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Post-Genomic Analysis of Members of the Family

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  • Authors: E. Fidelma Boyd1, Megan R. Carpenter2, Nityananda Chowdhury3, Analuisa L. Cohen4, Brandy L. Haines-Menges5, Sai S. Kalburge6, Joseph J. Kingston7, J.B. Lubin8, Serge Y. Ongagna-Yhombi9, W. Brian Whitaker10
  • Editor: Michael Sadowsky11
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 2: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 3: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 4: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 5: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 6: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 7: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 8: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 9: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 10: Department of Biological Sciences, University of Delaware, Newark, DE 19716; 11: University of Minnesota, St. Paul, MN
  • Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
  • Received 26 November 2014 Accepted 07 July 2015 Published 11 September 2015
  • E. Fidelma Boyd, fboyd@udel.edu
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  • Abstract:

    Similar to other genera and species of bacteria, whole genomic sequencing has revolutionized how we think about and address questions of basic biology. In this review we examined 36 completely sequenced and annotated members of the family, encompassing 12 different species of the genera , and . We reconstructed the phylogenetic relationships among representatives of this group of bacteria by using three housekeeping genes and 16S rRNA sequences. With an evolutionary framework in place, we describe the occurrence and distribution of primary and alternative sigma factors, global regulators present in all bacteria. Among we show that the number and function of many of these sigma factors differs from species to species. We also describe the role of the -specific regulator ToxRS in fitness and survival. Examination of the biochemical capabilities was and still is the foundation of classifying and identifying new species. Using comparative genomics, we examine the distribution of carbon utilization patterns among species as a possible marker for understanding bacteria-host interactions. Finally, we discuss the significant role that horizontal gene transfer, specifically, the distribution and structure of integrons, has played in evolution.

  • Citation: Boyd E, Carpenter M, Chowdhury N, Cohen A, Haines-Menges B, Kalburge S, Kingston J, Lubin J, Ongagna-Yhombi S, Whitaker W. 2015. Post-Genomic Analysis of Members of the Family . Microbiol Spectrum 3(5):VE-0009-2014. doi:10.1128/microbiolspec.VE-0009-2014.

Key Concept Ranking

RNA Polymerase beta Subunit
0.47545764
Mobile Genetic Elements
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0.47545764

References

1. Urbanczyk H, Ast JC, Higgins MJ, Carson J, Dunlap PV. 2007. Reclassification of Vibrio fischeri, Vibrio logei, Vibrio salmonicida and Vibrio wodanis as Aliivibrio fischeri gen. nov., comb. nov., Aliivibrio logei comb. nov., Aliivibrio salmonicida comb. nov. and Aliivibrio wodanis comb. nov. Int J Syst Evol Microbiol 57:2823–2829. [PubMed][CrossRef]
2. Thompson CC, Vicente AC, Souza RC, Vasconcelos AT, Vesth T, Alves N, Jr, Ussery DW, Iida T, Thompson FL. 2009. Genomic taxonomy of Vibrios. BMC Evol Biol 9:258. [PubMed][CrossRef]
3. Thompson FL, Gevers D, Thompson CC, Dawyndt P, Naser S, Hoste B, Munn CB, Swings J. 2005. Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis. Appl Environ Microbiol 71:5107–5115. [PubMed][CrossRef]
4. Thompson FL, Thompson CC, Dias GM, Naka H, Dubay C, Crosa JH. 2011. The genus Listonella MacDonell and Colwell 1986 is a later heterotypic synonym of the genus Vibrio Pacini 1854 (Approved Lists 1980)--a taxonomic opinion. Int J Syst Evol Microbiol 61:3023–3027. [PubMed][CrossRef]
5. Trucksis M, Michalski J, Deng YK, Kaper JB. 1998. The Vibrio cholerae genome contains two unique circular chromosomes. Proc Natl Acad Sci U S A 95:14464–14469. [PubMed][CrossRef]
6. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. [PubMed][CrossRef]
7. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. [PubMed]
8. Jukes TH, Cantor CR. 1969. Evolution of protein molecules, p 21–132. In Munro HN (ed), Mammalian Protein Metabolism. Academic Press, New York, NY. [CrossRef]
9. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. [CrossRef]
10. Lin B, Wang Z, Malanoski AP, O’Grady EA, Wimpee CF, Vuddhakul V, Alves N, Jr, Thompson FL, Gomez-Gil B, Vora GJ. 2010. Comparative genomic analyses identify the Vibrio harveyi genome sequenced strains BAA-1116 and HY01 as Vibrio campbellii. Environ Microbiol Rep 2:81–89. [PubMed][CrossRef]
11. Thompson FL, Iida T, Swings J. 2004. Biodiversity of vibrios. Microbiol Mol Biol Rev 68:403–431. [PubMed][CrossRef]
12. Osterberg S, del Peso-Santos T, Shingler V. 2011. Regulation of alternative sigma factor use. Annu Rev Microbiol 65:37–55. [PubMed][CrossRef]
13. Zhao JJ, Chen C, Zhang LP, Hu CQ. 2009. Cloning, identification, and characterization of the rpoS-like sigma factor rpoX from Vibrio alginolyticus. J Biomed Biotechnol 2009:126986. doi:10.1155/2009/126986. [PubMed][CrossRef]
14. Cao X, Studer SV, Wassarman K, Zhang Y, Ruby EG, Miyashiro T. 2012. The novel sigma factor-like regulator RpoQ controls luminescence, chitinase activity, and motility in Vibrio fischeri. MBio 3. doi:10.1128/mBio.00285-11 [PubMed][CrossRef]
15. McCarter LL. 1995. Genetic and molecular characterization of the polar flagellum of Vibrio parahaemolyticus. J Bacteriol 177:1595–1609. [PubMed]
16. McCarter LL, Wright ME. 1993. Identification of genes encoding components of the swarmer cell flagellar motor and propeller and a sigma factor controlling differentiation of Vibrio parahaemolyticus. J Bacteriol 175:3361–3371. [PubMed]
17. Stewart BJ, McCarter LL. 2003. Lateral flagellar gene system of Vibrio parahaemolyticus. J Bacteriol 185:4508–4518. [CrossRef]
18. Whitaker WB, Richards GP, Boyd EF. 2014. Loss of sigma factor RpoN increases intestinal colonization of Vibrio parahaemolyticus in an adult mouse model. Infect Immun 82:544–556. [PubMed][CrossRef]
19. Ho TD, Ellermeier CD. 2012. Extra cytoplasmic function sigma factor activation. Curr Opin Microbiol 15:182–188. [PubMed][CrossRef]
20. Rappas M, Bose D, Zhang X. 2007. Bacterial enhancer-binding proteins: unlocking sigma54-dependent gene transcription. Curr Opin Struct Biol 17:110–116. [PubMed][CrossRef]
21. Yildiz FH, Schoolnik GK. 1998. Role of rpoS in stress survival and virulence of Vibrio cholerae. J Bacteriol 180:773–784. [PubMed]
22. Merrell D, Tischler A, Lee S, Camilli A. 2000. Vibrio cholerae requires rpoS for efficient intestinal colonization. Infect Immun 68:6691–6696. [PubMed][CrossRef]
23. Nielsen AT, Dolganov NA, Otto G, Miller MC, Wu CY, Schoolnik GK. 2006. RpoS controls the Vibrio cholerae mucosal escape response. PLoS Pathog 2:e109. doi:10.1371/journal.ppat.0020109. [PubMed][CrossRef]
24. Rosche TM, Smith DJ, Parker EE, Oliver JD. 2005. RpoS involvement and requirement for exogenous nutrient for osmotically induced cross protection in Vibrio vulnificus. FEMS Microbiol Ecol 53:455–462. [PubMed][CrossRef]
25. Hulsmann A, Rosche TM, Kong IS, Hassan HM, Beam DM, Oliver JD. 2003. RpoS-dependent stress response and exoenzyme production in Vibrio vulnificus. Appl Environ Microbiol 69:6114–6120. [PubMed][CrossRef]
26. Weber B, Croxatto A, Chen C, Milton DL. 2008. RpoS induces expression of the Vibrio anguillarum quorum-sensing regulator VanT. Microbiology 154:767–780. [PubMed][CrossRef]
27. Whitaker WB, Parent MA, Naughton LM, Richards GP, Blumerman SL, Boyd EF. 2010. Modulation of responses of Vibrio parahaemolyticus O3:K6 to pH and temperature stresses by growth at different salt concentrations. Appl Environ Microbiol 76:4720–4729. [PubMed][CrossRef]
28. Smith B, Oliver J. 2006. In situ and in vitro gene expression by Vibrio vulnificus during entry into, persistence within, and resuscitation from the viable but nonculturable state. Appl Environ Microbiol 72:1445–1451. [PubMed][CrossRef]
29. Coutard F, Lozach S, Pommepuy M, Hervio-Heath D. 2007. Real-time reverse transcription-PCR for transcriptional expression analysis of virulence and housekeeping genes in viable but nonculturable Vibrio parahaemolyticus after recovery of culturability. Appl Environ Microbiol 73:5183–5189. [PubMed][CrossRef]
30. Richards GP, Fay JP, Dickens KA, Parent MA, Soroka DS, Boyd EF. 2012. Predatory bacteria as natural modulators of Vibrio parahaemolyticus and Vibrio vulnificus in seawater and oysters. Appl Environ Microbiol 78:7455–7466. [PubMed][CrossRef]
31. Whitaker WB, Parent MA, Boyd A, Richards GP, Boyd EF. 2012. The Vibrio parahaemolyticus ToxRS regulator is required for stress tolerance and colonization in a novel orogastric streptomycin-induced adult murine model. Infect Immun 80:1834–1845. [PubMed][CrossRef]
32. Haines-Menges B, Whitaker WB, Boyd EF. 2014. Alternative sigma factor RpoE is important for Vibrio parahaemolyticus cell envelope stress response and intestinal colonization. Infect Immun 82:3667–3677. [PubMed][CrossRef]
33. Tian Y, Wang Q, Liu Q, Ma Y, Cao X, Zhang Y. 2008. Role of RpoS in stress survival, synthesis of extracellular autoinducer 2, and virulence in Vibrio alginolyticus. Arch Microbiol 190:585–594. [PubMed][CrossRef]
34. Dong T, Schellhorn HE. 2009. Role of RpoS in virulence of pathogens. Infect Immun 78:887–897. [PubMed][CrossRef]
35. Sahu GK, Chowdhury R, Das J. 1997. The rpoH gene encoding sigma 32 homolog of Vibrio cholerae. Gene 189:203–207. [PubMed][CrossRef]
36. Slamti L, Livny J, Waldor MK. 2007. Global gene expression and phenotypic analysis of a Vibrio cholerae rpoH deletion mutant. J Bacteriol 189:351–362. [PubMed][CrossRef]
37. Kawagishi I, Nakada M, Nishioka N, Homma M. 1997. Cloning of a Vibrio alginolyticus rpoN gene that is required for polar flagellar formation. J Bacteriol 179:6851–6854. [PubMed]
38. O’Toole R, Milton DL, Horstedt P, Wolf-Watz H. 1997. RpoN of the fish pathogen Vibrio (Listonella) anguillarum is essential for flagellum production and virulence by the water-borne but not intraperitoneal route of inoculation. Microbiology 143(pt 12):3849–3859. [PubMed][CrossRef]
39. Lilley BN, Bassler BL. 2000. Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol Microbiol 36:940–954. [PubMed][CrossRef]
40. Wolfe AJ, Millikan DS, Campbell JM, Visick KL. 2004. Vibrio fischeri sigma54 controls motility, biofilm formation, luminescence, and colonization. Appl Environ Microbiol 70:2520–2524. [PubMed][CrossRef]
41. Ishikawa T, Rompikuntal PK, Lindmark B, Milton DL, Wai SN. 2009. Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. PLoS One 4:e6734. doi:10.1371/journal.pone.0006734. [PubMed][CrossRef]
42. Dong TG, Mekalanos JJ. 2012. Characterization of the RpoN regulon reveals differential regulation of T6SS and new flagellar operons in Vibrio cholerae O37 strain V52. Nucleic Acids Res 40:7766–7775. [PubMed][CrossRef]
43. Hao B, Mo ZL, Xiao P, Pan HJ, Lan X, Li GY. 2013. Role of alternative sigma factor 54 (RpoN) from Vibrio anguillarum M3 in protease secretion, exopolysaccharide production, biofilm formation, and virulence. Appl Microbiol Biotechnol 97:2575–2585. [PubMed][CrossRef]
44. Klose KE, Mekalanos JJ. 1998. Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol Microbiol 28:501–520. [PubMed][CrossRef]
45. Klose KE, Mekalanos JJ. 1998. Differential regulation of multiple flagellins in Vibrio cholerae. J Bacteriol 180:303–316. [PubMed]
46. Klose KE, Novik V, Mekalanos JJ. 1998. Identification of multiple sigma54-dependent transcriptional activators in Vibrio cholerae. J Bacteriol 180:5256–5259. [PubMed]
47. Prouty MG, Correa NE, Klose KE. 2001. The novel sigma54- and sigma28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol Microbiol 39:1595–1609. [PubMed][CrossRef]
48. 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. [PubMed][CrossRef]
49. Millikan DS, Ruby EG. 2003. FlrA, a sigma54-dependent transcriptional activator in Vibrio fischeri, is required for motility and symbiotic light-organ colonization. J Bacteriol 185:3547–3557. [CrossRef]
50. Kitaoka M, Miyata ST, Brooks TM, Unterweger D, Pukatzki S. 2011. VasH is a transcriptional regulator of the type VI secretion system functional in endemic and pandemic Vibrio cholerae. J Bacteriol 193:6471–6482. [PubMed][CrossRef]
51. Bernard CS, Brunet YR, Gavioli M, Lloubes R, Cascales E. 2011. Regulation of type VI secretion gene clusters by sigma54 and cognate enhancer binding proteins. J Bacteriol 193:2158–2167. [PubMed][CrossRef]
52. Gode-Potratz CJ, McCarter LL. 2011. Quorum sensing and silencing in Vibrio parahaemolyticus. J Bacteriol 193:4224–4237. [PubMed][CrossRef]
53. Fabich AJ, Leatham MP, Grissom JE, Wiley G, Lai H, Najar F, Roe BA, Cohen PS, Conway T. 2011. Genotype and phenotypes of an intestine-adapted Escherichia coli K-12 mutant selected by animal passage for superior colonization. Infect Immun 79:2430–2439. [PubMed][CrossRef]
54. Hild E, Takayama K, Olsson RM, Kjelleberg S. 2000. Evidence for a role of rpoE in stressed and unstressed cells of marine Vibrio angustum strain S14. J Bacteriol 182:6964–6974. [PubMed][CrossRef]
55. Kovacikova G, Skorupski K. 2002. The alternative sigma factor sigma(E) plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect Immun 70:5355–5362. [PubMed][CrossRef]
56. Mathur J, Davis BM, Waldor MK. 2007. Antimicrobial peptides activate the Vibrio cholerae sigmaE regulon through an OmpU-dependent signalling pathway. Mol Microbiol 63:848–858. [PubMed][CrossRef]
57. Brown RN, Gulig PA. 2009. Roles of RseB, sigmaE, and DegP in virulence and phase variation of colony morphotype of Vibrio vulnificus. Infect Immun 77:3768–3781. [PubMed][CrossRef]
58. Davis BM, Waldor MK. 2009. High-throughput sequencing reveals suppressors of Vibrio cholerae rpoE mutations: one fewer porin is enough. Nucleic Acids Res 37:5757–5767. [PubMed][CrossRef]
59. Rattanama P, Thompson JR, Kongkerd N, Srinitiwarawong K, Vuddhakul V, Mekalanos JJ. 2012. Sigma E regulators control hemolytic activity and virulence in a shrimp pathogenic Vibrio harveyi. PLoS One 7:e32523. doi:10.1371/journal.pone.0032523. [PubMed][CrossRef]
60. Miller VL, Taylor RK, Mekalanos JJ. 1987. Cholera toxin transcriptional activator toxR is a transmembrane DNA binding protein. Cell 48:271–279. [PubMed][CrossRef]
61. Miller VL, Mekalanos JJ. 1984. Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. Proc Natl Acad Sci U S A 81:3471–3475. [PubMed][CrossRef]
62. 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 U S A 84:2833–2837. [PubMed][CrossRef]
63. 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. [PubMed][CrossRef]
64. Pfau JD, Taylor RK. 1996. Genetic footprint on the ToxR-binding site in the promoter for cholera toxin. Mol Microbiol 20:213–222. [PubMed][CrossRef]
65. Skorupski K, Taylor RK. 1997. Control of the ToxR virulence regulon in Vibrio cholerae by environmental stimuli. Mol Microbiol 25:1003–1009. [PubMed][CrossRef]
66. DiRita VJ, Engleberg NC, Heath A, Miller A, Crawford JA, Yu R. 2000. Virulence gene regulation inside and outside. Philos Trans R Soc Lond B Biol Sci 355:657–665. [PubMed][CrossRef]
67. Das S, Chakrabortty A, Banerjee R, Roychoudhury S, Chaudhuri K. 2000. Comparison of global transcription responses allows identification of Vibrio cholerae genes differentially expressed following infection. FEMS Microbiol Lett 190:87–91. [PubMed][CrossRef]
68. Osorio CR, Klose KE. 2000. A region of the transmembrane regulatory protein ToxR that tethers the transcriptional activation domain to the cytoplasmic membrane displays wide divergence among Vibrio species. J Bacteriol 182:526–528. [PubMed][CrossRef]
69. Provenzano D, Klose KE. 2000. Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proc Natl Acad Sci U S A 97:10220–10224. [PubMed][CrossRef]
70. 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. [PubMed][CrossRef]
71. Provenzano D, Lauriano CM, Klose KE. 2001. Characterization of the role of the ToxR-modulated outer membrane porins OmpU and OmpT in Vibrio cholerae virulence. J Bacteriol 183:3652–3662. [PubMed][CrossRef]
72. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A 99:3129–3134. [PubMed][CrossRef]
73. Childers BM, Klose KE. 2007. Regulation of virulence in Vibrio cholerae: the ToxR regulon. Future Microbiol 2:335–344. [PubMed][CrossRef]
74. Krukonis ES, Yu RR, Dirita VJ. 2000. The Vibrio cholerae ToxR/TcpP/ToxT virulence cascade: distinct roles for two membrane-localized transcriptional activators on a single promoter. Mol Microbiol 38:67–84. [PubMed][CrossRef]
75. Morgan S, Felek S, Gadwal S, Koropatkin NM, Perry JW, Bryson AB, Krukonis E. 2011. The two faces of ToxR: activator of ompU, co-regulator of toxT in Vibrio cholerae. Mol Microbiol 81:113–128. [PubMed][CrossRef]
76. Goss T, Morgan SJ, French EL, Krukonis E. 2013. ToxR recognizes a direct repeat element in the toxT, ompU, ompT, and ctxA promoters of Vibrio cholerae to regulate transcription. Infect Immun 81:884–895. [PubMed][CrossRef]
77. 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. [PubMed][CrossRef]
78. Duperthuy M, Binesse J, Le Roux F, Romestand B, Caro A, Got P, Givaudan A, Mazel D, Bachere E, Destoumieux-Garzon D. 2010. The major outer membrane protein OmpU of Vibrio splendidus contributes to host antimicrobial peptide resistance and is required for virulence in the oyster Crassostrea gigas. Environ Microbiol 12:951–963. [PubMed][CrossRef]
79. Duperthuy M, Schmitt P, Garzon E, Caro A, Rosa RD, Le Roux F, Lautredou-Audouy N, Got P, Romestand B, de Lorgeril J, Kieffer-Jaquinod S, Bachere E, Destoumieux-Garzon D. 2011. Use of OmpU porins for attachment and invasion of Crassostrea gigas immune cells by the oyster pathogen Vibrio splendidus. Proc Natl Acad Sci U S A 108:2993–2998. [PubMed][CrossRef]
80. Gode-Potratz CJ, Chodur DM, McCarter LL. 2010. Calcium and iron regulate swarming and type III secretion in Vibrio parahaemolyticus. J Bacteriol 192:6025–6038. [PubMed][CrossRef]
81. Bassler B, Gibbons P, Roseman S. 1989. Chemotaxis to chitin oligosaccharides by Vibrio furnissii, a chitinivorous marine bacterium. Biochem Biophys Res Commun 161:1172–1176. [PubMed][CrossRef]
82. Bassler BL, Gibbons PJ, Yu C, Roseman S. 1991. Chitin utilization by marine bacteria. Chemotaxis to chitin oligosaccharides by Vibrio furnissii. J Biol Chem 266:24268–24275. [PubMed]
83. Bassler BL, Yu C, Lee YC, Roseman S. 1991. Chitin utilization by marine bacteria. Degradation and catabolism of chitin oligosaccharides by Vibrio furnissii. J Biol Chem 266:24276–24286. [PubMed]
84. Blokesch M. 2012. Chitin colonization, chitin degradation and chitin-induced natural competence of Vibrio cholerae are subject to catabolite repression. Environ Microbiol 14:1898–1912. [PubMed][CrossRef]
85. Hjerde E, Lorentzen MS, Holden MT, Seeger K, Paulsen S, Bason N, Churcher C, Harris D, Norbertczak H, Quail MA, Sanders S, Thurston S, Parkhill J, Willassen NP, Thomson NR. 2008. The genome sequence of the fish pathogen Aliivibrio salmonicida strain LFI1238 shows extensive evidence of gene decay. BMC Genomics 9:616. doi:10.1186/1471-2164-9-616. [CrossRef]
86. Keyhani NO, Wang LX, Lee YC, Roseman S. 1996. The chitin catabolic cascade in the marine bacterium Vibrio furnissii. Characterization of an N,N’-diacetyl-chitobiose transport system. J Biol Chem 271:33409–33413. [PubMed][CrossRef]
87. Meibom KL, Li XB, Nielsen AT, Wu CY, Roseman S, Schoolnik GK. 2004. The Vibrio cholerae chitin utilization program. Proc Natl Acad Sci U S A 101:2524–2529. [PubMed][CrossRef]
88. Park JK, Keyhani NO, Roseman S. 2000. Chitin catabolism in the marine bacterium Vibrio furnissii. Identification, molecular cloning, and characterization of A N,N’-diacetylchitobiose phosphorylase. J Biol Chem 275:33077–33083. [PubMed][CrossRef]
89. Pruzzo C, Vezzulli L, Colwell RR. 2008. Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol 10:1400–1410. [PubMed][CrossRef]
90. Svitil AL, Chadhain S, Moore JA, Kirchman DL. 1997. Chitin degradation proteins produced by the marine bacterium Vibrio harveyi growing on different forms of chitin. Appl Environ Microbiol 63:408–413. [PubMed]
91. Keyhani NO, Li XB, Roseman S. 2000. Chitin catabolism in the marine bacterium Vibrio furnissii. Identification and molecular cloning of a chitoporin. J Biol Chem 275:33068–33076. [PubMed][CrossRef]
92. Keyhani NO, Roseman S. 1996. The chitin catabolic cascade in the marine bacterium Vibrio furnissii. Molecular cloning, isolation, and characterization of a periplasmic beta-N-acetylglucosaminidase. J Biol Chem 271:33425–33432. [PubMed][CrossRef]
93. Keyhani NO, Roseman S. 1996. The chitin catabolic cascade in the marine bacterium Vibrio furnissii. Molecular cloning, isolation, and characterization of a periplasmic chitodextrinase. J Biol Chem 271:33414–33424. [PubMed][CrossRef]
94. Keyhani NO, Roseman S. 1997. Wild-type Escherichia coli grows on the chitin disaccharide, N,N’-diacetylchitobiose, by expressing the cel operon. Proc Natl Acad Sci U S A 94:14367–14371. [PubMed][CrossRef]
95. Keyhani NO, Wang LX, Lee YC, Roseman S. 2000. The chitin disaccharide, N,N’-diacetylchitobiose, is catabolized by Escherichia coli and is transported/phosphorylated by the phosphoenolpyruvate:glycose phosphotransferase system. J Biol Chem 275:33084–33090. [PubMed][CrossRef]
96. Benedek O, Schubert S. 2007. Mobility of the Yersinia high-pathogenicity island (HPI): transfer mechanisms of pathogenicity islands (PAIS) revisited (a review). Acta Microbiol Immunol Hung 54:89–105. [PubMed][CrossRef]
97. Boyd EF, Cohen AL, Naughton LM, Ussery DW, Binnewies TT, Stine OC, Parent MA. 2008. Molecular analysis of the emergence of pandemic Vibrio parahaemolyticus. BMC Microbiol 8:110. doi:10.1186/1471-2180-8-110. [PubMed][CrossRef]
98. Kalburge SS, Polson SW, Boyd Crotty K, Katz L, Turnsek M, Tarr CL, Martinez-Urtaza J, Boyd EF. 2014. Complete genome sequence of Vibrio parahaemolyticus environmental strain UCM-V493. Genome Announc 2. doi:10.1128/genomeA.00159-14. [PubMed][CrossRef]
99. Quirke AM, Reen FJ, Claesson MJ, Boyd EF. 2006. Genomic island identification in Vibrio vulnificus reveals significant genome plasticity in this human pathogen. Bioinformatics 22:905–910. [PubMed][CrossRef]
100. Varki A. 1992. Diversity in the sialic acids. Glycobiology 2:25–40. [PubMed][CrossRef]
101. Varki A. 2001. Loss of N-glycolylneuraminic acid in humans. Mechanisms, consequences, and implications for hominid evolution. Am J Phys Anthrop 33:54–69. [PubMed][CrossRef]
102. Varki A. 2008. Sialic acids in human health and disease. Trends Mol Med 14:351–360. [PubMed][CrossRef]
103. Almagro-Moreno S, Boyd EF. 2009. Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol Biol 9:118. doi:10.1186/1471-2148-9-118. [PubMed][CrossRef]
104. Almagro-Moreno S, Boyd EF. 2010. Bacterial catabolism of nonulosonic (sialic) acid and fitness in the gut. Gut Microbes 1:45–50. [PubMed][CrossRef]
105. Jermyn WS, Boyd EF. 2002. Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology 148:3681–3693. [PubMed][CrossRef]
106. Jermyn WS, Boyd EF. 2005. Molecular evolution of Vibrio pathogenicity island-2 (VPI-2): mosaic structure among Vibrio cholerae and Vibrio mimicus natural isolates. Microbiology 151:311–322. [PubMed][CrossRef]
107. Dziejman M, Serruto D, Tam VC, Sturtevant D, Diraphat P, Faruque SM, Rahman MH, Heidelberg JF, Decker J, Li L, Montgomery KT, Grills G, Kucherlapati R, Mekalanos JJ. 2005. Genomic characterization of non-O1, non-O139 Vibrio cholerae reveals genes for a type III secretion system. Proc Natl Acad Sci U S A 102:3465–3470. [PubMed][CrossRef]
108. Chen Y, Johnson JA, Pusch GD, Morris JG, Jr, Stine OC. 2007. The genome of non-O1 Vibrio cholerae NRT36S demonstrates the presence of pathogenic mechanisms that are distinct from O1 Vibrio cholerae. Infect Immun 75:2645–2647. [PubMed][CrossRef]
109. Murphy RA, Boyd EF. 2008. Three pathogenicity islands of Vibrio cholerae can excise from the chromosome and form circular intermediates. J Bacteriol 190:636–647. [PubMed][CrossRef]
110. Okada N, Iida T, Park KS, Goto N, Yasunaga T, Hiyoshi H, Matsuda S, Kodama T, Honda T. 2009. Identification and characterization of a novel type III secretion system in trh-positive Vibrio parahaemolyticus strain TH3996 reveal genetic lineage and diversity of pathogenic machinery beyond the species level. Infect Immun 77:904–913. [PubMed][CrossRef]
111. Lubin JB, Kingston JJ, Chowdhury N, Boyd EF. 2012. Sialic acid catabolism and transport gene clusters are lineage specific in Vibrio vulnificus. Appl Environ Microbiol 78:3407–3415. [PubMed][CrossRef]
112. 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. [PubMed][CrossRef]
113. Chowdhury N, Norris J, McAlister E, Lau SY, Thomas GH, Boyd EF. 2012. The VC1777-VC1779 proteins are members of a sialic acid-specific subfamily of TRAP transporters (SiaPQM) and constitute the sole route of sialic acid uptake in the human pathogen Vibrio cholerae. Microbiology 158:2158–2167. [PubMed][CrossRef]
114. Thomas GH, Boyd EF. 2011. On sialic acid transport and utilization by Vibrio cholerae. Microbiology 157:3253–3255. [PubMed][CrossRef]
115. Jeong H, Oh MH, Kim BS, Lee MY, Han HJ, Choi S. 2009. The capability of catabolic utilization of N-acetylneuraminic acid, a sialic acid, is essential for Vibrio vulnificus pathogenesis. Infect Immun 77:3209–3217. [PubMed][CrossRef]
116. Mulligan C, Leech AP, Kelly DJ, Thomas GH. 2011. The membrane proteins SiaQ and SiaM form an essential stoichiometric complex in the sialic acid tripartite ATP-independent periplasmic (TRAP) transporter SiaPQM (VC1777-1779) from Vibrio cholerae. J Biol Chem 287:3598–3608. [PubMed][CrossRef]
117. Sharma SK, Moe TS, Srivastava R, Chandra D, Srivastava BS. 2011. Functional characterization of VC1929 of Vibrio cholerae El Tor: role in mannose-sensitive haemagglutination, virulence and utilization of sialic acid. Microbiology 157:3180–3186. [PubMed][CrossRef]
118. Faruque SM, Mekalanos JJ. 2003. Pathogenicity islands and phages in Vibrio cholerae evolution. Trends Microbiol 11:505–510. [PubMed][CrossRef]
119. Karaolis DK, Johnson JA, Bailey CC, Boedeker EC, Kaper JB, Reeves PR. 1998. A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci U S A 95:3134–3139. [PubMed][CrossRef]
120. Waldor MK, Mekalanos JJ. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914. [PubMed][CrossRef]
121. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Umayam L, Gill SR, Nelson KE, Read TD, Tettelin H, Richardson D, Ermolaeva MD, Vamathevan J, Bass S, Qin H, Dragoi I, Sellers P, McDonald L, Utterback T, Fleishmann RD, Nierman WC, White O, Salzberg SL, Smith HO, Colwell RR, Mekalanos JJ, Venter JC, Fraser CM. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406:477–483. [PubMed][CrossRef]
122. Davies B, Bogard R, Young T, Mekalanos J. 2012. Coordinated regulation of accessory genetic elements produces cyclic di-nucleotides for V. cholerae virulence. Cell 149:358–370. [PubMed][CrossRef]
123. Feng L, Reeves PR, Lan R, Ren Y, Gao C, Zhou Z, Cheng J, Wang W, Wang J, Qian W, Li D, Wang L. 2008. A recalibrated molecular clock and independent origins for the cholera pandemic clones. PLoS One 3:e4053. doi:10.1371/journal.pone.0004053 [PubMed][CrossRef]
124. Grim CJ, Hasan NA, Taviani E, Haley B, Chun J, Brettin TS, Bruce DC, Detter JC, Han CS, Chertkov O, Challacombe J, Huq A, Nair GB, Colwell RR. 2010. Genome sequence of hybrid Vibrio cholerae O1 MJ-1236, B-33, and CIRS101 and comparative genomics with V. cholerae. J Bacteriol 192:3524–3533. [PubMed][CrossRef]
125. Garza DR, Thompson CC, Loureiro EC, Dutilh BE, Inada DT, Junior EC, Cardoso JF, Nunes MR, de Lima CP, Silvestre RV, Nunes KN, Santos EC, Edwards RA, Vicente AC, de Sa Morais LL. 2012. Genome-wide study of the defective sucrose fermenter strain of Vibrio cholerae from the Latin American cholera epidemic. PLoS One 7:e37283. doi:10.1371/journal.pone.0037283. [CrossRef]
126. 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. [PubMed][CrossRef]
127. Nair G, Ramamurthy T, Bhattacharya S, Dutta B, Takeda Y, Sack D. 2007. Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and its serovariants. Clin Microbiol Rev 20:39–48. [PubMed][CrossRef]
128. Oliver JD. 2005. Wound infections caused by Vibrio vulnificus and other marine bacteria. Epidemiol Infect 133:383–391. [PubMed][CrossRef]
129. Oliver JD, Warner RA, Cleland DR. 1982. Distribution and ecology of Vibrio vulnificus and other lactose-fermenting marine vibrios in coastal waters of the southeastern United States. Appl Environ Microbiol 44:1404–1414. [PubMed]
130. Jones M, Oliver JD. 2009. Vibrio vulnificus: disease and pathogenesis. Infect Immun 77:1723–1733. [PubMed][CrossRef]
131. Chen CY, Wu KM, Chang YC, Chang CH, Tsai HC, Liao TL, Liu YM, Chen HJ, Shen AB, Li JC, Su TL, Shao CP, Lee CT, Hor LI, Tsai SF. 2003. Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res 13:2577–2587. [PubMed][CrossRef]
132. Cohen AL, Oliver JD, DePaola A, Feil EJ, Boyd EF. 2007. Emergence of a virulent clade of Vibrio vulnificus and correlation with the presence of a 33-kilobase genomic island. Appl Environ Microbiol 73:5553–5565. [PubMed][CrossRef]
133. Hurley CC, Quirke A, Reen FJ, Boyd EF. 2006. Four genomic islands that mark post-1995 pandemic Vibrio parahaemolyticus isolates. BMC Genomics 7:104. doi:10.1186/1471-2164-7-104 [PubMed][CrossRef]
134. Valla S, Frydenlund K, Coucheron DH, Haugan K, Johansen B, Jorgensen T, Knudsen G, Strom A. 1992. Development of a gene transfer system for curing of plasmids in the marine fish pathogen Vibrio salmonicida. Appl Environ Microbiol 58:1980–1985. [PubMed]
135. Mandel MJ, Wollenberg MS, Stabb EV, Visick KL, Ruby EG. 2009. A single regulatory gene is sufficient to alter bacterial host range. Nature 458:215–218. [PubMed][CrossRef]
136. Vezzi A, Campanaro S, D’Angelo M, Simonato F, Vitulo N, Lauro FM, Cestaro A, Malacrida G, Simionati B, Cannata N, Romualdi C, Bartlett DH, Valle G. 2005. Life at depth: Photobacterium profundum genome sequence and expression analysis. Science 307:1459–1461. [PubMed][CrossRef]
137. Mazel D, Dychinco B, Webb VA, Davies J. 1998. A distinctive class of integron in the Vibrio cholerae genome. Science 280:605–608. [PubMed][CrossRef]
138. Hall RM, Collis CM. 1995. Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination. Mol Microbiol 15:593–600. [PubMed][CrossRef]
139. Mazel D. 2006. Integrons: agents of bacterial evolution. Nat Rev Microbiol 4:608–620. [PubMed][CrossRef]
140. Chowdhury N, Asakura M, Neogi SB, Hinenoya A, Haldar S, Ramamurthy T, Sarkar BL, Faruque SM, Yamasaki S. 2010. Development of simple and rapid PCR-fingerprinting methods for Vibrio cholerae on the basis of genetic diversity of the superintegron. J Appl Microbiol 109:304–312. [PubMed]
141. Rowe-Magnus DA, Guerout AM, Mazel D. 1999. Super-integrons. Res Microbiol 150:641–651. [PubMed][CrossRef]
142. Eisen JA, Heidelberg JF, White O, Salzberg SL. 2000. Evidence for symmetric chromosomal inversions around the replication origin in bacteria. Genome Biol 1:research0011. doi:10.1186/gb-2000-1-6-research0011. [PubMed][CrossRef]
143. Stokes HW, O’Gorman DB, Recchia GD, Parsekhian M, Hall RM. 1997. Structure and function of 59-base element recombination sites associated with mobile gene cassettes. Mol Microbiol 26:731–745. [PubMed][CrossRef]
144. Rowe-Magnus DA, Guerout AM, Biskri L, Bouige P, Mazel D. 2003. Comparative analysis of superintegrons: engineering extensive genetic diversity in the Vibrionaceae. Genome Res 13:428–442. [PubMed][CrossRef]
145. Rowe-Magnus DA, Guerout AM, Ploncard P, Dychinco B, Davies J, Mazel D. 2001. The evolutionary history of chromosomal super-integrons provides an ancestry for multiresistant integrons. Proc Natl Acad Sci U S A 98:652–657. [PubMed][CrossRef]
146. Hall RM, Collis CM. 1998. Antibiotic resistance in gram-negative bacteria: the role of gene cassettes and integrons. Drug Resist Updat 1:109–119. [PubMed][CrossRef]
147. Espinoza-Valles I, Soto-Rodriguez S, Edwards RA, Wang Z, Vora GJ, Gomez-Gil B. 2012. Draft genome sequence of the shrimp pathogen Vibrio harveyi CAIM 1792. J Bacteriol 194:2104. doi:10.1128/JB.00079-12. [PubMed][CrossRef]
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/content/journal/microbiolspec/10.1128/microbiolspec.VE-0009-2014
2015-09-11
2017-06-26

Abstract:

Similar to other genera and species of bacteria, whole genomic sequencing has revolutionized how we think about and address questions of basic biology. In this review we examined 36 completely sequenced and annotated members of the family, encompassing 12 different species of the genera , and . We reconstructed the phylogenetic relationships among representatives of this group of bacteria by using three housekeeping genes and 16S rRNA sequences. With an evolutionary framework in place, we describe the occurrence and distribution of primary and alternative sigma factors, global regulators present in all bacteria. Among we show that the number and function of many of these sigma factors differs from species to species. We also describe the role of the -specific regulator ToxRS in fitness and survival. Examination of the biochemical capabilities was and still is the foundation of classifying and identifying new species. Using comparative genomics, we examine the distribution of carbon utilization patterns among species as a possible marker for understanding bacteria-host interactions. Finally, we discuss the significant role that horizontal gene transfer, specifically, the distribution and structure of integrons, has played in evolution.

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Figures

Image of FIGURE 1
FIGURE 1

Evolutionary relationships of species based the concatenated housekeeping genes , , and . The evolutionary history was inferred by using the Neighbor-Joining method. The optimal tree with the sum of branch length = 2.24860938 is shown. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches. The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The evolutionary distances were computed by using the Jukes-Cantor method and are in the units of the number of base substitutions per site. The analysis involved 60 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All ambiguous positions were removed for each sequence pair. There were a total of 6,012 positions in the final data set. Evolutionary analyses were conducted in MEGA5 ( 120 ). doi:10.1128/microbiolspec.VE-0009-2014.f1

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
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Image of FIGURE 2
FIGURE 2

Evolutionary relationships of taxa based on 16S rDNA sequence. The evolutionary history was inferred by using the Neighbor-Joining method. The optimal tree with the sum of branch length = 0.47043464 is shown. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches ( 30 ). The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The evolutionary distances were computed by using the Jukes-Cantor method and are in the units of the number of base substitutions per site ( 52 ). The analysis involved 58 nucleotide sequences. All ambiguous positions were removed for each sequence pair. There were a total of 1,564 positions in the final data set. Evolutionary analyses were conducted in MEGA5 ( 120 ). doi:10.1128/microbiolspec.VE-0009-2014.f2

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
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Image of FIGURE 3
FIGURE 3

Phylogenetic tree constructed from the alignment of sigma-70 family sigma factors by using the amino acid sequences of the highly conserved domains 2 and 4. The program MEGA was used to construct a neighbor-joining tree using the Poisson model, complete deletion, and a bootstrap value of 1,000 ( 120 ). Abbreviations are: Ec, Vp, Vc, Vv; Vh, Vf, Va, Vs, Vaa, Vfu, . Phylogenetic analysis shows that there are two main subfamilies of sigma factors, primary and extracytoplasmic function (ECF) type. Phylogenetic analysis also shows that predicted RpoD, RpoF, RpoS, RpoH, and RpoE sigma factors encoded by each species analyzed do cluster with and are homologues to those found in . The analysis also shows additional primary-like alternative sigma factors found in five of the species that are closely related to RpoS. The analysis also demonstrates that there are multiple putative ECF factors found within the species analyzed, forming distinct clades. doi:10.1128/microbiolspec.VE-0009-2014.f3

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
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FIGURE 4

Phylogenetic analysis of . This phylogenetic tree illustrates the relationship among 57 species. The tree was constructed in MEGA5 by using the Neighbor-Joining method and a bootstrap value of 1,000 and complete deletion ( 30 , 52 , 120 ). doi:10.1128/microbiolspec.VE-0009-2014.f4

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
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FIGURE 5

Genome context and arrangement of region XII cluster among species. Open reading frames (ORFs) are indicated as arrows, the direction of which shows the direction of transcription; numbers underneath ORFs represent locus tags. ORFs of similar color represent homologous pathway genes among the different species examined. Asterisk represents incomplete genome sequence. The region is present in all strains examined. doi:10.1128/microbiolspec.VE-0009-2014.f5

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
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FIGURE 6

Phylogenetic tree based on the Neighbor-Joining method ( 13 ) using and concatenated sequences of , and genes of 20 strains of 11 different species whose whole genome sequences are completed. The locus tag of each gene was used whenever appropriate. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches ( 30 ). The evolutionary distances were computed by using the Jukes-Cantor method ( 52 ) and evolutionary analyses were conducted in MEGA5 ( 120 ). Here, Black circle and diamond indicate the strains that bear the superintegron in Chr II and Chr I, respectively. doi:10.1128/microbiolspec.VE-0009-2014.f6

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
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Tables

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TABLE 1

Genome features of sequenced species

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
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TABLE 2

Total and clade-specific variable and parsimony-informative sites and singleton percentages in the HK genes

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
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TABLE 3

Number of primary and alternative sigma factors present among species

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014
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TABLE 4

Superintegron (SI) in species

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.VE-0009-2014

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