To cause the diarrheal disease cholera, Vibrio cholerae must effectively colonize the small intestine. In order to do so, the bacterium needs to successfully travel through the stomach and withstand the presence of agents such as bile and antimicrobial peptides in the intestinal lumen and mucus. The bacterial cells penetrate the viscous mucus layer covering the epithelium and attach and proliferate on its surface. In this review, we discuss recent developments and known aspects of the early stages of V. cholerae intestinal colonization and highlight areas that remain to be fully understood. We propose mechanisms and postulate a model that covers some of the steps that are required in order for the bacterium to efficiently colonize the human host. A deeper understanding of the colonization dynamics of V. cholerae and other intestinal pathogens will provide us with a variety of novel targets and strategies to avoid the diseases caused by these organisms.
Vyšlo v časopise: Intestinal Colonization Dynamics of. PLoS Pathog 11(5): e32767. doi:10.1371/journal.ppat.1004787 Kategorie: Review prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004787
1. Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB (2012) Cholera. Lancet 379 : 2466–2476. doi: 10.1016/S0140-6736(12)60436-X 22748592
2. CDC (2015) Centers for Disease Control and Prevention. http://www.cdc.gov/
3. Ministère de la Santé Publique et de la Population (2015) Ministère de la Santé Publique et de la Population. http://mspp.gouv.ht/newsite/
4. Lutz C, Erken M, Noorian P, Sun S, McDougald D (2013) Environmental reservoirs and mechanisms of persistence of Vibrio cholerae. Front Microbiol 4 : 375. doi: 10.3389/fmicb.2013.00375 24379807
5. Almagro-Moreno S, Taylor RK (2013) Cholera: Environmental reservoirs and impact on disease transmission. Microbiol Spectrum 1(2):OH-0003-2012.
6. Kaper JB, Morris JG, Levine MM (1995) Cholera. Clin Microbiol Rev 8 : 48–86. 7704895
7. Merrell DS, Hava DL, Camilli A (2002) Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Mol Microbiol 43 : 1471–1491. 11952899
8. Merrell DS, Bailey C, Kaper JB, Camilli A (2001) The ToxR-mediated organic acid tolerance response of Vibrio cholerae requires OmpU. J Bacteriol 183 : 2746–2754. 11292792
9. Merrell DS, Camilli A (2000) Regulation of Vibrio cholerae genes required for acid tolerance by a member of the “ToxR-Like” family of transcriptional regulators. J Bacteriol 182 : 5342–5350. 10986235
10. Kovacikova G, Lin W, Skorupski K (2010) The LysR-type virulence activator AphB regulates the expression of genes in Vibrio cholerae in response to low pH and anaerobiosis. J Bacteriol 192 : 4181–4191. doi: 10.1128/JB.00193-10 20562308
11. Cash RA, Music SI, Libonati JP, Snyder MJ, Wenzel RP, et al. (1974) Response of man to infection with Vibrio cholerae. I. Clinical, serologic, and bacteriologic responses to a known inoculum. J Infect Dis 129 : 45–52. 4809112
12. Levine MM, Black RE, Clements ML, Nalin DR, Cisneros L, et al. (1981) Volunteer studies in development of vaccines against cholera and enterotoxigenic Escherichia coli: a review. In: Holme T, Holmgren J, Merson MH, Mollby R, editors. Acute enteric infections in children. New prospects for treatment and prevention. Amsterdam: Elsevier/North-Holland Biomedical Press. pp. 443–459.
13. Sack GH, Pierce NF, Hennessey KN, Mitra RC, Sack RB, et al. (1972) Gastric acidity in cholera and noncholera diarrhoea. Bull World Health Organ 47 : 31–36. 20604412
14. Nalin DR, Levine RJ, Levine MM, Hoover D, Bergquist E, et al. (1978) Cholera, non-vibrio cholera, and stomach acid. Lancet 2 : 856–859. 81410
15. Van Loon FP, Clemens JD, Shahrier M, Sack DA, Stephensen CB, et al. (1990) Low gastric acid as a risk factor for cholera transmission: application of a new non-invasive gastric acid field test. J Clin Epidemiol 43 : 1361–1367. 2254773
16. Colwell RR, Brayton PR, Grimes DJ, Roszak DB, Huq SA, et al. (1985) Viable but non-culturable Vibrio cholerae and related pathogens in the environment: Implications for release of genetically engineered microorganisms. Nat Biotechnol 3 : 817–820.
17. Alam M, Sultana M, Nair GB, Siddique AK, Hasan NA, 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 USA 104 : 17801–17806. 17968017
18. Colwell RR, Brayton P, Herrington D, Tall B, Huq A, et al. (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 24415083
19. Asakura H, Ishiwa A, Arakawa E, Makino S-I, Okada Y, et al. (2007) Gene expression profile of Vibrio cholerae in the cold stress-induced viable but non-culturable state. Environ Microbiol 9 : 869–879. 17359259
20. Wong HC, Wang P (2004) Induction of viable but nonculturable state in Vibrio parahaemolyticus and its susceptibility to environmental stresses. J Appl Microbiol 96 : 359–366. 14723697
21. Merrell DS, Butler SM, Qadri F, Dolganov NA, Alam A, et al. (2002) Host-induced epidemic spread of the cholera bacterium. Nature 417 : 642–645. 12050664
22. Nielsen AT, Dolganov NA, Rasmussen T, Otto G, Miller MC, et al. (2010) A bistable switch and anatomical site control Vibrio cholerae virulence gene expression in the intestine. PLoS Pathog 6: e1001102. doi: 10.1371/journal.ppat.1001102 20862321
23. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ (1987) Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci USA 84 : 2833–2837. 2883655
24. O'Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54 : 49–79. 11018124
25. Faruque SM, Biswas K, Udden SMN, Ahmad QS, Sack DA, et al. (2006) Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc Natl Acad Sci USA 103 : 6350–6355. 16601099
26. Tamayo R, Patimalla B, Camilli A (2010) Growth in a Biofilm Induces a Hyperinfectious Phenotype in Vibrio cholerae. Infect Immun 78 : 3560–3569. doi: 10.1128/IAI.00048-10 20515927
27. Hung DT, Zhu J, Sturtevant D, Mekalanos JJ (2006) Bile acids stimulate biofilm formation in Vibrio cholerae. Mol Microbiol 59 : 193–201. 16359328
28. Hay AJ, Zhu J (2015) Host intestinal signal-promoted biofilm dispersal induces Vibrio cholerae colonization. Infect Immun 83 : 317–323. doi: 10.1128/IAI.02617-14 25368110
29. Provenzano D, Schuhmacher DA, Barker JL, Klose KE (2000) The virulence regulatory protein ToxR mediates enhanced bile resistance in Vibrio cholerae and other pathogenic Vibrio species. Infect Immun 68 : 1491–1497. 10678965
30. Mathur J, Waldor MK (2004) The Vibrio cholerae ToxR-regulated porin OmpU confers resistance to antimicrobial peptides. Infect Immun 72 : 3577–3583. 15155667
31. Colwell RR, Huq A, Islam MS, Aziz KMA, Yunus M, et al. (2003) Reduction of cholera in Bangladeshi villages by simple filtration. Proc Natl Acad Sci USA 100 : 1051–1055. 12529505
32. Huq A, Yunus M, Sohel SS, Bhuiya A, Emch M, et al. (2010) Simple sari cloth filtration of water is sustainable and continues to protect villagers from cholera in Matlab, Bangladesh. mBio 1 : 1e00034–10
33. Colwell RR, Huq A (1994) Environmental reservoir of Vibrio cholerae. The causative agent of cholera. Ann N Y Acad Sci 740 : 44–54. 7840478
34. Faruque SM (2006) Transmissibility of cholera: In vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc Natl Acad Sci USA 103 : 6350–6355. 16601099
35. Liu Z, Miyashiro T, Tsou A, Hsiao A, Goulian M, et al. (2008) Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. Proc Natl Acad Sci USA 105 : 9769–9774. doi: 10.1073/pnas.0802241105 18606988
36. Lee SH, Butler SM, Camilli A (2001) Selection for in vivo regulators of bacterial virulence. Proc Natl Acad Sci USA 98 : 6889–6894. 11391007
37. Guentzel MN, Berry LJ (1975) Motility as a virulence factor for Vibrio cholerae. Infect Immun 11 : 890–897. 1091563
38. Millet YA, Alvarez D, Ringgaard S, Andrian von UH, Davis BM, et al. (2014) Insights into Vibrio cholerae intestinal colonization from monitoring fluorescently labeled bacteria. PLoS Pathog 10: e1004405. doi: 10.1371/journal.ppat.1004405 25275396
39. Brown II, Häse CC (2001) Flagellum-independent surface migration of Vibrio cholerae and Escherichia coli. J Bacteriol 183 : 3784–3790. 11371543
40. Freter R, O'Brien PC (1981) Role of chemotaxis in the association of motile bacteria with intestinal mucosa: fitness and virulence of nonchemotactic Vibrio cholerae mutants in infant mice. Infect Immun 34 : 222–233. 7298184
41. Butler SM, Camilli A (2004) Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc Natl Acad Sci USA 101 : 5018–5023. 15037750
42. Fu Y, Waldor MK, Mekalanos JJ (2013) Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host. Cell Host Microbe 14 : 652–663. doi: 10.1016/j.chom.2013.11.001 24331463
43. Kamp HD, Patimalla-Dipali B, Lazinski DW, Wallace-Gadsden F, Camilli A (2013) Gene fitness landscapes of Vibrio cholerae at important stages of its life cycle. PLoS Pathog 9: e1003800. doi: 10.1371/journal.ppat.1003800 24385900
44. Gunn JS (2000) Mechanisms of bacterial resistance and response to bile. Microbe Infect 2 : 907–913. 10962274
45. Gupta S, Chowdhury R (1997) Bile affects production of virulence factors and motility of Vibrio cholerae. Infect Immun 65 : 1131–1134. 9038330
46. Matson JS, Withey JH, DiRita VJ (2007) Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect Immun 75 : 5542–5549. 17875629
47. DiRita VJ, Parsot C, Jander G, Mekalanos JJ (1991) Regulatory cascade controls virulence in Vibrio cholerae. Proc Natl Acad Sci USA 88 : 5403–5407. 2052618
48. Higgins DE, Nazareno E, DiRita VJ (1992) The virulence gene activator ToxT from Vibrio cholerae is a member of the AraC family of transcriptional activators. J Bacteriol 174 : 6974–6980. 1400247
49. Champion GA, Neely MN, Brennan MA, DiRita VJ (1997) A branch in the ToxR regulatory cascade of Vibrio cholerae revealed by characterization of toxT mutant strains. Mol Microbiol 23 : 323–331. 9044266
50. Sanchez J, Holmgren J (2008) Cholera toxin structure, gene regulation and pathophysiological and immunological aspects. Cell Mol Life Sci 65 : 1347–1360. doi: 10.1007/s00018-008-7496-5 18278577
51. Chatterjee A, Dutta PK, 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. 17261615
52. Schuhmacher DA, Klose KE (1999) Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J Bacteriol 181 : 1508–1514. 10049382
53. Prouty MG, Osorio CR, Klose KE (2005) Characterization of functional domains of the Vibrio cholerae virulence regulator ToxT. Mol Microbiol 58 : 1143–1156. 16262796
54. Childers BM, Cao X, Weber GG, Demeler B, Hart PJ, et al. (2011) N-terminal residues of the Vibrio cholerae virulence regulatory protein ToxT involved in dimerization and modulation by fatty acids. J Biol Chem 286 : 28644–28655. doi: 10.1074/jbc.M111.258780 21673111
55. Lowden MJ, Skorupski K, Pellegrini M, Chiorazzo MG, Taylor RK, et al. (2010) Structure of Vibrio cholerae ToxT reveals a mechanism for fatty acid regulation of virulence genes. Proc Natl Acad Sci USA 107 : 2860–2865. doi: 10.1073/pnas.0915021107 20133655
56. Abuaita BH, Withey JH (2009) Bicarbonate induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect Immun 77 : 4111–4120. doi: 10.1128/IAI.00409-09 19564378
57. Thomson JJ, Withey JH (2014) Bicarbonate increases binding affinity of Vibrio cholerae ToxT to virulence gene promoters. J Bacteriol 196 : 3872–3880. doi: 10.1128/JB.01824-14 25182489
58. Thomson JJ, Plecha SC, Withey JH (2015) A small unstructured region in Vibrio cholerae ToxT mediates the response to positive and negative effectors and ToxT proteolysis. J Bacteriol 197 : 654–668. doi: 10.1128/JB.02068-14 25422303
59. Hogan DL, Ainsworth MA, Isenberg JI (1994) Gastroduodenal bicarbonate secretion. Aliment Pharmacol Ther 8 : 475–488. 7865639
60. Flemström G, Isenberg JI (2001) Gastroduodenal mucosal alkaline secretion and mucosal protection. News Physiol Sci 16 : 23–28. 11390942
61. McGuckin MA, Lindén SK, Sutton P, Florin TH (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9 : 265–278. doi: 10.1038/nrmicro2538 21407243
62. Booth BA, Boesman-Finkelstein M, Finkelstein RA (1983) Vibrio cholerae soluble hemagglutinin/protease is a metalloenzyme. Infect Immun 42 : 639–644. 6417020
63. Silva AJ, Pham K, Benitez JA (2003) Haemagglutinin/protease expression and mucin gel penetration in El Tor biotype Vibrio cholerae. Microbiology 149 : 1883–1891. 12855739
64. Zhu J, Mekalanos JJ (2003) Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5 : 647–656. 14536065
65. Szabady RL, Yanta JH, Halladin DK, Schofield MJ, Welch RA (2011) TagA is a secreted protease of Vibrio cholerae that specifically cleaves mucin glycoproteins. Microbiology 157 : 516–525. doi: 10.1099/mic.0.044529-0 20966091
66. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, et al. (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 99 : 3129–3134. 11854465
67. Galen JE, Ketley JM, Fasano A, Richardson SH, Wasserman SS, et al. (1992) Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect Immun 60 : 406–415. 1730470
68. Holmgren J, Lönnroth I, Månsson J, Svennerholm L (1975) Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proc Natl Acad Sci USA 72 : 2520–2524. 1058471
69. Krebs SJ, Taylor RK (2011) Protection and attachment of Vibrio cholerae mediated by the toxin-coregulated pilus in the infant mouse model. J Bacteriol 193 : 5260–5270. doi: 10.1128/JB.00378-11 21804008
70. Kirn TJ, Jude BA, Taylor RK (2005) A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438 : 863–866. 16341015
71. Syed KA, Beyhan S, Correa N, Queen J, Liu J, et al. (2009) The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. J Bacteriol 191 : 6555–6570. doi: 10.1128/JB.00949-09 19717600
72. Attridge SR, Rowley D (1983) The role of the flagellum in the adherence of Vibrio cholerae. J Infect Dis 147 : 864–872. 6842021
73. Krachler AM, Ham H, Orth K (2011) Outer membrane adhesion factor multivalent adhesion molecule 7 initiates host cell binding during infection by gram-negative pathogens. Proc Natl Acad Sci USA 108 : 11614–11619. doi: 10.1073/pnas.1102360108 21709226
74. Sperandio V, Girón JA, Silveira WD, Kaper JB (1995) The OmpU outer membrane protein, a potential adherence factor of Vibrio cholerae. Infect Immun 63 : 4433–4438. 7591082
75. Bhowmick R, Ghosal A, Das B, Koley H, Saha DR, et al. (2008) Intestinal adherence of Vibrio cholerae involves a coordinated interaction between colonization factor GbpA and mucin. Infect Immun 76 : 4968–4977. doi: 10.1128/IAI.01615-07 18765724
76. Wong E, Vaaje-Kolstad G, Ghosh A, Hurtado-Guerrero R, Konarev PV, et al. (2012) The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces. PLoS Pathog 8: e1002373. doi: 10.1371/journal.ppat.1002373 22253590
77. Tarsi R, Pruzzo C (1999) Role of surface proteins in Vibrio cholerae attachment to chitin. Appl Environ Microbiol 65 : 1348–1351. 10049907
78. Aeckersberg F, Lupp C, Feliciano B, Ruby EG (2001) Vibrio fischeri outer membrane protein OmpU plays a role in normal symbiotic colonization. J Bacteriol 183 : 6590–6597. 11673429
79. Adams EL, Almagro-Moreno S, Boyd EF (2011) An atomic force microscopy method for the detection of binding forces between bacteria and a lipid bilayer containing higher order gangliosides. J Microbiol Methods 84 : 352–354. doi: 10.1016/j.mimet.2010.12.014 21192989
80. Almagro-Moreno S, Boyd EF (2009) Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect Immun 77 : 3807–3816. doi: 10.1128/IAI.00279-09 19564383
81. Lee SH, Hava DL, Waldor MK, Camilli A (1999) Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99 : 625–634. 10612398
82. Ghosh S, Rao KH, Sengupta M, Bhattacharya SK, Datta A (2011) Two gene clusters co-ordinate for a functional N-acetylglucosamine catabolic pathway in Vibrio cholerae. Mol Microbiol 80 : 1549–1560. doi: 10.1111/j.1365-2958.2011.07664.x 21488982
83. Richard AL, Withey JH, Beyhan S, Yildiz F, DiRita VJ (2010) The Vibrio cholerae virulence regulatory cascade controls glucose uptake through activation of TarA, a small regulatory RNA. Mol Microbiol 78 : 1171–1181. doi: 10.1111/j.1365-2958.2010.07397.x 21091503
84. Watnick PI, Fullner KJ, Kolter R (1999) A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J Bacteriol 181 : 3606–3609. 10348878
85. Kirn TJ, Lafferty MJ, Sandoe CM, Taylor RK (2000) Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol Microbiol 35 : 896–910. 10692166
86. Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272 : 1910–1914. 8658163
87. Kirn TJ, Bose N, Taylor RK (2003) Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae. Mol Microbiol 49 : 81–92. 12823812
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