Phenotypic analysis reveals that the 2010 haiti cholera epidemic is linked to a hypervirulent strain

Infection and Immunity

Volumn 84, Issue 9, 2016, Pages 2473-2481

  Satchell, Karla J F ^a   Jones, Christopher J ^b,c   Wong, Jennifer ^a,d   Queen, Jessica ^a,e   Agarwal, Shivani ^a   Yildiz, Fitnat H ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d INDIANA UNIVERSITY   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLERA TOXIN; HEMOLYSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOFILM; CHOLERA; CONTROLLED STUDY; EPIDEMIC; FEMALE; GENE SEQUENCE; GNTR GENE; HAITI; HNS GENE; HUMAN; HUMAN CELL; INFANT; LYSR GENE; MOUSE; NONHUMAN; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REGULATOR GENE; VIBRIO CHOLERAE O1; VIEA GENE; ALLELE; ANIMAL; EVOLUTION; GENETIC VARIATION; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; MICROBIOLOGY; PATHOGENICITY; PHYLOGENY; VIRULENCE;

ALLELES; ANIMALS; BIOLOGICAL EVOLUTION; CHOLERA; CHOLERA TOXIN; EPIDEMICS; GENES, REGULATOR; GENETIC VARIATION; HAITI; HEMOLYSIN PROTEINS; MICE; MICE, INBRED ICR; PHENOTYPE; PHYLOGENY; VIBRIO CHOLERAE O1; VIRULENCE;

EID: 84984799730     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00189-16     Document Type: Article

References (48)

1. Sack DA, Sack RB, Nair GB, Siddique AK. 2004. Cholera. Lancet 363: 223-233. http://dx.doi.org/10.1016/S0140-6736(03)15328-7.
2. Safa A, Nair GB, Kong RY. 2010. Evolution of new variants of Vibrio cholerae O1. Trends Microbiol 18: 46-54. http://dx.doi.org/10.1016/j.tim.2009.10.003.
3. Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH, Kariuki S, Croucher NJ, Choi SY, Harris SR, Lebens M, Niyogi SK, Kim EJ, Ramamurthy T, Chun J, Wood JL, Clemens JD, Czerkinsky C, Nair GB, Holmgren J, Parkhill J, Dougan G. 2011. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477: 462-465. http://dx.doi.org/10.1038/nature10392.
4. Moore S, Thomson N, Mutreja A, Piarroux R. 2014. Widespread epidemic cholera caused by a restricted subset of Vibrio cholerae clones. Clin Microbiol Infect 20: 373-379. http://dx.doi.org/10.1111/1469-0691.12610.
5. Comstock LE, Maneval D, Jr, Panigrahi P, Joseph A, Levine MM, Kaper JB, Morris JG, Jr, Johnson JA. 1995. The capsule and O antigen in Vibrio cholerae O139 Bengal are associated with a genetic region not present in Vibrio cholerae O1. Infect Immun 63: 317-323.
6. Kim EJ, Lee D, Moon SH, Lee CH, Kim SJ, Lee JH, Kim JO, Song M, Das B, Clemens JD, Pape JW, Nair GB, Kim DW. 2014. Molecular insights into the evolutionary pathway of Vibrio cholerae O1 atypical El Tor variants. PLoS Pathog 10: e1004384. http://dx.doi.org/10.1371/journal.ppat.1004384.
7. Ghosh P, Naha A, Pazhani GP, Ramamurthy T, Mukhopadhyay AK. 2014. Genetic traits of Vibrio cholerae O1 Haitian isolates that are absent in contemporary strains from Kolkata, India. PLoS One 9: e112973. http://dx.doi.org/10.1371/journal.pone.0112973.
8. Kutar BM, Rajpara N, Upadhyay H, Ramamurthy T, Bhardwaj AK. 2013. Clinical isolates of Vibrio cholerae O1 El Tor Ogawa of 2009 from Kolkata, India: preponderance of SXT element and presence of Haitian ctxB variant. PLoS One 8: e56477. http://dx.doi.org/10.1371/journal.pone.0056477.
9. Dalia AB, Seed KD, Calderwood SB, Camilli A. 2015. A globally distributed mobile genetic element inhibits natural transformation of Vibrio cholerae. Proc Natl Acad Sci U S A 112: 10485-10490. http://dx.doi.org/10.1073/pnas.1509097112.
10. Katz LS, Petkau A, Beaulaurier J, Tyler S, Antonova ES, Turnsek MA, Guo Y, Wang S, Paxinos EE, Orata F, Gladney LM, Stroika S, Folster JP, Rowe L, Freeman MM, Knox N, Frace M, Boncy J, Graham M, Hammer BK, Boucher Y, Bashir A, Hanage WP, Van Domselaar G, Tarr CL. 2013. Evolutionary dynamics of Vibrio cholerae O1 following a singlesource introduction to Haiti. mBio 4: e00398-13. http://dx.doi.org/10.1128/mBio.00398-13.
11. Hasan NA, Choi SY, Eppinger M, Clark PW, Chen A, Alam M, Haley BJ, Taviani E, Hine E, Su Q, Tallon LJ, Prosper JB, Furth K, Hoq MM, Li H, Fraser-Liggett CM, Cravioto A, Huq A, Ravel J, Cebula TA, Colwell RR. 2012. Genomic diversity of 2010 Haitian cholera outbreak strains. Proc Natl Acad Sci U S A 109: E2010-E2017. http://dx.doi.org/10.1073/pnas.1207359109.
12. Azarian T, Ali A, Johnson JA, Mohr D, Prosperi M, Veras NM, Jubair M, Strickland SL, Rashid MH, Alam MT, Weppelmann TA, Katz LS, Tarr CL, Colwell RR, Morris JG, Jr, Salemi M. 2014. Phylodynamic analysis of clinical and environmental Vibrio cholerae isolates from Haiti reveals diversification driven by positive selection. mBio 5: e01824-14. http://dx.doi.org/10.1128/mBio.01824-14.
13. Reimer AR, Van Domselaar G, Stroika S, Walker M, Kent H, Tarr C, Talkington D, Rowe L, Olsen-Rasmussen M, Frace M, Sammons S, Dahourou GA, Boncy J, Smith AM, Mabon P, Petkau A, Graham M, Gilmour MW, Gerner-Smidt P. 2011. Comparative genomics of Vibrio cholerae from Haiti, Asia, and Africa. Emerg Infect Dis 17: 2113-2121. http://dx.doi.org/10.3201/eid1711.110794.
14. Hendriksen RS, Price LB, Schupp JM, Gillece JD, Kaas RS, Engelthaler DM, Bortolaia V, Pearson T, Waters AE, Upadhyay BP, Shrestha SD, Adhikari S, Shakya G, Keim PS, Aarestrup FM. 2011. Population genetics of Vibrio cholerae from Nepal in 2010: evidence on the origin of the Haitian outbreak. mBio 2: e00157-11. http://dx.doi.org/10.1128/mBio.00157-11.
15. Eppinger M, Pearson T, Koenig SS, Pearson O, Hicks N, Agrawal S, Sanjar F, Galens K, Daugherty S, Crabtree J, Hendriksen RS, Price LB, Upadhyay BP, Shakya G, Fraser CM, Ravel J, Keim PS. 2014. Genomic epidemiology of the Haitian cholera outbreak: a single introduction followed by rapid, extensive, and continued spread characterized the onset of the epidemic. mBio 5: e01721-14. http://dx.doi.org/10.1128/mBio.01721-14.
16. Chin CS, Sorenson J, Harris JB, Robins WP, Charles RC, Jean-Charles RR, Bullard J, Webster DR, Kasarskis A, Peluso P, Paxinos EE, Yamaichi Y, Calderwood SB, Mekalanos JJ, Schadt EE, Waldor MK. 2011. The origin of the Haitian cholera outbreak strain. N Engl J Med 364: 33-42. http://dx.doi.org/10.1056/NEJMoa1012928.
17. Son MS, Megli CJ, Kovacikova G, Qadri F, Taylor RK. 2011. Characterization of Vibrio cholerae O1 El Tor biotype variant clinical isolates from Bangladesh and Haiti, including a molecular genetic analysis of virulence genes. J Clin Microbiol 49: 3739-3749. http://dx.doi.org/10.1128/JCM.01286-11.
18. Dolores J, Satchell KJ. 2013. Analysis of Vibrio cholerae genome sequences reveals unique rtxA variants in environmental strains and an rtxA-null mutation in recent altered El Tor isolates. mBio 4: e00624-12. http://dx.doi.org/10.1128/mBio.00624-12.
19. Kumar P, Jain M, Goel AK, Bhadauria S, Sharma SK, Kamboj DV, Singh L, Ramamurthy T, Nair GB. 2009. A large cholera outbreak due to a new cholera toxin variant of the Vibrio cholerae O1 El Tor biotype in Orissa, Eastern India. J Med Microbiol 58: 234-238. http://dx.doi.org/10.1099/jmm.0.002089-0.
20. Rashid MU, Rashed SM, Islam T, Johura FT, Watanabe H, Ohnishi M, Alam M. 19 October 2015. CtxB1 outcompetes CtxB7 in Vibrio cholerae O1, Bangladesh. J Med Microbiol http://dx.doi.org/10.1099/jmm.0.000190.
21. Kumar P, Mishra DK, Deshmukh DG, Jain M, Zade AM, Ingole KV, Goel AK, Yadava PK. 2014. Vibrio cholerae O1 Ogawa El Tor strains with the ctxB7 allele driving cholera outbreaks in south-western India in 2012. Infect Genet Evol 25: 93-96. http://dx.doi.org/10.1016/j.meegid.2014.03.020.
22. Qadri F, Bhuiyan TR, Dutta KK, Raqib R, Alam MS, Alam NH, Svennerholm AM, Mathan MM. 2004. Acute dehydrating disease caused by Vibrio cholerae serogroups O1 and O139 induce increases in innate cells and inflammatory mediators at the mucosal surface of the gut. Gut 53: 62-69. http://dx.doi.org/10.1136/gut.53.1.62.
23. Qadri F, Raqib R, Ahmed F, Rahman T, Wenneras C, Das SK, Alam NH, Mathan MM, Svennerholm AM. 2002. Increased levels of inflammatory mediators in children and adults infected with Vibrio cholerae O1 and O139. Clin Diagn Lab Immunol 9: 221-229. http://dx.doi.org/10.1128/CDLI.9.2.221-229.2002.
24. Alam M, Islam A, Bhuiyan NA, Rahim N, Hossain A, Khan GY, Ahmed D, Watanabe H, Izumiya H, Faruque AS, Akanda AS, Islam S, Sack RB, Huq A, Colwell RR, Cravioto A. 2011. Clonal transmission, dual peak, and off-season cholera in Bangladesh. Infect Ecol Epidemiol 1: 7273.
25. Fullner KJ, Mekalanos JJ. 1999. Genetic characterization of a new type IV pilus gene cluster found in both classical and El Tor biotypes of Vibrio cholerae. Infect Immun 67: 1393-1404.
26. Queen J, Agarwal S, Dolores JS, Stehlik C, Satchell KJ. 2015. Mechanisms of inflammasome activation by Vibrio cholerae secreted toxins vary with strain biotype. Infect Immun 83: 2496-2506. http://dx.doi.org/10.1128/IAI.02461-14.
27. Gardel CL, Mekalanos JJ. 1994. Regulation of cholera toxin by temperature, pH, and osmolarity. Methods Enzymol 235: 517-526. http://dx.doi.org/10.1016/0076-6879(94)35167-8.
28. Iwanaga M, Yamamoto K, Higa N, Ichinose Y, Nakasone N, Tanabe M. 1986. Culture conditions for stimulating cholera toxin production by Vibrio cholerae O1 El Tor. Microbiol Immunol 30: 1075-1083. http://dx.doi.org/10.1111/j.1348-0421.1986.tb03037.x.
29. Jones CJ, Utada A, Davis KR, Thongsomboon W, Zamorano Sanchez D, Banakar V, Cegelski L, Wong GC, Yildiz FH. 2015. c-di-GMP regulates motile to sessile transition by modulating MshA pili biogenesis and near-surface motility behavior in Vibrio cholerae. PLoS Pathog 11: e1005068. http://dx.doi.org/10.1371/journal.ppat.1005068.
30. Liu X, Beyhan S, Lim B, Linington RG, Yildiz FH. 2010. Identification and characterization of a phosphodiesterase that inversely regulates motility and biofilm formation in Vibrio cholerae. J Bacteriol 192: 4541-4552. http://dx.doi.org/10.1128/JB.00209-10.
31. Ghosh-Banerjee J, Senoh M, Takahashi T, Hamabata T, Barman S, Koley H, Mukhopadhyay AK, Ramamurthy T, Chatterjee S, Asakura M, Yamasaki S, Nair GB, Takeda Y. 2010. Cholera toxin production by the El Tor variant of Vibrio cholerae O1 compared to prototype El Tor and classical biotypes. J Clin Microbiol 48: 4283-4286. http://dx.doi.org/10.1128/JCM.00799-10.
32. Olivier V, Queen J, Satchell KJ. 2009. Successful small intestine colonization of adult mice by Vibrio cholerae requires ketamine anesthesia and accessory toxins. PLoS One 4: e7352. http://dx.doi.org/10.1371/journal.pone.0007352.
33. Syed KA, Beyhan S, Correa N, Queen J, Liu J, Peng F, Satchell KJ, Yildiz F, Klose KE. 2009. The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. J Bacteriol 191: 6555-6570. http://dx.doi.org/10.1128/JB.00949-09.
34. Teschler JK, Zamorano-Sanchez D, Utada AS, Warner CJ, Wong GC, Linington RG, Yildiz FH. 2015. Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nat Rev Microbiol 13: 255-268. http://dx.doi.org/10.1038/nrmicro3433.
35. Waters CM, Lu W, Rabinowitz JD, Bassler BL. 2008. Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Bacteriol 190: 2527-2536. http://dx.doi.org/10.1128/JB.01756-07.
36. Tischler AD, Camilli A. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun 73: 5873-5882. http://dx.doi.org/10.1128/IAI.73.9.5873-5882.2005.
37. Lazinski DW, Camilli A. 2013. Homopolymer tail-mediated ligation PCR: a streamlined and highly efficient method for DNA cloning and library construction. Biotechniques 54: 25-34. http://dx.doi.org/10.2144/000113981.
38. 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. http://dx.doi.org/10.1016/j.chom.2013.11.001.
39. Wang H, Ayala JC, Benitez JA, Silva AJ. 2015. RNA-seq analysis identifies new genes regulated by the histone-like nucleoid structuring protein (H-NS) affecting Vibrio cholerae virulence, stress response and chemotaxis. PLoS One 10: e0118295. http://dx.doi.org/10.1371/journal.pone.0118295.
40. Kazi MI, Conrado AR, Mey AR, Payne SM, Davies BW. 2016. ToxR antagonizes H-NS regulation of horizontally acquired genes to drive host colonization. PLoS Pathog 12: e1005570. http://dx.doi.org/10.1371/journal.ppat.1005570.
41. Bogard RW, Davies BW, Mekalanos JJ. 2012. MetR-regulated Vibrio cholerae metabolism is required for virulence. mBio 3: e00236-12. http://dx.doi.org/10.1128/mBio.00236-12.
42. Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53: 857-869. http://dx.doi.org/10.1111/j.1365-2958.2004.04155.x.
43. Peterson KM, Mekalanos JJ. 1988. Characterization of the Vibrio cholerae ToxR regulon: identification of novel genes involved in intestinal colonization. Infect Immun 56: 2822-2829.
44. Gosink KK, Kobayashi R, Kawagishi I, Hase CC. 2002. Analyses of the roles of the three cheA homologs in chemotaxis of Vibrio cholerae. J Bacteriol 184: 1767-1771. http://dx.doi.org/10.1128/JB.184.6.1767-1771.2002.
45. Díaz-Quiñonez JA, Hernandez-Monroy I, Montes-Colima NA, Moreno-Perez MA, Galicia-Nicolas AG, Lopez-Martinez I, Ruiz-Matus C, Kuri-Morales P, Ortiz-Alcantara JM, Garces-Ayala F, Ramirez-Gonzalez JE. 2016. Biochemical and full genome sequence analyses of clinical Vibrio cholerae isolates in Mexico reveals the presence of novel V. cholerae strains. Microbes Infect 18: 322-328. http://dx.doi.org/10.1016/j.micinf.2016.01.004.
46. Bishop AL, Patimalla B, Camilli A. 2014. Vibrio cholerae-induced inflammation in the neonatal mouse cholera model. Infect Immun 82: 2434-2447. http://dx.doi.org/10.1128/IAI.00054-14.
47. Olivier V, Salzman NH, Satchell KJ. 2007. Prolonged colonization of mice by Vibrio cholerae El Tor O1 depends on accessory toxins. Infect Immun 75: 5043-5051. http://dx.doi.org/10.1128/IAI.00508-07.
48. Queen J, Satchell KJ. 2013. Promotion of colonization and virulence by cholera toxin is dependent on neutrophils. Infect Immun 81: 3338-3345. http://dx.doi.org/10.1128/IAI.00422-13.