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PMID: 19099551 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

The genome sequence of the fish pathogen Aliivibrio salmonicida strain LFI1238 shows extensive evidence of gene decay.

BMC genomics ·Vol. 9 ·2008-12-19 ·Pages 616

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

Abstract

The fish pathogen Aliivibrio salmonicida is the causative agent of cold-water vibriosis in marine aquaculture. The Gram-negative bacterium causes tissue degradation, hemolysis and sepsis in vivo. In total, 4 286 protein coding sequences were identified, and the 4.6 Mb genome of A. salmonicida has a six partite architecture with two chromosomes and four plasmids. Sequence analysis revealed a highly fragmented genome structure caused by the insertion of an extensive number of insertion sequence (IS) elements. The IS elements can be related to important evolutionary events such as gene acquisition, gene loss and chromosomal rearrangements. New A. salmonicida functional capabilities that may have been aquired through horizontal DNA transfer include genes involved in iron-acquisition, and protein secretion and play potential roles in pathogenicity. On the other hand, the degeneration of 370 genes and consequent loss of specific functions suggest that A. salmonicida has a reduced metabolic and physiological capacity in comparison to related Vibrionaceae species. Most prominent is the loss of several genes involved in the utilisation of the polysaccharide chitin. In particular, the disruption of three extracellular chitinases responsible for enzymatic breakdown of chitin makes A. salmonicida unable to grow on the polymer form of chitin. These, and other losses could restrict the variety of carrier organisms A. salmonicida can attach to, and associate with. Gene acquisition and gene loss may be related to the emergence of A. salmonicida as a fish pathogen.

MeSH Terms
Aliivibrio salmonicida/genetics Animals Chromosomes, Bacterial/genetics DNA Transposable Elements DNA, Bacterial/genetics Fishes/microbiology Genome, Bacterial Genomics Plasmids/genetics Sequence Alignment Sequence Analysis, DNA
Chemicals
DNA Transposable Elements DNA, Bacterial
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Hjerde Erik
Department of Molecular Biotechnology, Institute of Medical Biology, Faculty of Medicine, University of Tromsø, N-9037 Tromsø, Norway. [email protected]
Lorentzen Marit Sjo
Holden Matthew Tg
Seeger Kathy
Paulsen Steinar
Bason Nathalie
Churcher Carol
Harris David
Norbertczak Halina
Quail Michael A
Sanders Suzanne
Thurston Scott
Parkhill Julian
Willassen Nils Peder
Thomson Nicholas R
References (67)
67 references, click to expand
  1. Attachment of Vibrio alginolyticus to chitin mediated by chitin-binding proteins.
    Microbiology (Reading). 1996 Aug;142 ( Pt 8):2181-6 PMID: 8760933
  2. Conservation of the chitin utilization pathway in the Vibrionaceae.
    Appl Environ Microbiol. 2008 Jan;74(1):44-51 PMID: 17933912
  3. The tad locus: postcards from the widespread colonization island.
    Nat Rev Microbiol. 2007 May;5(5):363-75 PMID: 17435791
  4. Characterization of heme uptake cluster genes in the fish pathogen Vibrio anguillarum.
    J Bacteriol. 2004 Sep;186(18):6159-67 PMID: 15342586
  5. Artemis: sequence visualization and annotation.
    Bioinformatics. 2000 Oct;16(10):944-5 PMID: 11120685
  6. The genomic code: inferring Vibrionaceae niche specialization.
    Nat Rev Microbiol. 2006 Sep;4(9):697-704 PMID: 16894340
  7. Universal replication biases in bacteria.
    Mol Microbiol. 1999 Apr;32(1):11-6 PMID: 10216855
  8. Chitin catabolism in the marine bacterium Vibrio furnissii. Identification and molecular cloning of a chitoporin.
    J Biol Chem. 2000 Oct 20;275(42):33068-76 PMID: 10913115
  9. Channel-tunnels: outer membrane components of type I secretion systems and multidrug efflux pumps of Gram-negative bacteria.
    Rev Physiol Biochem Pharmacol. 2003;147:122-65 PMID: 12783268
  10. The chitinolytic cascade in Vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/kinase.
    Proc Natl Acad Sci U S A. 2004 Jan 13;101(2):627-31 PMID: 14699052
  11. Combining diverse evidence for gene recognition in completely sequenced bacterial genomes.
    Nucleic Acids Res. 1998 Jun 15;26(12):2941-7 PMID: 9611239
  12. Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence.
    Mol Microbiol. 1993 Aug;9(4):773-86 PMID: 8231809
  13. Development of a gene transfer system for curing of plasmids in the marine fish pathogen Vibrio salmonicida.
    Appl Environ Microbiol. 1992 Jun;58(6):1980-5 PMID: 1622274
  14. The Pfam protein families database.
    Nucleic Acids Res. 2002 Jan 1;30(1):276-80 PMID: 11752314
  15. Role of Chitin-Binding Proteins in the Specific Attachment of the Marine Bacterium Vibrio harveyi to Chitin.
    Appl Environ Microbiol. 1993 Feb;59(2):373-9 PMID: 16348865
  16. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications.
    Nucleic Acids Res. 1987 Feb 11;15(3):1281-95 PMID: 3547335
  17. Vibrio cholerae phage K139: complete genome sequence and comparative genomics of related phages.
    J Bacteriol. 2002 Dec;184(23):6592-601 PMID: 12426348
  18. Improved microbial gene identification with GLIMMER.
    Nucleic Acids Res. 1999 Dec 1;27(23):4636-41 PMID: 10556321
  19. Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis.
    Appl Environ Microbiol. 2005 Sep;71(9):5107-15 PMID: 16151093
  20. Improved tools for biological sequence comparison.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444-8 PMID: 3162770
  21. Codon usages in different gene classes of the Escherichia coli genome.
    Mol Microbiol. 1998 Sep;29(6):1341-55 PMID: 9781873
  22. The PROSITE database, its status in 2002.
    Nucleic Acids Res. 2002 Jan 1;30(1):235-8 PMID: 11752303
  23. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1301-14 PMID: 9841673
  24. Vibrios commonly possess two chromosomes.
    J Bacteriol. 2005 Jan;187(2):752-7 PMID: 15629946
  25. Quorum sensing in vibrios: complexity for diversification.
    Int J Med Microbiol. 2006 Apr;296(2-3):61-71 PMID: 16487746
  26. Four novel hemolysin genes of Vibrio anguillarum and their virulence to rainbow trout.
    Microb Pathog. 2005 Oct;39(4):109-19 PMID: 16126365
  27. Plasmid profiling of Vibrio salmonicida for epidemiological studies of cold-water vibriosis in Atlantic salmon (Salmo salar) and cod (Gadus morhua).
    Appl Environ Microbiol. 1990 Apr;56(4):1033-7 PMID: 2160218
  28. Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners.
    Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3004-9 PMID: 15703294
  29. Programmed translational frameshifting.
    Microbiol Rev. 1996 Mar;60(1):103-34 PMID: 8852897
  30. Growth of Atlantic salmon Salmo salar after intraperitoneal administration of vaccines containing adjuvants.
    Dis Aquat Organ. 1998 Mar 5;32(2):91-7 PMID: 9696628
  31. Genomic islands in pathogenic and environmental microorganisms.
    Nat Rev Microbiol. 2004 May;2(5):414-24 PMID: 15100694
  32. Rfam: an RNA family database.
    Nucleic Acids Res. 2003 Jan 1;31(1):439-41 PMID: 12520045
  33. Comparative and genetic analyses of the putative Vibrio cholerae lipopolysaccharide core oligosaccharide biosynthesis (wav) gene cluster.
    Infect Immun. 2002 May;70(5):2419-33 PMID: 11953379
  34. Slipped-strand mispairing can function as a phase variation mechanism in Escherichia coli.
    J Bacteriol. 2003 Dec;185(23):6990-4 PMID: 14617664
  35. Actions of Vibrio vulnificus metalloprotease on human plasma proteinase-proteinase inhibitor systems: a comparative study of native protease with its derivative modified by polyethylene glycol.
    Microbiol Immunol. 1995;39(12):959-66 PMID: 8789055
  36. Haemolysins in Vibrio species.
    J Appl Microbiol. 2005;98(5):1011-9 PMID: 15836469
  37. Genes involved in Haemophilus influenzae type b capsule expression are frequently amplified.
    J Infect Dis. 1993 Feb;167(2):356-64 PMID: 8421169
  38. Massive gene decay in the leprosy bacillus.
    Nature. 2001 Feb 22;409(6823):1007-11 PMID: 11234002
  39. Bisucaberin--a dihydroxamate siderophore isolated from Vibrio salmonicida, an important pathogen of farmed Atlantic salmon (Salmo salar).
    Biometals. 2002 Jun;15(2):153-60 PMID: 12046923
  40. Widespread N-acetyl-D-glucosamine uptake among pelagic marine bacteria and its ecological implications.
    Appl Environ Microbiol. 2002 Nov;68(11):5554-62 PMID: 12406749
  41. Type VI secretion is a major virulence determinant in Burkholderia mallei.
    Mol Microbiol. 2007 Jun;64(6):1466-85 PMID: 17555434
  42. The two TonB systems of Vibrio cholerae: redundant and specific functions.
    Mol Microbiol. 2001 Feb;39(3):801-12 PMID: 11169119
  43. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system.
    Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1528-33 PMID: 16432199
  44. The variation of dTDP-L-rhamnose pathway genes in Vibrio cholerae.
    Microbiology (Reading). 2003 Sep;149(Pt 9):2463-2474 PMID: 12949172
  45. Insertion sequences in prokaryotic genomes.
    Curr Opin Microbiol. 2006 Oct;9(5):526-31 PMID: 16935554
  46. Biodiversity of vibrios.
    Microbiol Mol Biol Rev. 2004 Sep;68(3):403-31, table of contents PMID: 15353563
  47. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18.
    Nature. 2001 Oct 25;413(6858):848-52 PMID: 11677608
  48. The chitin catabolic cascade in the marine bacterium Vibrio furnissii. Molecular cloning, isolation, and characterization of a periplasmic chitodextrinase.
    J Biol Chem. 1996 Dec 27;271(52):33414-24 PMID: 8969204
  49. Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands.
    Bioinformatics. 2006 Sep 15;22(18):2196-203 PMID: 16837528
  50. A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites.
    Int J Neural Syst. 1997 Oct-Dec;8(5-6):581-99 PMID: 10065837
  51. Gene essentiality determines chromosome organisation in bacteria.
    Nucleic Acids Res. 2003 Nov 15;31(22):6570-7 PMID: 14602916
  52. Incidence of Vibrio cholerae and related vibrios in a coastal lagoon and seawater influenced by lake discharges along an annual cycle.
    Appl Environ Microbiol. 1985 Aug;50(2):426-30 PMID: 4051487
  53. ACT: the Artemis Comparison Tool.
    Bioinformatics. 2005 Aug 15;21(16):3422-3 PMID: 15976072
  54. Two tonB systems function in iron transport in Vibrio anguillarum, but only one is essential for virulence.
    Infect Immun. 2004 Dec;72(12):7326-9 PMID: 15557661
  55. Roles of four chitinases (chia, chib, chic, and chid) in the chitin degradation system of marine bacterium Alteromonas sp. strain O-7.
    Appl Environ Microbiol. 2005 Apr;71(4):1811-5 PMID: 15812005
  56. Prediction and experimental testing of ferric uptake regulator regulons in vibrios.
    J Mol Microbiol Biotechnol. 2009;16(3-4):159-68 PMID: 18431050
  57. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae.
    Nature. 2000 Aug 3;406(6795):477-83 PMID: 10952301
  58. Acetylation (O-factor 5) affects the structural and immunological properties of Salmonella typhimurium lipopolysaccharide O antigen.
    Infect Immun. 1995 Feb;63(2):437-41 PMID: 7529745
  59. Genome sequence of Yersinia pestis, the causative agent of plague.
    Nature. 2001 Oct 4;413(6855):523-7 PMID: 11586360
  60. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
    J Mol Biol. 2001 Jan 19;305(3):567-80 PMID: 11152613
  61. Comparative genome analysis of Vibrio vulnificus, a marine pathogen.
    Genome Res. 2003 Dec;13(12):2577-87 PMID: 14656965
  62. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica.
    Nat Genet. 2003 Sep;35(1):32-40 PMID: 12910271
  63. A chitin-binding domain in a marine bacterial chitinase and other microbial chitinases: implications for the ecology and evolution of 1,4-beta-glycanases.
    Microbiology (Reading). 1998 May;144 ( Pt 5):1299-1308 PMID: 9611805
  64. The Vibrio cholerae chitin utilization program.
    Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2524-9 PMID: 14983042
  65. The Widespread Colonization Island of Actinobacillus actinomycetemcomitans.
    Nat Genet. 2003 Jun;34(2):193-8 PMID: 12717435
  66. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  67. 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. 2007 Dec;57(Pt 12):2823-2829 PMID: 18048732
Article Info
Journal
BMC genomics
Abbr.
BMC Genomics
ISSN
1471-2164
Published
2008-12-19
Epub
2008-00-19
Pages
616
Language
English
Region
England
NLM ID
100965258
PMCID
PMC2627896
Subset
IM
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