A polyphasic approach for the differentiation of environmental Vibrio isolates from temperate waters

FEMS Microbiology Ecology

Volumn 75, Issue 1, 2011, Pages 145-162

  Oberbeckmann, Sonja ^a   Wichels, Antje ^a   Maier, Thomas ^b   Kostrzewa, Markus ^b   Raffelberg, Sarah ^a   Gerdts, Gunnar ^a  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^b BRUKER DALTONIK GMBH   (Germany)

Author keywords

Classification; Environmental samples; Genomic fingerprinting; Multivariate statistics; RpoB; Vibrio parahaemolyticus

Indexed keywords

BACTERIAL DNA; RNA 16S; SEA WATER;

BACTERIUM; CLIMATE CHANGE; CLUSTER ANALYSIS; COMMUNITY STRUCTURE; ENVIRONMENTAL MONITORING; GENETIC ANALYSIS; GENOMICS; IONIZATION; LASER; MARINE ENVIRONMENT; MATRIX; PATHOGENICITY; POPULATION STRUCTURE; SEAWATER; TAXONOMY; TEMPERATE ENVIRONMENT;

ARTICLE; ATLANTIC OCEAN; BACTERIAL GENE; CLASSIFICATION; COMPARATIVE STUDY; DNA FINGERPRINTING; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METHODOLOGY; MICROBIOLOGY; MULTIVARIATE ANALYSIS; PATHOGENICITY; PHYLOGENY; POLYMERASE CHAIN REACTION; TEMPERATURE; VIBRIO ALGINOLYTICUS; VIBRIO PARAHAEMOLYTICUS; VIRULENCE;

DNA FINGERPRINTING; DNA, BACTERIAL; GENES, BACTERIAL; MULTIVARIATE ANALYSIS; NORTH SEA; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, DNA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TEMPERATURE; VIBRIO ALGINOLYTICUS; VIBRIO PARAHAEMOLYTICUS; VIRULENCE; WATER MICROBIOLOGY;

ATLANTIC OCEAN; GERMAN BIGHT; NORTH SEA;

VIBRIO; VIBRIO ALGINOLYTICUS; VIBRIO PARAHAEMOLYTICUS;

EID: 78650018925     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2010.00998.x     Document Type: Article

References (84)

1. Altschul S, Gish W, Miller W, Myers E & Lipman D (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Anderson D & McKay L (1983) Simple and rapid method for isolating large plasmid DNA from lactic streptococci. Appl Environ Microb 46: 549-552.
3. Ansaruzzaman M, Lucas M, Deen J et al. (2005) Pandemic serovars (O3:K6 and O4:K68) of Vibrio parahaemolyticus associated with diarrhea in Mozambique: spread of the pandemic into the African continent. J Clin Microbiol 43: 2559-2562.
4. Baker-Austin C, Stockley L, Rangdale R & Martinez-Urtaza J (2010) Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: a European perspective. Environ Microbiol Rep 2: 7-18.
5. Bauer A & Rørvik L (2007) A novel multiplex PCR for the identification of Vibrio parahaemolyticus, Vibrio cholerae and Vibrio vulnificus. Lett Appl Microbiol 45: 371-375.
6. Bej A, Patterson D, Brasher C, Vickery M, Jones D & Kaysner C (1999) Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh and trh. J Microbiol Meth 36: 215-225.
7. Cabanillas-Beltrán H, LLausás-Magaña E, Romero R et al. (2006) Outbreak of gastroenteritis caused by the pandemic Vibrio parahaemolyticus O3:K6 in Mexico. FEMS Microbiol Lett 265: 76-80.
8. Caburlotto G, Gennari M, Ghidini V, Tafi M & Lleo MM (2009) Presence of T3SS2 and other virulence-related genes in tdh-negative Vibrio parahaemolyticus environmental strains isolated from marine samples in the area of the Venetian Lagoon, Italy. FEMS Microbiol Ecol 70: 506-514.
9. Chowdhury A, Ishibashi M, Thiem VD et al. (2004) Emergence and serovar transition of Vibrio parahaemolyticus pandemic strains isolated during a diarrhea outbreak in Vietnam between 1997 and 1999. Microbiol Immunol 48: 319-327.
10. Clarke K & Gorley R (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UK.
11. Colwell R (1996) Global climate and infectious disease: the cholera paradigm. Science 274: 2025-2031.
12. Croci L, Suffredini E, Cozzi L et al. (2007) Comparison of different biochemical and molecular methods for the identification of Vibrio parahaemolyticus. J Appl Microbiol 102: 229-237.
13. Daniels N, MacKinnon L, Bishop R et al. (2000) Vibrio parahaemolyticus infections in the United States, 1973-1998. J Infect Dis 181: 1661-1666.
14. DePaola A & Kaysner CA (2004) Vibrio- Bacteriological Analytical Manual Online. U.S. Food and Drug Administration. Available at
15. Dieckmann R, Strauch E & Alter T (2010) Rapid identification and characterization of Vibrio species using whole-cell MALDI-TOF mass spectrometry. J Appl Microbiol 109: 199-211.
16. Drake LA, Doblin MA & Dobbs FC (2007) Potential microbial bioinvasions via ships' ballast water, sediment, and biofilm. Mar Pollut Bull 55: 333-341.
17. Eiler A, Johansson M & Bertilsson S (2006) Environmental influences on Vibrio populations in northern temperate and Boreal coastal waters (Baltic and Skagerrak Seas). Appl Environ Microb 72: 6004-6011.
18. Ellingsen A, Jørgensen H, Wagley S, Monshaugen M & Rørvik L (2008) Genetic diversity among Norwegian Vibrio parahaemolyticus. J Appl Microbiol 105: 2195-2202.
19. Farmer JJ III, Janda M, Brenner FW, Cameron DN & Birkhead KM (2005) Genus I. Vibrio Pacini 1854, 411. Bergey's Manual of Systematic Bacteriology, The Prokaryotes, Part B: The Gammaproteobacteria, Vol. 2 (Brenner DJ, Krieg NR & Staley JT, eds), pp. 494-546. Springer, East Lansing, MI.
20. FDA (2001) Wagatsuma Agar (M178). Bacteriological Analytical Manual Online. U.S. Food and Drug Administration. Available at
21. Felsenstein J (1993) PHYLIP (Phylogeny Inference Package). 3.5c ed.
22. Fenselau C & Demirev P (2001) Characterization of intact microorganisms by MALDI mass spectrometry. Mass Spectrom Rev 20: 157-171.
23. García K, Torres R, Uribe P, Hernández C, Rioseco M, Romero J & Espejo R (2009) Dynamics of clinical and environmental Vibrio parahaemolyticus strains during seafood-related summer diarrhea outbreaks in southern Chile. Appl Environ Microb 75: 7482-7487.
24. Gonzalez N, Cachicas V, Acevedo C et al. (2005) Vibrio parahaemolyticus diarrhea, Chile, 1998 and 2004. Emerg Infect Dis 11: 129-131.
25. Gonzalez-Escalona N, Romero J & Espejo RT (2005) Polymorphism and gene conversion of the 16S rRNA genes in the multiple rRNA operons of Vibrio parahaemolyticus. FEMS Microbiol Lett 246: 213-219.
26. Hazen T, Kennedy K, Chen S, Yi S & Sobecky P (2009a) Inactivation of mismatch repair increases the diversity of Vibrio parahaemolyticus. Environ Microbiol 11: 1254-1266.
27. Hazen T, Martinez R, Chen Y et al. (2009b) Rapid identification of Vibrio parahaemolyticus by whole-cell matrix-assisted laser desorption ionization-time of flight mass spectrometry. Appl Environ Microb 75: 6745-6756.
28. Honda T & Iida T (1993) The pathogenicity of Vibrio parahaemolyticus and the role of the thermostable direct haemolysin and related haemolysins. Rev Med Microbiol 4: 106-113.
29. Honda T, Ni Y & Miwatani T (1989) Purification of a tdh-related hemolysin produced by a Kanagawa phenomenon-negative clinical isolate of Vibrio parahaemolyticus 06-K46. FEMS Microbiol Lett 57: 241-246.
30. Honda T, Abad-Lapuebla M, Ni Y, Yamamoto K & Miwatani T (1991) Characterization of a new thermostable direct haemolysin produced by a Kanagawa-phenomenon-negative clinical isolate of Vibrio parahaemolyticus. J Gen Microbiol 137: 253-259.
31. Hulton C, Higgins C & Sharp P (1991) ERIC sequences: a novel family of repetitive elements in the genomes of Escherichia coli, Salmonella typhimurium and other enterobacteria. Mol Microbiol 5: 825-834.
32. Izutsu K, Kurokawa K, Tashiro K, Kuhara S, Hayashi T, Honda T & Iida T (2008) Comparative genomic analysis using microarray demonstrates a strong correlation between the presence of the 80-kilobase pathogenicity Island and pathogenicity in Kanagawa phenomenon-positive Vibrio parahaemolyticus strains. Infect Immun 76: 1016-1023.
33. Jark U & Kirschke C (2009) Qualitativer Nachweis von Vibrionen. (Fischereierzeugnisse LAVES Institut für Fische und Fischereierzeugnisse ed.), Cuxhaven.
34. Jegathesan M & Paramasivam T (1976) Emergence of Vibrio parahaemolyticus as an important cause of diarrhea in Malaysia. Am J Trop Med Hyg 25: 201-202.
35. Ki J, Zhang R, Zhang W, Huang Y & Qian P (2009) Analysis of RNA polymerase beta subunit (rpoB) gene sequences for the discriminative power of marine Vibrio species. Microb Ecol 58: 679-691.
36. Kim Y, Okuda J, Matsumoto C, Takahashi N, Hashimoto S & Nishibuchi M (1999) Identification of Vibrio parahaemolyticus strains at the species level by PCR targeted to the toxR gene. J Clin Microbiol 37: 1173-1177.
37. Kita-Tsukamoto K, Oyaizu H, Nanba K & Simidu U (1993) Phylogenetic relationships of marine bacteria, mainly members of the family Vibrionaceae, determined on the basis of 16S rRNA sequences. Int J Syst Bacteriol 43: 8-19.
38. Kobayashi T, Enomoto S, Sakazaki R & Kuwahara S (1963) A new selective isolation medium for the Vibrio group; on a modified Nakanishi's medium (TCBS agar medium. Nippon Saikingaku Zasshi 18: 387-392.
39. Lesmana M, Subekti D, Simanjuntak CH, Tjaniadi P, Campbell JR & Oyofo BA (2001) Vibrio parahaemolyticus associated with cholera-like diarrhea among patients in North Jakarta, Indonesia. Diag Microbiol Infect Dis 39: 71-75.
40. Lhafi SK & Kühne M (2007) Occurrence of Vibrio spp. in blue mussels (Mytilus edulis) from the German Wadden Sea. Int J Food Microbiol 116: 297-300.
41. Lin Z, Kumagai K, Baba K, Mekalanos JJ & Nishibuchi M (1993) Vibrio parahaemolyticus has a homolog of the Vibrio cholerae ToxRS operon that mediates environmentally induced regulation of the thermostable direct hemolysin gene. J Bacteriol 175: 3844-3855.
42. Ludwig W, Strunk O, Westram R et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
43. Makino K, Oshima K, Kurokawa K et al. (2003) Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 361: 743-749.
44. Maluping RP, Ravelo C, Lavilla-Pitogo CR, Krovacek K & Romalde JL (2005) Molecular typing of Vibrio parahaemolyticus strains isolated from the Philippines by PCR-based methods. J Appl Microbiol 99: 383-391.
45. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ & Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microb 64: 795-799.
46. Martin B, Humbert O, Camara M et al. (1992) A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae. Nucleic Acids Res 20: 3479-3483.
47. Martinez-Urtaza J, Simental L, Velasco D et al. (2005) Pandemic Vibrio parahaemolyticus O3:K6, Europe. Emerg Infect Dis 11: 1319-1320.
48. Massad G & Oliver JD (1987) New selective and differential medium for Vibrio cholerae and Vibrio vulnificus. Appl Environ Microb 53: 2262-2264.
49. McCarthy SA & Khambaty FM (1994) International dissemination of epidemic Vibrio cholerae by chargo ship ballast and other nonpotable waters. Appl Environ Microb 60: 2597-2601.
50. Mellmann A, Cloud J, Maier T et al. (2008) Evaluation of matrix-assisted laser desorption ionization-time-of-flight mass spectrometry in comparison to 16S rRNA gene sequencing for species identification of nonfermenting bacteria. J Clin Microbiol 46: 1946-1954.
51. Mimura H, Katakura R & Ishida H (2005) Changes of microbial populations in a ship's ballast water and sediments on a voyage from Japan to Qatar. Mar Pollut Bull 50: 751-757.
52. Mollet C, Drancourt M & Raoult D (1997) rpoB sequence analysis as a novel basis for bacterial identification. Mol Microbiol 26: 1005-1011.
53. Moreno C, Romero J & Espejo RT (2002) Polymorphism in repeated 16S rRNA genes is a common property of type strains and environmental isolates of the genus Vibrio. Microbiology-Sgm 148: 1233-1239.
54. Muyzer G, De Waal E & Uitterlinden A (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microb 59: 695-700.
55. 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.
56. Nasu H, Iida T, Sugahara T et al. (2000) A filamentous phage associated with recent pandemic Vibrio parahaemolyticus O3:K6 strains. J Clin Microbiol 38: 2156-2161.
57. Nishibuchi M & Kaper JB (1985) Nucleotide sequence of the thermostable direct hemolysin gene of Vibrio parahaemolyticus. J Bacteriol 162: 558-564.
58. Nishibuchi M & Kaper JB (1995) Thermostable direct hemolysin gene of Vibrio parahaemolyticus- a virulence gene aquired by a marine bacterium. Infect Immun 63: 2093-2099.
59. Nishibuchi M, Taniguchi T, Misawa T, Khaeomaneeiam V, Honda T & Miwatani T (1989) Cloning and nucleotide sequence of the gene (trh) encoding the hemolysin related to the thermostable direct hemoylsin of Vibrio parahaemolyticus. Infect Immun 57: 2691-2697.
60. Okuda J & Nishibuchi M (1998) Manifestation of the Kanagawa phenomenon, the virulence-associated phenotype, of Vibrio parahaemolyticus depends on a particular single base change in the promoter of the thermostable direct haemolysin gene. Mol Microbiol 30: 499-511.
61. Okuda J, Ishibashi M, Hayakawa E et al. (1997) Emergence of a unique O3:K6 clone of Vibrio parahaemolyticus in Calcutta, India, and isolation of strains from the same clonal group from Southeast Asian travelers arriving in Japan. J Clin Microbiol 35: 3150-3155.
62. Oliver JD & Kaper JB (1997) Vibrio species. Food Microbiology, Fundamentals and Frontiers (Doyle MP, Beuchat LR & Montville TJ, eds), pp. 228-264. ASM Press, Washington DC.
63. Ottaviani D, Leoni F, Rocchegiani E et al. (2008) First clinical report of pandemic Vibrio parahaemolyticus O3:K6 infection in Italy. J Clin Microbiol 46: 2144-2145.
64. Paz S, Bisharat N, Paz E, Kidar O & Cohen D (2007) Climate change and the emergence of Vibrio vulnificus disease in Israel. Environ Res 103: 390-396.
65. Rademaker JLW & De Bruijn FJ (1997) Characterization and classification of microbes by rep-PCR genomic fingerprinting and computer-assisted pattern analysis. DNA Markers: Protocols, Applications and Overviews (Caetoan-Anollés aPMG G, eds), pp. 151-171. John Wiley & Sons Inc., New York.
66. Robert-Pillot A, Guenole A & Fournier JM (2002) Usefulness of R72H PCR assay for differentiation between Vibrio parahaemolyticus and Vibrio alginolyticus species: validation by DNA-DNA hybridization. FEMS Microbiol Lett 215: 1-6.
67. Rosec JP, Simon M, Causse V & Boudjemaa M (2009) Detection of total and pathogenic Vibrio parahaemolyticus in shellfish: comparison of PCR protocols using pR72H or toxR targets with a culture method. Int J Food Microbiol 129: 136-145.
68. Sauer S, Freiwald A, Maier T, Kube M, Reinhardt R, Kostrzewa M & Geider K (2008) Classification and identification of bacteria by mass spectrometry and computational analysis. PLoS ONE 3: e2843.
69. Sen B, Dutta B, Chatterjee S et al. (2007) The first outbreak of acute diarrhea due to a pandemic strain of Vibrio parahaemolyticus O3:K6 in Kolkata, India. Int J Infect Dis 11: 185-187.
70. Stern M, Ames G, Smith N, Robinson E & Higgins C (1984) Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell 37: 1015-1026.
71. Stewart JR, Gast RJ, Fujioka RS et al. (2008) The coastal environment and human health: microbial indicators, pathogens, sentinels and reservoirs. Environ Health 7 suppl. 2, p. 3.
72. Tada J, Ohashi T, Nishimura N et al. (1992) Detection of the thermostable direct hemolysin gene (tdh) and the thermostable direct hemolysin-related hemolysin gene (trh) of Vibrio parahaemolyticus by polymerase chain-reaction. Mol Cell Probes 6: 477-487.
73. Takahashi CK, Lourenco N, Lopes TF, Rall VLM & Lopes CAM (2008) Ballast water: a review of the impact on the world public health. J Venom Anim Toxins Incl Trop Dis 14: 393-408.
74. Taniguchi H, Ohta H, Ogawa M & Mizuguchi Y (1985) Cloning and expression in Escherichia coli of Vibrio parahaemolyticus thermostable direct hemolysin and thermolabile hemolysin genes. J Bacteriol 162: 510-515.
75. Taniguchi H, Hirano H, Kubomura S, Higashi K & Mizuguchi Y (1986) Comparison of the nucleotide sequences of the genes for the thermostable direct hemolysin and the thermolabile hemolysin from Vibrio parahaemolyticus. Microb Pathogenesis 1: 425-432.
76. Tarr C, Patel J, Puhr N, Sowers E, Bopp C & Strockbine N (2007) Identification of Vibrio isolates by a multiplex PCR assay and rpoB sequence determination. J Clin Microbiol 45: 134-140.
77. Thompson FL, Iida T & Jean Swings J (2004) Biodiversity of Vibrios. Microbiol Mol Biol R 68: 1092-2172.
78. Versalovic J, Koeuth T & Lupski J (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19: 6823-6831.
79. Versalovic J, Schneider M, De Bruijn F & Lupski J (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Method Mol Cell Biol 5: 25-40.
80. Wagatsuma S (1968) A medium for the test of the hemolytic activity of Vibrio parahaemolyticus. Media Circle 13: 159-162.
81. Wiltshire KH & Manly BFJ (2004) The warming trend at Helgoland Roads, North Sea: phytoplankton response. Helgoland Mar Res 58: 269-273.
82. Wong HC & Lin CH (2001) Evaluation of typing of Vibrio parahaemolyticus by three PCR methods using specific primers. J Clin Microbiol 39: 4233-4240.
83. Xie ZY, Hu CQ, Chen C, Zhang LP & Ren CH (2005) Investigation of seven Vibrio virulence genes among Vibrio alginolyticus and Vibrio parahaemolyticus strains from the coastal mariculture systems in Guangdong, China. Lett Appl Microbiol 41: 202-207.
84. Yeung P & Boor K (2004) Epidemiology, pathogenesis, and prevention of foodborne Vibrio parahaemolyticus infections. Foodborne Pathog Dis 1: 74-88.