The genomic code: inferring Vibrionaceae niche specialization

Article metrics

Abstract

The Vibrionaceae show a wide range of niche specialization, from free-living forms to those attached to biotic and abiotic surfaces, from symbionts to pathogens and from estuarine inhabitants to deep-sea piezophiles. The existence of complete genome sequences for closely related species from varied aquatic niches makes this group an excellent case study for genome comparison.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Niche specialization of the Vibrionaceae.
Figure 2: Genome mining to define Vibrionaceae characteristics.
Figure 3: Linear pairwise genome comparison of the Vibrionaceae.
Figure 4: Genomic appraisal of osmoregulation among the Vibrionaceae.

References

  1. 1

    Garrity, G. M., Bell, J. A. & Lilburn, T. in Bergey's Manual of Systematic Bacteriology (eds Brenner, D. J., Krieg, N. R., Staley, J. T. & Garrity, G. M.) 491?494 (Springer, New York, 2005).

  2. 2

    Heidelberg, J. F. et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406, 477?483 (2000).

  3. 3

    Chen, C. Y. et al. Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res. 13, 2577?2587 (2003).

  4. 4

    Makino, K. et al. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 361, 743?749 (2003).

  5. 5

    Ruby, E. G. et al. Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc. Natl Acad. Sci. USA 102, 3004?3009 (2005).

  6. 6

    Vezzi, A. et al. Life at depth: Photobacterium profundum genome sequence and expression analysis. Science 307, 1459?1461 (2005).

  7. 7

    Gulig, P. A., Bourdage, K. L. & Starks, A. M. Molecular pathogenesis of Vibrio vulnificus. J. Microbiol. 43, 118?131 (2005).

  8. 8

    Nyholm, S. V. & McFall-Ngai, M. J. The winnowing: establishing the squid?vibrio symbiosis. Nature Rev. Microbiol. 2, 632?642 (2004).

  9. 9

    Mrazek, J., Spormann, A. M. & Karlin, S. Genomic comparisons among γ-Proteobacteria. Environ. Microbiol. 8, 273?288 (2006).

  10. 10

    Aiyar, S. E., Gaal, T. & Gourse, R. L. rRNA promoter activity in the fast-growing bacterium Vibrio natriegens. J. Bacteriol. 184, 1349?1358 (2002).

  11. 11

    Hurley, C. C., Quirke, A., Reen, F. J. & Boyd, E. F. Four genomic islands that mark post-1995 pandemic Vibrio parahaemolyticus isolates. BMC Genomics 7, 104 (2006).

  12. 12

    Quirke, A.-M., Reen, F. J., Claesson, M. J. & Boyd, E. F. Genomic island identification in Vibrio vulnificus reveals significant genome plasticity in this human pathogen. Bioinformatics 22, 905?910 (2006).

  13. 13

    Williams, K. P. Traffic at the tmRNA gene. J. Bacteriol. 185, 1059?1070 (2003).

  14. 14

    Okada, K., Iida, T., Kita-Tsukamoto, K. & Honda, T. Vibrios commonly possess two chromosomes. J. Bacteriol. 187, 752?757 (2005).

  15. 15

    Trucksis, M., Michalski, J., Deng, Y. K. & Kaper, J. B. The Vibrio cholerae genome contains two unique circular chromosomes. Proc. Natl Acad. Sci. USA 95, 14464?14469 (1998).

  16. 16

    Campanaro, S. et al. Laterally transferred elements and high pressure adaptation in Photobacterium profundum strains. BMC Genomics 6, 122 (2005).

  17. 17

    Schoolnik, G. K. & Yildiz, F. H. The complete genome sequence of Vibrio cholerae: a tale of two chromosomes and of two lifestyles. Genome Biol. 1, R1?R3 (2000).

  18. 18

    Xu, Q., Dziejman, M. & Mekalanos, J. J. Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro. Proc. Natl Acad. Sci. USA 100, 1286?1291 (2003).

  19. 19

    Egan, E. S. & Waldor, M. K. Distinct replication requirements for the two Vibrio cholerae chromosomes. Cell 114, 521?530 (2003).

  20. 20

    Egan, E. S., Lobner-Olesen, A. & Waldor, M. K. Synchronous replication initiation of the two Vibrio cholerae chromosomes. Curr. Biol. 14, R501?R502 (2004).

  21. 21

    Abbott, J. C., Aanensen, D. M., Rutherford, K., Butcher, S. & Spratt, B. G. WebACT? an online companion for the Artemis Comparison Tool. Bioinformatics 21, 3665?3666 (2005).

  22. 22

    Hallin, P. F. & Ussery, D. W. CBS genome atlas database: a dynamic storage for bioinformatic results and sequence data. Bioinformatics 20, 3682?3686 (2004).

  23. 23

    Eberhard, A. et al. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20, 2444?2449 (1981).

  24. 24

    Milton, D. L. Quorum sensing in vibrios: complexity for diversification. Int. J. Med. Microbiol. 296, 61?71 (2006).

  25. 25

    Lupp, C. & Ruby, E. G. Vibrio fischeri uses two quorum-sensing systems for the regulation of early and late colonization factors. J. Bacteriol. 187, 3620?3629 (2005).

  26. 26

    Henke, J. M. & Bassler, B. L. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J. Bacteriol. 186, 6902?6914 (2004).

  27. 27

    Hammer, B. K. & Bassler, B. L. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50, 101?104 (2003).

  28. 28

    McDougald, D. et al. Defences against oxidative stress during starvation in bacteria. Antonie Van Leeuwenhoek 81, 3?13 (2002).

  29. 29

    McDougald, D., Rice, S. A. & Kjelleberg, S. SmcR-dependent regulation of adaptive phenotypes in Vibrio vulnificus. J. Bacteriol. 183, 758?762 (2001).

  30. 30

    Yildiz, F. H., Liu, X. S., Heydorn, A. & Schoolnik, G. K. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol. Microbiol. 53, 497?515 (2004).

  31. 31

    Chatzidaki-Livanis, M., Jones, M. K. & Wright, A. C. Genetic variation in the Vibrio vulnificus group 1 capsular polysaccharide operon. J. Bacteriol. 188, 1987?1998 (2006).

  32. 32

    Kierek, K. & Watnick, P. I. Environmental determinants of Vibrio cholerae biofilm development. Appl. Environ. Microbiol. 69, 5079?5088 (2003).

  33. 33

    Ali, A., Rashid, M. H. & Karaolis, D. K. High-frequency rugose exopolysaccharide production by Vibrio cholerae. Appl. Environ. Microbiol. 68, 5773?5778 (2002).

  34. 34

    Wai, S. N., Mizunoe, Y., Takade, A., Kawabata, S. I. & Yoshida, S. I. 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 (1998).

  35. 35

    Watnick, P. I., Lauriano, C. M., Klose, K. E., Croal, L. & Kolter, R. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol. Microbiol. 39, 223?235 (2001).

  36. 36

    Yildiz, F. H. & Schoolnik, G. K. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc. Natl Acad. Sci. USA 96, 4028?4033 (1999).

  37. 37

    Matz, C. et al. Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proc. Natl Acad. Sci. USA 102, 16819?16824 (2005).

  38. 38

    Yip, E. S., Grublesky, B. T., Hussa, E. A. & Visick, K. L. A novel, conserved cluster of genes promotes symbiotic colonization and σ-dependent biofilm formation by Vibrio fischeri. Mol. Microbiol. 57, 1485?1498 (2005).

  39. 39

    Merrell, D. S. & Camilli, A. The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol. Microbiol. 34, 836?849 (1999).

  40. 40

    Merrell, D. S. & Camilli, A. 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 (2000).

  41. 41

    Smith, B. & Oliver, J. D. 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 (2006).

  42. 42

    Kapfhammer, D., Karatan, E., Pflughoeft, K. J. & Watnick, P. I. Role for glycine betaine transport in Vibrio cholerae osmoadaptation and biofilm formation within microbial communities. Appl. Environ. Microbiol. 71, 3840?3847 (2005).

  43. 43

    Pflughoeft, K. J., Kierek, K. & Watnick, P. I. Role of ectoine in Vibrio cholerae osmoadaptation. Appl. Environ. Microbiol. 69, 5919?5927 (2003).

  44. 44

    Karaolis, D. K. et al. A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc. Natl Acad. Sci. USA 95, 3134?3139 (1998).

  45. 45

    Waldor, M. K. & Mekalanos, J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910?1914 (1996).

  46. 46

    Huq, A., West, P. A., Small, E. B., Huq, M. I. & Colwell, R. R. Influence of water temperature, salinity, and pH on survival and growth of toxigenic Vibrio cholerae serovar 01 associated with live copepods in laboratory microcosms. Appl. Environ. Microbiol. 48, 420?424 (1984).

  47. 47

    Islam, M. S., Drasar, B. S. & Sack, R. B. Probable role of blue-green algae in maintaining endemicity and seasonality of cholera in Bangladesh: a hypothesis. J. Diarrhoeal Dis. Res. 12, 245?256 (1994).

  48. 48

    Kaper, J. B., Morris, J. G. Jr. & Levine, M. M. Cholera. Clin. Microbiol. Rev. 8, 48?86 (1995).

  49. 49

    Tamplin, M. L., Gauzens, A. L., Huq, A., Sack, D. A. & Colwell, R. R. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl. Environ. Microbiol. 56, 1977?1980 (1990).

  50. 50

    Chiavelli, D. A., Marsh, J. W. & Taylor, R. K. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl. Environ. Microbiol. 67, 3220?3225 (2001).

  51. 51

    Kirn, T. J., Jude, B. A. & Taylor, R. K. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438, 863?866 (2005).

  52. 52

    Zampini, M. et al. Vibrio cholerae persistence in aquatic environments and colonization of intestinal cells: involvement of a common adhesion mechanism. FEMS Microbiol. Lett. 244, 267?273 (2005).

  53. 53

    McFall-Ngai, M. J. & Ruby, E. G. Sepiolids and vibrios: when first they meet. BioScience 48, 257?265 (1998).

  54. 54

    Stabb, E. V. & Ruby, E. G. Contribution of pilA to competitive colonization of the squid Euprymna scolopes by Vibrio fischeri. Appl. Environ. Microbiol. 69, 820?826 (2003).

  55. 55

    Nyholm, S. V., Stabb, E. V., Ruby, E. G. & McFall-Ngai, M. J. Establishment of an animal?bacterial association: recruiting symbiotic vibrios from the environment. Proc. Natl Acad. Sci. USA 97, 10231?10235 (2000).

  56. 56

    Riemann, L. & Azam, F. Widespread N-acetyl-D-glucosamine uptake among pelagic marine bacteria and its ecological implications. Appl. Environ. Microbiol. 68, 5554?5562 (2002).

  57. 57

    Reguera, G. & Kolter, R. Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin. J. Bacteriol. 187, 3551?3555 (2005).

  58. 58

    Watnick, P. I., Fullner, K. J. & Kolter, R. A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J. Bacteriol. 181, 3606?3609 (1999).

  59. 59

    Cowell, R. R. et al. in Vibrios in the environment (ed. Colwell, R. R.) 367?387 (John Wiley & Sons, New York, 1984).

  60. 60

    Huq, A. et al. Colonization of the gut of the blue crab (Callinectes sapidus) by Vibrio cholerae. Appl. Environ. Microbiol. 52, 586?588 (1986).

  61. 61

    Boyd, E. F., Heilpern, A. J. & Waldor, M. K. Molecular analyses of a putative CTXphi precursor and evidence for independent acquisition of distinct CTX(phi)s by toxigenic Vibrio cholerae. J. Bacteriol. 182, 5530?5538 (2000).

  62. 62

    Jermyn, W. S. & Boyd, E. F. Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology 148, 3681?3693 (2002).

  63. 63

    Galen, J. E. et al. Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect. Immun. 60, 406?415 (1992).

  64. 64

    Schneider, D. R. & Parker, C. D. Purification and characterization of the mucinase of Vibrio cholerae. J. Infect. Dis. 145, 474?482 (1982).

  65. 65

    Islam, M. S. et al. Chemotaxis between Vibrio cholerae O1 and a blue-green alga, Anabaena sp. Epidemiol. Infect. 134, 645?648 (2006).

  66. 66

    Islam, M. S. et al. Involvement of the hap gene (mucinase) in the survival of Vibrio cholerae O1 in association with the blue-green alga, Anabaena sp. Can. J. Microbiol. 48, 793?800 (2002).

  67. 67

    Jermyn, W. S. & Boyd, E. F. Molecular evolution of Vibrio pathogenicity island-2 (VPI-2): mosaic structure among Vibrio cholerae and Vibrio mimicus natural isolates. Microbiology 151, 311?322 (2005).

  68. 68

    Meibom, K. L., Blokesch, M., Dolganov, N. A., Wu, C. Y. & Schoolnik, G. K. Chitin induces natural competence in Vibrio cholerae. Science 310, 1824?1827 (2005).

  69. 69

    Faruque, S. M. et al. Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area. Proc. Natl Acad. Sci. USA 101, 2123?2128 (2004).

  70. 70

    Dziejman, M. et al. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc. Natl Acad. Sci. USA 99, 1556?1561 (2002).

  71. 71

    O'Shea, Y. A. et al. The Vibrio seventh pandemic island-II is a 26.9 kb genomic island present in Vibrio cholerae El Tor and O139 serogroup isolates that shows homology to a 43.4 kb genomic island in V. vulnificus. Microbiology 150, 4053?4063 (2004).

  72. 72

    Dziejman, M. et al. Genomic characterization of non-O1, non-O139 Vibrio cholerae reveals genes for a type III secretion system. Proc. Natl Acad. Sci. USA 102, 3465?3470 (2005).

  73. 73

    Purdy, A., Rohwer, F., Edwards, R., Azam, F. & Bartlett, D. H. A glimpse into the expanded genome content of Vibrio cholerae through identification of genes present in environmental strains. J. Bacteriol. 187, 2992?3001 (2005).

  74. 74

    Blake, P. A., Weaver, R. E. & Hollis, D. G. Diseases of humans (other than cholera) caused by vibrios. Annu. Rev. Microbiol. 34, 341?367 (1980).

  75. 75

    Daniels, N. A. et al. Vibrio parahaemolyticus infections in the United States, 1973?1998. J. Infect. Dis. 181, 1661?1666 (2000).

  76. 76

    Matsumoto, C. et al. Pandemic spread of an O3:K6 clone of Vibrio parahaemolyticus and emergence of related strains evidenced by arbitrarily primed PCR and toxRS sequence analyses. J. Clin. Microbiol. 38, 578?585 (2000).

  77. 77

    Linkous, D. A. & Oliver, J. D. Pathogenesis of Vibrio vulnificus. FEMS Microbiol. Lett. 174, 207?214 (1999).

  78. 78

    Strom, M. S. & Paranjpye, R. N. Epidemiology and pathogenesis of Vibrio vulnificus. Microbes Infect. 2, 177?188 (2000).

  79. 79

    Nilsson, W. B., Paranjype, R. N., DePaola, A. & Strom, M. S. Sequence polymorphism of the 16S rRNA gene of Vibrio vulnificus is a possible indicator of strain virulence. J. Clin. Microbiol. 41, 442?446 (2003).

  80. 80

    Panicker, G., Vickery, M. C. & Bej, A. K. Multiplex PCR detection of clinical and environmental strains of Vibrio vulnificus in shellfish. Can. J. Microbiol. 50, 911?922 (2004).

  81. 81

    Rosche, T. M., Yano, Y. & Oliver, J. D. A rapid and simple PCR analysis indicates there are two subgroups of Vibrio vulnificus which correlate with clinical or environmental isolation. Microbiol. Immunol. 49, 381?389 (2005).

  82. 82

    Boucher, Y. et al. Recovery and evolutionary analysis of complete integron gene cassette arrays from Vibrio. BMC Evol. Biol. 6, 3 (2006).

  83. 83

    Bartlett, D. H. Pressure effects on in vivo microbial processes. Biochim. Biophys. Acta. 1595, 367?381 (2002).

  84. 84

    Allen, E. E., Facciotti, D. & Bartlett, D. H. Monounsaturated but not polyunsaturated fatty acids are required for growth of the deep-sea bacterium Photobacterium profundum SS9 at high pressure and low temperature. Appl. Environ. Microbiol. 65, 1710?1720 (1999).

Download references

Acknowledgements

Research in E.F.B.'s laboratory is funded by a Science Foundation Ireland (SFI) Research Frontier programme grant and a SFI Investigator programme grant. F.J.R. is funded by an Irish Research Council Science Engineering and Technology Postdoctoral fellowship. S.A.M. is funded by SFI and a Cork City Council grant.

Author information

Correspondence to E. Fidelma Boyd.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

DATABASES

Entrez Genome Project

Escherichia coli

Photobacterium profundum SS9

Pseudoaltermonas haloplanktis

Shewanella oneidensis

Vibrio alginolyticus

Vibrio cholerae N16961

Vibrio fischeri ES114

Vibrio lentus

Vibrio parahaemolyticus RIMD 2210633

Vibrio salmonicida

Vibrio splendidus

Vibrio vulnificus CMCP6

Vibrio vulnificus YJ016

FURTHER INFORMATION

E. Fidelma Boyd's homepage

Artemis Comparison Tool

Rights and permissions

Reprints and Permissions

About this article

Further reading