, A., Ostensvik, O., Florvag, M., Ormen, O., and Rorvik, L. M. (2006). Occurrence of Vibrio parahaemolyticus, V. cholerae, and V. vulnificus in Norwegian blue mussels(Mytilus edulis). Appl. Environ. Microbiol. 72, 3058-3061. doi: 10.1128/AEM.72.4.3058-3061.2006.
22. Berk, V., Fong, J. C. N., Dempsey, G. T., Develioglu, O. N., Zhuang, X., Liphardt, J., et al. (2012). Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science 337, 236-239. doi: 10.1126/science.1222981.
23. Binsztein, N., Costagliola, M. C., Pichel, M., Jurquiza, V., Ramiez, F. C., Akselman, R., et al. (2004). Viable but nonculturable Vibrio cholerae O1 in the aquatic environment of Argentina. Appl. Environ. Microbiol. 70, 7481-7486. doi: 10.1128/AEM.70.12.7481-7486.2004.
24. Birkbeck, T., McHenery, J., and Nottage, A. (1987). Inhibition of filtration in bivalves by marine Vibrios. Aquaculture 67, 247-248. doi: 10.1016/0044-8486(87)90045-7.
25. Blackburn, N., Fenchel, T., and Mitchell, J. (1998). Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282, 2254-2256. doi: 10.1126/science.282.5397.2254.
26. Blackwell, K. D., and Oliver, J. D. (2008). The ecology of Vibrio vulnificus, Vibrio cholerae, and Vibrio parahaemolyticus in North Carolina estuaries. J. Microbiol. 46, 146-153. doi: 10.1007/s12275-007-0216-2.
27. Bloomfield, S. F., Stewart, G. S. A. B., Dodd, C. E. R., Booth, I. R., and Power, E. G. M. (1998). The viable but non-culturable phenomenon explained? Microbiology 144, 1-3. doi: 10.1099/00221287-144-1-1.
28. Bourassa, L., and Camilli, A. (2009). Glycogen contributes to the environmental persistence and transmission of Vibrio cholerae. Mol. Microbiol. 72, 124-138. doi: 10.1111/j.1365-2958.2009.06629.x.
29. Böer, S., Heinemeyer, E. A., Luden, K., Erler, R., Gerdts, G., Janssen, F., et al. (2013). Temporal and spatial distribution patterns of potentially pathogenic Vibrio spp. at recreational beaches of the German North Sea. Microb. Ecol. 65, 1052-1067. doi: 10.1007/s00248-013-0221-4.
30. Boyd, E. F., and Waldor, M. K. (2002). Evolutionary and functional analyses of variants of the toxin-coregulated pilus protein TcpA from toxigenic Vibrio cholerae non-O1/non-O139 serogroup isolates. Microbiology 148, 1655-1666.
31. Bozue, J. A., and Johnson, W. (1996). Interaction of Legionella pneumophila with Acanthamoeba castellanii: uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion. Infect. Immun. 64, 668-673.
32. Brandl, M. T., Rosenthal, B. M., Haxo, A. F., and Berk, S. G. (2005). Enhanced survival of Salmonella enterica in vesicles released by a soilborne Tetrahymena species. Appl. Environ. Microbiol. 71, 1562-1569. doi: 10.1128/AEM.71.3.1562-1569.2005.
33. Brown, M. R. W., and Barker, J. (1999). Unexplored reservoirs of pathogenic bacteria: protozoa and biofilms. Trends Microbiol. 7, 46-50. doi: 10.1016/S0966-842X(98)01425-5.
34. Broza, M., Gancz, H., Halpern, M., and Kashi, Y. (2005). Adult non-biting midges: possible windborne carriers of Vibrio cholerae non-O1 non-O139. Environ. Microbiol. 7, 576-585. doi: 10.1111/j.1462-2920.2005.00745.x.
35. Broza, M., and Halpern, M. (2001). Pathogen reservoirs. Chironomid egg masses and Vibrio cholerae. Nature 412, 40. doi: 10.1038/35083691.
36. Buerger, S., Spoering, A., Gavrish, E., Leslin, C., Ling, L., and Epstein, S. (2012a). Microbial scout hypothesis and microbial discovery. Appl. Environ. Microbiol. 78, 3229-3233. doi: 10.1128/AEM.07308-11.
37. Buerger, S., Spoering, A., Gavrish, E., Leslin, C., Ling, L., and Epstein, S. (2012b). Microbial scout hypothesis, stochastic exit from dormancy, and the nature of slow growers. Appl. Environ. Microbiol. 78, 3221-3228. doi: 10.1128/AEM.07307-11.
38. Cantet, F., Hervio-Heath, D., Caro, A., Le Mennec, C., Monteil, C., Quéméré, C., et al. (2013). Quantification of Vibrio parahaemolyticus, Vibrio vulnificus and Vibrio cholerae in French Mediterranean coastal lagoons. Res. Microbiol. 164, 867-874. doi: 10.1016/j.resmic.2013.06.005.
39. Carroll, J., Mateescu, M., Chava, K., Colwell, R. R., and Bej, A. (2001). Response and tolerance of toxigenic Vibro cholerae O1 to cold temperatures. Antonie Van Leeuwenhoek 79, 377-384. doi: 10.1023/A:1012004725373.
40. Casper-Lindley, C., and Yildiz, F. H. (2004). VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J. Bacteriol. 186, 1574-1578. doi: 10.1128/JB.186.5.1574-1578.2004.
41. Castro-Rosas, J., and Escartìn, E. F. (2005). Increased tolerance of Vibrio cholerae O1 to temperature, pH, or drying associated with colonization of shrimp carapaces. Int. J. Food Microbiol. 102, 195-201. doi: 10.1016/j.ijfoodmicro.2004.12.015.
42. Chatterjee, A., Dutta, P. K., and Chowdhury, R. (2007). Effect of fatty acids and cholesterol present in bile on expression of virulence factors and motility of Vibrio cholerae. Infect. Immun. 75, 1946-1953. doi: 10.1128/IAI.01435-06.
43. Chen, H., Young, S., Berhane, T. K., and Williams, H. N. (2012). Predatory Bacteriovorax communities ordered by various prey species. PLoS ONE 7:e34174. doi:10.1371/journal.pone.0034174.
44. Chiavelli, D. A., Marsh, J. W., and Taylor, R. K. (2001). The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl. Environ. Microbiol. 67, 3220-3225. doi: 10.1128/AEM.67.7.3220-3225.2001.
45. Collin, B., and Rehnstam-Holm, A. S. (2011). Occurrence and potential pathogenesis of Vibrio cholerae, Vibrio parahaemolyticus and Vibrio vulnificus on the South Coast of Sweden. FEMS Microbiol. Ecol. 78, 306-313. doi: 10.1111/j.1574-6941.2011.01157.x.
46. Collin, B., Rehnstam-Holm, A. S., Lindmark, B., Pal, A., Wai, S. N., and Hernroth, B. (2012). The origin of Vibrio cholerae influences uptake and persistence in the blue mussel Mytilus edulis. J. Shellfish Res. 31, 87-92. doi: 10.2983/035.031.0111.
47. Colwell, R. R. (2000). Viable but nonculturable bacteria: a survival strategy. J. Infect. Chemother. 6, 121-125. doi: 10.1007/PL00012151.
48. Colwell, R. R., Brayton, P., Herrington, D., Tall, B., Huq, A., and Levine, M. M. (1996). Viable but non-culturable Vibrio cholerae O1 revert to a cultivable state in the human intestine. World J. Microbiol. Biotechnol. 12, 28-31. doi: 10.1007/BF00327795.
49. Colwell, R. R., Brayton, P. R., Grimes, D. J., Roszak, D. B., Huq, S. A., and Palmer, L. M. (1985). Viable but non-culturable Vibrio cholerae and related pathogens in the environment: implications for release of genetically engineered microorganisms. Biotechnology 3, 817-820. doi: 10.1038/nbt0985-817.
50. Colwell, R. R., Huq, A., Islam, M. S., Aziz, K. M., Yunus, M., Khan, N. H., et al. (2003). Reduction of cholera in Bangladeshi villages by simple filtration. Proc. Natl. Acad. Sci. U.S.A. 100, 1051-1055. doi: 10.1073/pnas.0237386100.
51. Colwell, R. R., Kaper, J., and Joseph, S. (1977). Vibrio cholerae, Vibrio parahaemolyticus, and other vibrios: occurrence and distribution in Chesapeake Bay. Science 198, 394-396.
52. Colwell, R. R., Seidler, R. J., Kaper, J., Joseph, S. W., Garges, S., Lockman, H., et al. (1981). Occurrence of Vibrio cholerae serotype O1 in Maryland and Louisiana estuaries. Appl. Environ. Microbiol. 41, 555-558.
53. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., and Lappin-Scott, H. M. (1995). Microbial biofilms. Annu. Rev. Microbiol. 49, 711-745. doi: 10.1146/annurev.mi.49.100195.003431.
54. Covazzi Harriague, A., Brino, M. D., Zampini, M., Albertelli, G., Pruzzo, C., and Misic, C. (2008). Vibrios in association with sedimentary crustaceans in three beaches of the northern Adriatic Sea (Italy). Mar. Pollut. Bull. 56, 574-579. doi: 10.1016/j.marpolbul.2007.12.011.
55. Coyne, V. E., and al-Harthi, L. (1992). Induction of melanin biosynthesis in Vibrio cholerae. Appl. Environ. Microbiol. 58, 2861-2865.
56. Dawson, M. P., Humphrey, B. A., and Marshall, K. C. (1981). Adhesion: a tactic in the survival strategy of a marine Vibrio during starvation. Curr. Microbiol. 6, 195-199. doi: 10.1007/BF01566971.
57. de Magny, G. C., Mozumder, P. K., Grim, C. J., Hasan, N. A., Naser, M. N., Alam, M., et al. (2011). Role of zooplankton diversity in Vibrio cholerae population dynamics and in the incidence of cholera in the Bangladesh Sundarbans. Appl. Environ. Microbiol. 77, 6125-6132. doi: 10.1128/AEM.01472-10.
58. Deriu, A., Sechi, L. A., Molicotti, P., Spanu, M. L., and Zanetti, S. (2002). Virulence genes in halophilic Vibrio spp. isolated in common mussels. New Microbiol. 25, 93-96.
59. Desmarchelier, P., Wong, F., and Mallard, K. (1995). An epidemiological study of Vibrio cholerae O1 in the Australian environment based on rRNA gene polymorphisms. Epidemiol. Infect. 115, 435-446. doi: 10.1017/S0950268800058593.
60. Dickinson, G., Lim, K. Y., and Jiang, S. C. (2013). Quantitative microbial risk assessment of pathogenic Vibrios in marine recreational waters of Southern California. Appl. Environ. Microbiol. 79, 294-302. doi: 10.1128/AEM.02674-12.
61. Eiler, A., Gonzalez-Rey, C., Allen, S., and Bertilsson, S. (2007). Growth response of Vibrio cholerae and other Vibrio spp. to cyanobacterial dissolved organic matter and temperature in brackish water. FEMS Microbiol. Ecol. 60, 411-418. doi: 10.1111/j.1574-6941.2007.00303.x.
62. Eiler, A., Johansson, M., and Bertilsson, S. (2006). Environmental influences on Vibrio populations in northern temperate and boreal coastal waters (Baltic and Skagerrak Seas). Appl. Environ. Microbiol. 72, 6004-6011. doi: 10.1128/AEM.00917-06.
63. Epstein, P. R. (1993). Algal blooms in the spread and persistence of cholera. Biosystems 31, 209-221. doi: 10.1016/0303-2647(93)90050-M.
64. Epstein, S. (2009). "General model of microbial uncultivability," in Uncultivated Microorganisms, ed. S. S. Epstein (Berlin: Springer), 131-159.
65. Erken, M., Weitere, M., Kjelleberg, S., and McDougald, D. (2011). In situ grazing resistance of Vibrio cholerae in the marine environment. FEMS Microbiol. Ecol. 76, 504-512. doi: 10.1111/j.1574-6941.2011.01067.x.
66. Faruque, S. M., Chowdhury, N., Kamruzzaman, M., Dziejman, M., Rahman, M. H., Sack, D. A., et al. (2004). Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area. Proc. Natl. Acad. Sci. U.S.A. 101, 2123-2128. doi: 10.1073/pnas.0308485100.
67. Faruque, S. M., Islam, M. J., Ahmad, Q. S., Faruque, A. S. G., Sack, D. A., Nair, G. B., et al. (2005). Self-limiting nature of seasonal cholera epidemics: role of host-mediated amplification of phage. Proc. Natl. Acad. Sci. U.S.A. 102, 6119-6124. doi: 10.1073/pnas.0502069102.
68. Focareta, T., and Manning, P. A. (1991). Distinguishing between the extracellular DNases of Vibrio cholerae and development of a transformation system. Mol. Microbiol. 5, 2547-2555. doi: 10.1111/j.1365-2958.1991.tb02101.x.
69. Fong, J. C., Karplus, K., Schoolnik, G. K., and Yildiz, F. H. (2006). Identification and characterization of RbmA, a novel protein required for the development of rugose colony morphology and biofilm structure in Vibrio cholerae. J. Bacteriol. 188, 1049-1059. doi: 10.1128/JB.188.3.1049-1059.2006.
70. Fong, J. C., Syed, K. A., Klose, K. E., and Yildiz, F. H. (2010). Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology 156, 2757-2769. doi: 10.1099/mic.0.040196-0.
71. Fong, J. C., and Yildiz, F. H. (2007). The rbmBCDEF gene cluster modulates development of rugose colony morphology and biofilm formation in Vibrio cholerae. J. Bacteriol. 189, 2319-2330. doi: 10.1128/JB.01569-06.
72. Franco, A. A., Fix, A. D., Prada, A., Paredes, E., Palomino, J. C., Wright, A. C., et al. (1997). Cholera in Lima, Peru, correlates with prior isolation of Vibrio cholerae from the environment. Am. J. Epidemiol. 146, 1067-1075. doi: 10.1093/oxfordjournals.aje.a009235.
73. Freter, R., and O'Brien, P. C. (1981). Role of chemotaxis in the association of motile bacteria with intestinal mucosa: chemotactic responses of Vibrio cholerae and description of motile nonchemotactic mutants. Infect. Immun. 34, 215-221.
74. Goldberg, M. B., Boyko, S. A., and Calderwood, S. B. (1991). Positive transcriptional regulation of an iron-regulated virulence gene in Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 88, 1125-1129. doi: 10.1073/pnas.88.4.1125.
75. González-Escalona, N., Fey, A., Höfle, M. G., Espejo, R. T., and A. Guzmán, C. (2006). Quantitative reverse transcription polymerase chain reaction analysis of Vibrio cholerae cells entering the viable but non-culturable state and starvation in response to cold shock. Environ. Microbiol. 8, 658-666. doi: 10.1111/j.1462-2920.2005.00943.x.
76. Gosink, K. K., Kobayashi, R., Kawagishi, I., and Hase, C. C. (2002). Analyses of the roles of the three cheA homologs in chemotaxis of Vibrio cholerae. J. Bacteriol. 184, 1767-1771. doi: 10.1128/JB.184.6.1767-1771.2002.
77. Griffiths, G. L., Sigel, S. P., Payne, S. M., and Neilands, J. B. (1984). Vibriobactin, a siderophore from Vibrio cholerae. J. Biol. Chem. 259, 383-385.
78. Grim, C. J., Jaiani, E., Whitehouse, C. A., Janelidze, N., Kokashvili, T., Tediashvili, M., et al. (2010). Detection of toxigenic Vibrio cholerae O1 in freshwater lakes of the former Soviet Republic of Georgia. Environ. Microbiol. Rep. 2, 2-6. doi: 10.1111/j.1758-2229.2009.00073.x.
79. Gurbanov, S., Akhmadov, R., Shamkhalova, G., Akhmadova, S., Haley, B., Colwell, R. R., et al. (2011). Occurrence of Vibrio cholerae in municipal and natural waters and incidence of cholera in Azerbaijan. Ecohealth 8, 468-477. doi: 10.1007/s10393-012-0756-8.
80. Hahn, M. W., and Höfle, M. G. (2001). Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol. Ecol. 35, 113-121. doi: 10.1111/j.1574-6941.2001.tb00794.x.
81. Haley, B. J., Chen, A., Grim, C. J., Clark, P., Diaz, C. M., Taviani, E., et al. (2012). Vibrio cholerae in a historically cholera-free country. Environ. Microbiol. Rep. 4, 381-389. doi: 10.1111/j.1758-2229.2012.00332.x.
82. Hall-Stoodley, L., Costerton, J. W., and Stoodley, P. (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95-108. doi: 10.1038/nrmicro821.
83. Halpern, M. (2011). "Chironomids and Vibrio cholerae," in Beneficial Microorganisms in Multicellular Life Forms, eds E. Rosenberg and U. Gophna (Berlin: Springer), 43-56.
84. Halpern, M., Broza, Y. B., Mittler, S., Arakawa, E., and Broza, M. (2004). Chironomid egg masses as a natural reservoir of Vibrio cholerae non-O1 and non-O139 in freshwater habitats. Microb. Ecol. 47, 341-349. doi: 10.1007/s00248-003-2007-6.
85. Halpern, M., Gancz, H., Broza, M., and Kashi, Y. (2003). Vibrio cholerae hemagglutinin/protease degrades chironomid egg masses. Appl. Environ. Microbiol. 69, 4200-4204. doi: 10.1128/AEM.69.7.4200-4204.2003.
86. Halpern, M., Landsberg, O., Raats, D., and Rosenberg, E. (2007). Culturable and VBNC Vibrio cholerae: interactions with chironomid egg masses and their bacterial population. Microb. Ecol. 53, 285-293. doi: 10.1007/s00248-006-9094-0.
87. Halpern, M., Raats, D., Lavion, R., and Mittler, S. (2006). Dependent population dynamics between chironomids (nonbiting midges) and Vibrio cholerae. FEMS Microbiol. Ecol. 55, 98-104. doi: 10.1111/j.1574-6941.2005.00020.x.
88. Halpern, M., Senderovich, Y., and Izhaki, I. (2008). Waterfowl: the missing link in epidemic and pandemic cholera dissemination? PLoS Pathog. 4:e1000173. doi:10.1371/journal.ppat.1000173.
89. Hamana, K., and Matsuzaki, S. (1982). Widespread occurrence of norspermidine and norspermine in eukaryotic algae. J. Biochem. 91, 1321-1328.
90. Hammer, B. K., and Bassler, B. L. (2003). Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50, 101-104. doi: 10.1046/j.1365-2958.2003.03688.x.
91. Haugo, A. J., and Watnick, P. I. (2002). Vibrio cholerae CytR is a repressor of biofilm development. Mol. Microbiol. 45, 471-483. doi: 10.1046/j.1365-2958.2002.03023.x.
92. Heidelberg, J. F., Eisen, J. A., Nelson, W. C., Clayton, R. A., Gwinn, M. L., Dodson, R. J., et al. (2000). DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406, 477-483. doi: 10.1038/35020000.
93. Hernroth, B., Lothigius, Å., and Bölin, I. (2010). Factors influencing survival of enterotoxigenic Escherichia coli, Salmonella enterica (serovar Typhimurium) and Vibrio parahaemolyticus in marine environments. FEMS Microbiol. Ecol. 71, 272-280. doi: 10.1111/j.1574-6941.2009.00803.x.
94. Hill, V. R., Cohen, N., Kahler, A. M., Jones, J. L., Bopp, C. A., Marano, N., et al. (2011). Toxigenic Vibrio cholerae O1 in water and seafood, Haiti. Emerg. Infect. Dis. 17, 2147. doi: 10.3201/eid1711.110748.
95. Hood, M. A., and Winter, P. A. (1997). Attachment of Vibrio cholerae under various environmental conditions and to selected substrates. FEMS Microbiol. Ecol. 22, 215-223. doi: 10.1111/j.1574-6941.1997.tb00373.x.
96. Houot, L., Chang, S., Pickering, B. S., Absalon, C., and Watnick, P. I. (2010). The phosphoenolpyruvate phosphotransferase system regulates Vibrio cholerae biofilm formation through multiple independent pathways. J. Bacteriol. 192, 3055-3067. doi: 10.1128/JB.00213-10.
97. Houot, L., and Watnick, P. I. (2008). A novel role for enzyme I of the Vibrio cholerae phosphoenolpyruvate phosphotransferase system in regulation of growth in a biofilm. J. Bacteriol. 190, 311-320. doi: 10.1128/JB.01410-07.
98. Hranitzky, K. W., Mulholland, A., Larson, A. D., Eubanks, E. R., and Hart, L. T. (1980). Characterization of a flagellar sheath protein of Vibrio cholerae. Infect. Immun. 27, 597-603.
99. Hunt, D. E., Gevers, D., Vahora, N. M., and Polz, M. F. (2008). Conservation of the chitin utilization pathway in the Vibrionaceae. Appl. Environ. Microbiol. 74, 44-51. doi: 10.1128/AEM.01412-07.
100. Huq, A., Sack, R. B., Nizam, A., Longini, I. M., Nair, G. B., Ali, A., et al. (2005). Critical factors influencing the occurrence of Vibrio cholerae in the environment of Bangladesh. Appl. Environ. Microbiol. 71, 4645-4654. doi: 10.1128/AEM.71.8.4645-4654.2005.
101. Huq, A., Small, E., West, P., Huq, M., Rahman, R., and Colwell, R. R. (1983). Ecological relationship between Vibrio cholerae and planktonic copepods. Appl. Environ. Microbiol. 45, 275-283.
102. Huq, A., Xu, B., Chowdhury, M. A., Islam, M. S., Montilla, R., and Colwell, R. R. (1996). A simple filtration method to remove plankton-associated Vibrio cholerae in raw water supplies in developing countries. Appl. Environ. Microbiol. 62, 2508-2512.
103. Huq, A., Yunus, M., Sohel, S. S., Bhuiya, A., Emch, M., Luby, S. P., et al. (2010). Simple sari cloth filtration of water is sustainable and continues to protect villagers from cholera in Matlab, Bangladesh. MBio 1. e0003410. doi:10.1128/mBio.00034-10.
104. Ishikawa, T., Rompikuntal, P. K., Lindmark, B., Milton, D. L., and Wai, S. N. (2009). Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. PLoS ONE 4:e6734. doi:10.1371/journal.pone.0006734.
105. Islam, A., Labbate, M., Djordjevic, S. P., Alam, M., Darling, A., Melvold, J., et al. (2013). Indigenous Vibrio cholerae strains from a non-endemic region are pathogenic. Open Biol. 3, 120181. doi: 10.1098/rsob.120181.
106. Islam, M., Hasan, M., Miah, M., Yunus, M., Zaman, K., and Albert, M. (1994). Isolation of Vibrio cholerae O139 synonym Bengal from the aquatic environment in Bangladesh: implications for disease transmission. Appl. Environ. Microbiol. 60, 1684-1686.
107. Islam, M. S., Drasar, B. S., and Bradley, D. J. (1989). Attachment of toxigenic Vibrio cholerae 01 to various freshwater plants and survival with a filamentous green alga, Rhizoclonium fontanum. J. Trop. Med. Hyg. 92, 396-401.
108. Islam, M. S., Rahim, Z., Alam, M. J., Begum, S., Moniruzzaman, S. M., Umeda, A., et al. (1999). Association of Vibrio cholerae O1 with the cyanobacterium, Anabaena sp.,elucidated by polymerase chain reaction and transmission electron microscopy. Trans. R. Soc. Trop. Med. Hyg. 93, 36-40. doi: 10.1016/S0035-9203(99)90171-2.
109. Jahid, I. K., Silva, A. J., and Benitez, J. A. (2006). Polyphosphate stores enhance the ability of Vibrio cholerae to overcome environmental stresses in a low-phosphate environment. Appl. Environ. Microbiol. 72, 7043-7049. doi: 10.1128/AEM.00924-06.
110. Jain, V., Dongre, M., and Raychaudhuri, S. (2006). Interaction of Vibrio cholerae O139 with an intestinal parasite, Entamoeba histolytica. J. Med. Microbiol. 55, 1755-1756. doi: 10.1099/jmm.0.46812-0.
111. Jiang, S. C. (2001). Vibrio cholerae in recreational beach waters and tributaries of Southern California. Hydrobiologia 460, 157-164. doi: 10.1023/A:1013152407425.
112. Jobling, M. G., and Holmes, R. K. (1997). Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Mol. Microbiol. 26, 1023-1034. doi: 10.1046/j.1365-2958.1997.6402011.x.
113. Johnson, C., Flowers, A., Noriea, N., Zimmerman, A., Bowers, J., Depaola, A., et al. (2010). Relationships between environmental factors and pathogenic Vibrios in the Northern Gulf of Mexico. Appl. Environ. Microbiol. 76, 7076-7084. doi: 10.1128/AEM.00697-10.
114. Johnson, C. N., Bowers, J. C., Griffitt, K. J., Molina, V., Clostio, R. W., Pei, S., et al. (2012). Ecology of Vibrio parahaemolyticus and Vibrio vulnificus in the coastal and estuarine waters of Louisiana, Maryland, Mississippi, and Washington (United States). Appl. Environ. Microbiol. 78, 7249-7257. doi: 10.1128/AEM.01296-12.
115. Jubair, M., Morris, J. G. Jr., and Ali, A. (2012). Survival of Vibrio cholerae in nutrient-poor environments is associated with a novel "persister" phenotype. PLoS ONE 7:e45187. doi:10.1371/journal.pone.0045187.
116. Jutla, A. S., Akanda, A. S., Griffiths, J. K., Colwell, R. R., and Islam, S. (2011). Warming oceans, phytoplankton, and river discharge: implications for cholera outbreaks. Am. J. Trop. Med. Hyg. 85, 303-308. doi: 10.4269/ajtmh.2011.11-0181.
117. Kamruzzaman, M., Udden, S. N., Cameron, D. E., Calderwood, S. B., Nair, G. B., Mekalanos, J. J., et al. (2010). Quorum-regulated biofilms enhance the development of conditionally viable, environmental Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 107, 1588-1593. doi: 10.1073/pnas.0913404107.
118. Kan, B., Habibi, H., Schmid, M., Liang, W., Wang, R., Wang, D., et al. (2004). Proteome comparison of Vibrio cholerae cultured in aerobic and anaerobic conditions. Proteomics 4, 3061-3067. doi: 10.1002/pmic.200400944.
119. Karatan, E., Duncan, T. R., and Watnick, P. I. (2005). NspS, a predicted polyamine sensor, mediates activation of Vibrio cholerae biofilm formation by norspermidine. J. Bacteriol. 187, 7434-7443. doi: 10.1128/JB.187.21.7434-7443.2005.
120. Kierek, K., and Watnick, P. I. (2003). Environmental determinants of Vibrio cholerae biofilm development. Appl. Environ. Microbiol. 69, 5079-5088. doi: 10.1128/AEM.69.9.5079-5088.2003.
121. Kiiyukia, C., Nakajima, A., Nakai, T., Muroga, K., Kawakami, H., and Hashimoto, H. (1992). Vibrio cholerae non-O1 isolated from ayu fish (Plecoglossus altivelis) in Japan. Appl. Environ. Microbiol. 58, 3078-3082.
122. Kirn, T. J., Jude, B. A., and Taylor, R. K. (2005). A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438, 863-866. doi: 10.1038/nature04249.
123. Kirs, M., Depaola, A., Fyfe, R., Jones, J., Krantz, J., Van Laanen, A., et al. (2011). A survey of oysters Crassostrea gigas in New Zealand for Vibrio parahaemolyticus and Vibrio vulnificus. Int. J. Food Microbiol. 147, 149-153. doi: 10.1016/j.ijfoodmicro.2011.03.012.
124. Kirschner, A. K. T., Schlesinger, J., Farnleitner, A. H., Hornek, R., Süß, B., Golda, B., et al. (2008). Rapid growth of planktonic Vibrio cholerae non-O1/non-O139 strains in a large alkaline lake in Austria: dependence on temperature and dissolved organic carbon quality. Appl. Environ. Microbiol. 74, 2004-2015. doi: 10.1128/AEM.01739-07.
125. Kojima, S., Yamamoto, K., Kawagishi, I., and Homma, M. (1999). The polar flagellar motor of Vibrio cholerae is driven by an Na+ motive force. J. Bacteriol. 181, 1927-1930.
126. Kong, I. S., Bates, T. C., Hülsmann, A., Hassan, H., Smith, B. E., and Oliver, J. D. (2004). Role of catalase and oxyR in the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol. Ecol. 50, 133-142. doi: 10.1016/j.femsec.2004.06.004.
127. Krasteva, P. V., Fong, J. C., Shikuma, N. J., Beyhan, S., Navarro, M. V., Yildiz, F. H., et al. (2010). Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327, 866-868. doi: 10.1126/science.1181185.
128. Lama, J. R., Seas, C. R., León-Barúa, R., Gotuzzo, E., and Sack, R. B. (2011). Environmental temperature, cholera, and acute diarrhoea in adults in Lima, Peru. J. Health Popul. Nutr. 22, 399-403.
129. Leal, N. C., De Araújo Figueiroa, â. C. T., Cavalcanti, V. O., Da Silva, S. C., Leal-Balbino, T. C., De Almeida, A. M. P., et al. (2008). Characterization of Vibrio cholerae isolated from the aquatic basins of the State of Pernambuco, Brazil. Trans. R. Soc. Trop. Med. Hyg. 102, 272-276. doi: 10.1016/j.trstmh.2007.12.008.
130. Lipp, E. K., Rivera, I. N., Gil, A. I., Espeland, E. M., Choopun, N., Louis, V. R., et al. (2003). Direct detection of Vibrio cholerae and ctxA in Peruvian coastal water and plankton by PCR. Appl. Environ. Microbiol. 69, 3676-3680. doi: 10.1128/AEM.69.6.3676-3680.2003.
131. Liu, Z., Stirling, F. R., and Zhu, J. (2007). Temporal quorum-sensing induction regulates Vibrio cholerae biofilm architecture. Infect. Immun. 75, 122-126. doi: 10.1128/IAI.01190-06.
132. Lizárraga-Partida, M. L., Mendez-Gomez, E., Rivas-Montano, A. M., Vargas-Hernandez, E., Portillo-Lopez, A., Gonzalez-Ramirez, A. R., et al. (2009). Association of Vibrio cholerae with plankton in coastal areas of Mexico. Environ. Microbiol. 11, 201-208. doi: 10.1111/j.1462-2920.2008.01753.x.
133. Lo Scrudato, M., and Blokesch, M. (2012). The regulatory network of natural competence and transformation of Vibrio cholerae. PLoS Genet. 8:e1002778. doi:10.1371/journal.pgen.1002778.
134. Lobitz, B., Beck, L., Huq, A., Wood, B., Fuchs, G., Faruque, A. S., et al. (2000). Climate and infectious disease: use of remote sensing for detection of Vibrio cholerae by indirect measurement. Proc. Natl. Acad. Sci. U.S.A. 97, 1438-1443. doi: 10.1073/pnas.97.4.1438.
135. Lock, R., Öhman, L., and Dahlgren, C. (1987). Phagocytic recognition mechanisms in human granulocytes and Acanthamoeba castellanii using type 1 fimbriated Escherichia coli as phagocytic prey. FEMS Microbiol. Lett. 44, 135-140.
136. Louis, V. R., Russek-Cohen, E., Choopun, N., Rivera, I. N. G., Gangle, B., Jiang, S. C., et al. (2003). Predictability of Vibrio cholerae in Chesapeake Bay. Appl. Environ. Microbiol. 69, 2773-2785. doi: 10.1128/AEM.69.5.2773-2785.2003.
137. Macek, M., Carlos, G., Memije, P., and Ramãrez, P. (1997). Ciliate-Vibrio cholerae interactions within a microbial loop: an experimental study. Aquat. Microb. Ecol. 13, 257-266. doi: 10.3354/ame013257.
138. MacIntyre, D. L., Miyata, S. T., Kitaoka, M., and Pukatzki, S. (2010). The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl. Acad. Sci. U.S.A. 107, 19520-19524. doi: 10.1073/pnas.1012931107.
139. Maina, A. N., Mwaura, F. B., Oyugi, J., Goulding, D., Toribio, A. L., and Kariuki, S. (2013). Characterization of Vibrio cholerae bacteriophages isolated from the environmental waters of the Lake Victoria region of Kenya. Curr. Microbiol. 1-7. [Epub ahead of print].
140. Martin, J. H. (1992). "Iron as a limiting factor in oceanic productivity," in Primary Productivity and Biogeochemical Cycles in the Sea, eds P. Falkowski and A. Woodhead (New York: Plenum Press), 123-137.
141. Martin, J. H., and Michael Gordon, R. (1988). Northeast Pacific iron distributions in relation to phytoplankton productivity. Deep-Sea Res. 35, 177-196. doi: 10.1016/0198-0149(88)90035-0.
142. Martinelli Filho, J. E., Lopes, R. M., Rivera, I. N. G., and Colwell, R. R. (2010). Vibrio cholerae O1 detection in estuarine and coastal zooplankton. J. Plankton Res. 33, 51-62. doi: 10.1093/plankt/fbq093.
143. Martínez, J. P., Falomir, M. P., and Gozalbo, D. (2009). "Chitin: a structural biopolysaccharide," in eLS. John Wiley & Sons, Ltd.
144. Martínez Pérez, M. E., Macek, M., and Castro Galván, M. T. (2004). Do protozoa control the elimination of Vibrio cholerae in brackish water? Int. Rev. Hydrobiol. 89, 215-227. doi: 10.1002/iroh.200310644.
145. Matz, C., and Kjelleberg, S. (2005). Off the hook-how bacteria survive protozoan grazing. Trends Microbiol. 13, 302-307. doi: 10.1016/j.tim.2005.05.009.
146. Matz, C., McDougald, D., Moreno, A. M., Yung, P. Y., Yildiz, F. H., and Kjelleberg, S. (2005). Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 102, 16819-16824. doi: 10.1073/pnas.0505350102.
147. Maugeri, T., Caccamo, D., and Gugliandolo, C. (2001). Potentially pathogenic Vibrios in brackish waters and mussels. J. Appl. Microbiol. 89, 261-266. doi: 10.1046/j.1365-2672.2000.01096.x.
148. McDougald, D., Rice, S. A., and Kjelleberg, S. (1999). New perspectives on the viable but nonculturable response. Biologia-bratislava 54, 617-624.
149. McDougald, D., Rice, S. A., Weichart, D., and Kjelleberg, S. (1998). Nonculturability: adaptation or debilitation? FEMS Microbiol. Ecol. 25, 1-9. doi: 10.1111/j.1574-6941.1998.tb00455.x.
150. Meibom, K. L., Li, X. B., Nielsen, A. T., Wu, C. Y., Roseman, S., and Schoolnik, G. K. (2004). The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. U.S.A. 101, 2524-2529. doi: 10.1073/pnas.0308707101.
151. Merrell, D. S., and Camilli, A. (1999). The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol. Microbiol. 34, 836-849. doi: 10.1046/j.1365-2958.1999.01650.x.
152. Miller, V. L., and Mekalanos, J. J. (1988). A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170, 2575-2583.
153. Mishra, A., Taneja, N., and Sharma, M. (2012). Viability kinetics, induction, resuscitation and quantitative real-time polymerase chain reaction analyses of viable but nonculturable Vibrio cholerae O1 in freshwater microcosm. J. Appl. Microbiol. 112, 945-953. doi: 10.1111/j.1365-2672.2012.05255.x.
154. Mitta, G., Vandenbulcke, F., and Roch, P. (2000). Original involvement of antimicrobial peptides in mussel innate immunity. FEBS Lett. 486, 185-190. doi: 10.1016/S0014-5793(00)02192-X.
155. Miyagi, K., Nakano, T., Yagi, T., Hanafusa, M., Imura, S., Honda, T., et al. (2003). Survey of Vibrio cholerae O1 and its survival over the winter in marine water of Port of Osaka. Epidemiol. Infect. 131, 613-619. doi: 10.1017/S0950268803008756.
156. Miyata, S. T., Kitaoka, M., Brooks, T. M., McAuley, S. B., and Pukatzki, S. (2011). Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum. Infect. Immun. 79, 2941-2949. doi: 10.1128/IAI.01266-10.
157. Miyata, S. T., Kitaoka, M., Wieteska, L., Frech, C., Chen, N., and Pukatzki, S. (2010). The Vibrio cholerae type VI secretion system: evaluating its role in the human disease cholera. Front. Microbiol. 1:117. doi:10.3389/fmicb.2010.00117.
158. Mizunoe, Y., Wai, S. N., Takade, A., and Yoshida, S. I. (1999). Restoration of culturability of starvation-stressed and low-temperature-stressed Escherichia coli O157 cells by using H2O2-degrading compounds. Arch. Microbiol. 172, 63-67. doi: 10.1007/s002030050741.
159. Moorthy, S., and Watnick, P. I. (2004). Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Mol. Microbiol. 52, 573-587. doi: 10.1111/j.1365-2958.2004.04000.x.
160. Morris, J. G. Jr., Sztein, M. B., Rice, E. W., Nataro, J. P., Losonsky, G. A., Panigrahi, P., et al. (1996). Vibrio cholerae O1 can assume a chlorine-resistant rugose survival form that is virulent for humans. J. Infect. Dis. 174, 1364-1368. doi: 10.1093/infdis/174.6.1364.
161. Mouriño-Pérez, R. R., Worden, A. Z., and Azam, F. (2003). Growth of Vibrio cholerae O1 in red tide waters off California. Appl. Environ. Microbiol. 69, 6923-6931. doi: 10.1128/AEM.69.11.6923-6931.2003.
162. Muller, J., Miller, M. C., Nielsen, A. T., Schoolnik, G. K., and Spormann, A. M. (2007). vpsA-and luxO-independent biofilms of Vibrio cholerae. FEMS Microbiol. Lett. 275, 199-206. doi: 10.1111/j.1574-6968.2007.00884.x.
163. Murphree, R. L., and Tamplin, M. L. (1995). Uptake and retention of Vibrio cholerae O1 in the Eastern oyster, Crassostrea virginica. Appl. Environ. Microbiol. 61, 3656-3660.
164. Nalin, D., Daya, V., Reid, A., Levine, M., and Cisneros, L. (1979). Adsorption and growth of Vibrio cholerae on chitin. Infect. Immun. 25, 768-770.
165. Nesper, J., Lauriano, C. M., Klose, K. E., Kapfhammer, D., Kraiss, A., and Reidl, J. (2001). Characterization of Vibrio cholerae O1 El Tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect. Immun. 69, 435-445. doi: 10.1128/IAI.69.1.435-445.2001.
166. Nilsson, L., Oliver, J., and Kjelleberg, S. (1991). Resuscitation of Vibrio vulnificus from the viable but nonculturable state. J. Bacteriol. 173, 5054-5059.
167. Ogawa, N., Tzeng, C. M., Fraley, C. D., and Kornberg, A. (2000). Inorganic polyphosphate in Vibrio cholerae: genetic, biochemical, and physiologic features. J. Bacteriol. 182, 6687-6693. doi: 10.1128/JB.182.23.6687-6693.2000.
168. Ogg, J. E., Ryder, R. A., and Smith, H. L. Jr. (1989). Isolation of Vibrio cholerae from aquatic birds in Colorado and Utah. Appl. Environ. Microbiol. 55, 95-99.
169. Olafsen, J. A., Mikkelsen, H. V., Giæver, H. M., and Høvik Hansen, G. (1993). Indigenous bacteria in hemolymph and tissues of marine bivalves at low temperatures. Appl. Environ. Microbiol. 59, 1848-1854.
170. Oliver, J. D. (2005). The viable but nonculturable state in bacteria. J. Microbiol. 43, 93-100.
171. Oliver, J. D. (2010). Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev. 34, 415-425.
172. Oliver, J. D., Hite, F., McDougald, D., Andon, N. L., and Simpson, L. M. (1995). Entry into, and resuscitation from, the viable but nonculturable state by Vibrio vulnificus in an estuarine environment. Appl. Environ. Microbiol. 61, 2624-2630.
173. Pearson, G. D., Woods, A., Chiang, S. L., and Mekalanos, J. J. (1993). CTX genetic element encodes a site-specific recombination system and an intestinal colonization factor. Proc. Natl. Acad. Sci. U.S.A. 90, 3750-3754. doi: 10.1073/pnas.90.8.3750.
174. Pollitzer, R. (1954). History of the disease. Cholera. Bull. World Health Organ. 10, 421.
175. Pratt, J. T., McDonough, E., and Camilli, A. (2009). PhoB regulates motility, biofilms, and cyclic di-GMP in Vibrio cholerae. J. Bacteriol. 191, 6632-6642. doi: 10.1128/JB.00708-09.
176. Preiss, J., and Romeo, T. (1994). Molecular biology and regulatory aspects of glycogen biosynthesis in bacteria. Prog. Nucleic Acid Res. Mol. Biol. 47, 299-329. doi: 10.1016/S0079-6603(08)60255-X.
177. Pruzzo, C., Gallo, G., and Canesi, L. (2005). Persistence of Vibrios in marine bivalves: the role of interactions with haemolymph components. Environ. Microbiol. 7, 761-772. doi: 10.1111/j.1462-2920.2005.00792.x.
178. Pruzzo, C., Tarsi, R., Del Mar Lleò, M., Signoretto, C., Zampini, M., Pane, L., et al. (2003). Persistence of adhesive properties in Vibrio cholerae after long-term exposure to sea water. Environ. Microbiol. 5, 850-858. doi: 10.1046/j.1462-2920.2003.00498.x.
179. Pruzzo, C., Vezzulli, L., and Colwell, R. R. (2008). Global impact of Vibrio cholerae interactions with chitin. Environ. Microbiol. 10, 1400-1410. doi: 10.1111/j.1462-2920.2007.01559.x.
180. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant, D., and Mekalanos, J. J. (2007). Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. U.S.A. 104, 15508-15513. doi: 10.1073/pnas.0706532104.
181. Pukatzki, S., Ma, A. T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W. C., et al. (2006). Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. U.S.A. 103, 1528-1533. doi: 10.1073/pnas.0510322103.
182. Rashid, A., Haley, B. J., Rajabov, M., Ahmadova, S., Gurbanov, S., Colwell, R. R., et al. (2013). Detection of Vibrio cholerae in environmental waters including drinking water reservoirs of Azerbaijan. Environ. Microbiol. Rep. 5, 30-38. doi: 10.1111/j.1758-2229.2012.00369.x.
183. Ravel, J., Knight, I. T., Monahan, C. E., Hill, R. T., and Colwell, R. R. (1995). Temperature-induced recovery of Vibrio cholerae from the viable but nonculturable state: growth or resuscitation? Microbiology 141, 377-383. doi: 10.1099/13500872-141-2-377.
184. Rawlings, T. K., Ruiz, G. M., and Colwell, R. R. (2007). Association of Vibrio cholerae O1 El Tor and O139 Bengal with the Copepods Acartia tonsa and Eurytemora affinis. Appl. Environ. Microbiol. 73, 7926-7933. doi: 10.1128/AEM.01238-07.
185. Reguera, G., and Kolter, R. (2005). Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin. J. Bacteriol. 187, 3551-3555. doi: 10.1128/JB.187.10.3551-3555.2005.
186. Rice, E. W., Johnson, C. J., Clark, R. M., Fox, K. R., Reasoner, D. J., Dunnigan, M. E., et al. (1992). Chlorine and survival of "rugose" Vibrio cholerae. Lancet 340, 740. doi: 10.1016/0140-6736(92)92289-R.
187. Rinaudo, M. (2006). Chitin and chitosan: properties and applications. Prog. Polym. Sci. 31, 603-632. doi: 10.1016/j.progpolymsci.2006.06.001.
188. Rowbotham, T. J. (1980). Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33, 1179-1183. doi: 10.1136/jcp.33.12.1179.
189. Sá, L. L. C., Vale, E. R. V., Garza, D. R., and Vicente, A. C. P. (2012). Vibrio cholerae O1 from superficial water of the Tucunduba Stream, Brazilian Amazon. Braz. J. Microbiol. 43, 635-638. doi: 10.1590/S1517-83822012000200027.
190. Sack, D. A., Sack, R. B., Nair, G. B., and Siddique, A. K. (2004). Cholera. Lancet 363, 223-233. doi: 10.1016/S0140-6736(03)15328-7.
191. Sandström, G., Saeed, A., and Abd, H. (2010). Acanthamoeba polyphaga is a possible host for Vibrio cholerae in aquatic environments. Exp. Parasitol. 126, 65-68. doi: 10.1016/j.exppara.2009.09.021.
192. Schuster, B. M., Tyzik, A. L., Donner, R. A., Striplin, M. J., Almagro-Moreno, S., Jones, S. H., et al. (2011). Ecology and genetic structure of a northern temperate Vibrio cholerae population related to toxigenic isolates. Appl. Environ. Microbiol. 77, 7568-7575. doi: 10.1128/AEM.00378-11.
193. Seed, K. D., Bodi, K. L., Kropinski, A. M., Ackermann, H. W., Calderwood, S. B., Qadri, F., et al. (2011). Evidence of a dominant lineage of Vibrio cholerae-specific lytic bacteriophages shed by cholera patients over a 10-year period in Dhaka, Bangladesh. MBio 2. doi:10.1128/mBio.00334-10.
194. Seeligmann, C. T., Mirande, V., Tracanna, B. C., Silva, C., Aulet, O., Cecilia, M., et al. (2008). Phytoplankton-linked viable non-culturable Vibrio cholerae O1 (VNC) from rivers in Tucumán, Argentina. J. Plankton Res. 30, 367-377. doi: 10.1093/plankt/fbn008.
195. Sen, A., and Ghosh, A. N. (2005). New Vibrio cholerae O1 biotype El Tor bacteriophages. Virol. J. 2, 28. doi: 10.1186/1743-422X-2-28.
196. Senderovich, Y., Izhaki, I., and Halpern, M. (2010). Fish as reservoirs and vectors of Vibrio cholerae. PLoS ONE 5:e8607. doi:10.1371/journal.pone.0008607.
197. Senoh, M., Ghosh-Banerjee, J., Ramamurthy, T., Hamabata, T., Kurakawa, T., Takeda, M., et al. (2010). Conversion of viable but nonculturable Vibrio cholerae to the culturable state by co-culture with eukaryotic cells. Microbiol. Immunol. 54, 502-507. doi: 10.1111/j.1348-0421.2010.00245.x.
198. Seper, A., Fengler, V. H. I., Roier, S., Wolinski, H., Kohlwein, S. D., Bishop, A. L., et al. (2011). Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Mol. Microbiol. 82, 1015-1037. doi: 10.1111/j.1365-2958.2011.07867.x.
199. Shikuma, N. J., and Hadfield, M. G. (2010). Marine biofilms on submerged surfaces are a reservoir for Escherichia coli and Vibrio cholerae. Biofouling 26, 39-46. doi: 10.1080/08927010903282814.
200. Singh, R., Narayan, V., McLenachan, P., Winkworth, R. C., Mitra, S., Lockhart, P. J., et al. (2012). Detection and diversity of pathogenic Vibrio from Fiji. Environ. Microbiol. Rep. 4, 403-411. doi: 10.1111/j.1758-2229.2012.00344.x.
201. Singleton, F. L., Attwell, R. W., Jangi, M. S., and Colwell, R. R. (1982). Influence of salinity and organic nutrient concentration on survival and growth of Vibrio cholerae in aquatic microcosms. Appl. Environ. Microbiol. 43, 1080-1085.
202. Snow, J. (1855). On the Mode of Communication of Cholera. New Burlington Street, London: John Churchill.
203. Srivastava, D., Harris, R. C., and Waters, C. M. (2011). Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae. J. Bacteriol. 193, 6331-6341. doi: 10.1128/JB.05167-11.
204. Srivastava, D., and Waters, C. M. (2012). A tangled web: regulatory connections between quorum sensing and cyclic di-GMP. J. Bacteriol. 194, 4485-4493. doi: 10.1128/JB.00379-12.
205. Stauder, M., Vezzulli, L., Pezzati, E., Repetto, B., and Pruzzo, C. (2010). Temperature affects Vibrio cholerae O1 El Tor persistence in the aquatic environment via an enhanced expression of GbpA and MSHA adhesins. Environ. Microbiol. Rep. 2, 140-144. doi: 10.1111/j.1758-2229.2009.00121.x.
206. Stocker, R., and Seymour, J. R. (2012). Ecology and physics of bacterial chemotaxis in the ocean. Microbiol. Mol. Biol. Rev. 76, 792-812. doi: 10.1128/MMBR.00029-12.
207. Sultan, S. Z., Silva, A. J., and Benitez, J. A. (2010). The PhoB regulatory system modulates biofilm formation and stress response in El Tor biotype Vibrio cholerae. FEMS Microbiol. Lett. 302, 22-31. doi: 10.1111/j.1574-6968.2009.01837.x.
208. Sun, S., Kjelleberg, S., and McDougald, D. (2013). Relative contributions of Vibrio polysaccharide and quorum sensing to the resistance of Vibrio cholerae to predation by heterotrophic protists. PLoS ONE 8:e56338. doi:10.1371/journal.pone.0056338.
209. Tall, A., Hervio-Heath, D., Teillon, A., Boisset-Helbert, C., Delesmont, R., Bodilis, J., et al. (2013). Diversity of Vibrio spp. isolated at ambient environmental temperature in the eastern English Channel as determined by pyrH sequencing. J. Appl. Microbiol. 114, 1713-1724. doi: 10.1111/jam.12181.
210. Talledo, M., Rivera, I. N., Lipp, E. K., Neale, A., Karaolis, D., Huq, A., et al. (2003). Characterization of a Vibrio cholerae phage isolated from the coastal water of Peru. Environ. Microbiol. 5, 350-354. doi: 10.1046/j.1462-2920.2003.00411.x.
211. Tamplin, M., Gauzens, A., Huq, A., Sack, D., and Colwell, R. R. (1990). Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl. Environ. Microbiol. 56, 1977-1980.
212. Taviani, E., Ceccarelli, D., Lazaro, N., Bani, S., Cappuccinelli, P., Colwell, R. R., et al. (2008). Environmental Vibrio spp., isolated in Mozambique, contain a polymorphic group of integrative conjugative elements and class 1 integrons. FEMS Microbiol. Ecol. 64, 45-54. doi: 10.1111/j.1574-6941.2008.00455.x.
213. Thom, S., Warhurst, D., and Drasar, B. S. (1992). Association of Vibrio cholerae with fresh water amoebae. J. Med. Microbiol. 36, 303-306. doi: 10.1099/00222615-36-5-303.
214. Thomas, K. U., Joseph, N., Raveendran, O., and Nair, S. (2006). Salinity-induced survival strategy of Vibrio cholerae associated with copepods in Cochin backwaters. Mar. Pollut. Bull. 52, 1425-1430. doi: 10.1016/j.marpolbul.2006.04.011.
215. Turner, J. W., Good, B., Cole, D., and Lipp, E. K. (2009). Plankton composition and environmental factors contribute to Vibrio seasonality. ISME J. 3, 1082-1092. doi: 10.1038/ismej.2009.50.
216. Turner, J. W., Malayil, L., Guadagnoli, D., Cole, D., and Lipp, E. K. (2013). Detection of Vibrio parahaemolyticus, Vibrio vulnificus and Vibrio cholerae with respect to seasonal fluctuations in temperature and plankton abundance. Environ. Microbiol. doi:10.1111/1462-2920.12246 [Epub ahead of print].
217. Unterweger, D., Kitaoka, M., Miyata, S. T., Bachmann, V., Brooks, T. M., Moloney, J., et al. (2012). Constitutive type VI secretion system expression gives Vibrio cholerae intra-and interspecific competitive advantages. PLoS ONE 7:e48320. doi:10.1371/journal.pone.0048320.
218. Vaitkevicius, K., Lindmark, B., Ou, G., Song, T., Toma, C., Iwanaga, M., et al. (2006). A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing. Proc. Natl. Acad. Sci. U.S.A. 103, 9280-9285. doi: 10.1073/pnas.0601754103.
219. Valeru, S., Wai, S., Saeed, A., Sandström, G., and Abd, H. (2012). ToxR of Vibrio cholerae affects biofilm, rugosity and survival with Acanthamoeba castellanii. BMC Res. Notes 5:33. doi:10.1186/1756-0500-5-33.
220. Valeru, S. P., Rompikuntal, P. K., Ishikawa, T., Vaitkevicius, K., Sjoling, A., Dolganov, N., et al. (2009). Role of melanin pigment in expression of Vibrio cholerae virulence factors. Infect. Immun. 77, 935-942. doi: 10.1128/IAI.00929-08.
221. Vezzulli, L., Brettar, I., Pezzati, E., Reid, P. C., Colwell, R. R., Höfle, M. G. et al. (2011). Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios. ISME J. 6, 21-30. doi: 10.1038/ismej.2011.89.
222. Vezzulli, L., Pezzati, E., Moreno, M., Fabiano, M., Pane, L., Pruzzo, C., et al. (2009). Benthic ecology of Vibrio spp. and pathogenic Vibrio species in a coastal Mediterranean environment (La Spezia Gulf, Italy). Microb. Ecol. 58, 808-818. doi: 10.1007/s00248-009-9542-8.
223. Vezzulli, L., Pruzzo, C., Huq, A., and Colwell, R. R. (2010). Environmental reservoirs of Vibrio cholerae and their role in cholera. Environ. Microbiol. Rep. 2, 27-33. doi: 10.1111/j.1758-2229.2009.00128.x.
224. Vimala, B., Thong, K. L., and Chong, V. (2010). Isolation, detection and genomic differentiation of Vibrio cholerae and Vibrio parahaemolyticus in Bachok, Kelantan. Malays. J. Sci. 29, 1-10.
225. Vugia, D. J., Shefer, A. M., Douglas, J., Greene, K. D., Bryant, R. G., and Werner, S. B. (1997). Cholera from raw seaweed transported from the Philippines to California. J. Clin. Microbiol. 35, 284-285.
226. Wackett, L., Orme-Johnson, W., and Walsh, C. (1989). "Transition metal enzymes in bacterial metabolism," in Metal Ions and Bacteria, eds T. J. Beveridge and R. J. Doyle (New York, NY: Wiley-Interscience), 165-206.
227. Wai, S. N., Mizunoe, Y., Takade, A., Kawabata, S. I., and Yoshida, S. I. (1998). Vibrio cholerae O1 Strain TSI-4 produces the exopolysaccharide materials that determine colony morphology, stress resistance, and biofilm formation. Appl. Environ. Microbiol. 64, 3648-3655.
228. Waldor, M. K., and Mekalanos, J. J. (1996). Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910-1914. doi: 10.1126/science.272.5270.1910.
229. Watnick, P. I., and Kolter, R. (1999). Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34, 586-595. doi: 10.1046/j.1365-2958.1999.01624.x.
230. Watnick, P. I., Lauriano, C. M., Klose, K. E., Croal, L., and Kolter, R. (2001). The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol. Microbiol. 39, 223-235. doi: 10.1046/j.1365-2958.2001.02195.x.
231. Wei, Y., Kirby, A., and Levin, B. R. (2011). The population and evolutionary dynamics of Vibrio cholerae and its bacteriophage: conditions for maintaining phage-limited communities. Am. Nat. 178, 715-725. doi: 10.1086/662677.
232. Weichart, D., McDougald, D., Jacobs, D., and Kjelleberg, S. (1997). In situ analysis of nucleic acids in cold-induced nonculturable Vibrio vulnificus. Appl. Environ. Microbiol. 63, 2754-2758.
233. Winiecka-Krusnell, J., and Linder, E. (2001). Bacterial infections of free-living amoebae. Res. Microbiol. 152, 613-619. doi: 10.1016/S0923-2508(01)01240-2.
234. Worden, A. Z., Seidel, M., Smriga, S., Wick, A., Malfatti, F., Bartlett, D., et al. (2006). Trophic regulation of Vibrio cholerae in coastal marine waters. Environ. Microbiol. 8, 21-29. doi: 10.1111/j.1462-2920.2005.00863.x.
235. Wright, A. C., and Harwood, V. J. (2013). "Vibrios," in Foodborne Infections and Intoxications, 4th Edn, eds J. M. Glenn and P. Morris (San Diego: Academic Press), 113-128.
236. Wyckoff, E. E., Mey, A. R., Leimbach, A., Fisher, C. F., and Payne, S. M. (2006). Characterization of ferric and ferrous iron transport systems in Vibrio cholerae. J. Bacteriol. 188, 6515-6523. doi: 10.1128/JB.00626-06.
237. Wyckoff, E. E., Mey, A. R., and Payne, S. M. (2007). Iron acquisition in Vibrio cholerae. Biometals 20, 405-416. doi: 10.1007/s10534-006-9073-4.
238. Xu, H. S., Roberts, N., Singleton, F. L., Attwell, R. W., Grimes, D. J., and Colwell, R. R. (1982). Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8, 313-323. doi: 10.1007/BF02010671.
239. Yamamoto, S., Okujo, N., Fujita, Y., Saito, M., Yoshida, T., and Shinoda, S. (1993). Structures of two polyamine-containing catecholate siderophores from Vibrio fluvialis. J. Biochem. 113, 538-544.
240. Yamguchi, T., Ikawa, T., and Nisizawa, K. (1969). Pathway of mannitol formation during photosynthesis in brown algae. Plant Cell Physiol. 10, 425-440.
241. Yildiz, F. H. (2008). Cyclic dimeric GMP signaling and regulation of surface-associated developmental programs. J. Bacteriol. 190, 781-783. doi: 10.1128/JB.01852-07.
242. Yildiz, F. H., Dolganov, N. A., and Schoolnik, G. K. (2001). VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPS(ETr)-associated phenotypes in Vibrio cholerae O1 El Tor. J. Bacteriol. 183, 1716-1726. doi: 10.1128/JB.183.5.1716-1726.2001.
243. Yildiz, F. H., Liu, X. S., Heydorn, A., and Schoolnik, G. K. (2004). Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol. Microbiol. 53, 497-515. doi: 10.1111/j.1365-2958.2004.04154.x.
244. Yildiz, F. H., and Schoolnik, G. K. (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. U.S.A. 96, 4028-4033. doi: 10.1073/pnas.96.7.4028.
245. Yildiz, F. H., and Visick, K. L. (2009). Vibrio biofilms: so much the same yet so different. Trends Microbiol. 17, 109-118. doi: 10.1016/j.tim.2008.12.004.
246. Ymele-Leki, P., Houot, L., and Watnick, P. I. (2013). Mannitol and the mannitol-specific enzyme IIB subunit activate Vibrio cholerae biofilm formation. Appl. Environ. Microbiol. 79, 4675-4683. doi: 10.1128/AEM.01184-13.
247. Zhu, J., and Mekalanos, J. J. (2003). Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 5, 647-656. doi: 10.1016/S1534-5807(03)00295-8.
248. Zhu, J., Miller, M. B., Vance, R. E., Dziejman, M., Bassler, B. L., and Mekalanos, J. J. (2002). Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. U.S.A. 99, 3129-3134. doi: 10.1073/pnas.052694299.