Science China Earth Sciences

, Volume 61, Issue 10, pp 1357–1368 | Cite as

Significance of Vibrio species in the marine organic carbon cycle—A review

  • Xiaohua ZhangEmail author
  • Heyu Lin
  • Xiaolei Wang
  • Brian Austin


The genus Vibrio, belonging to Gammaproteobacteria of the phylum Proteobacteria, is a genetically and ecologically diverse group of heterotrophic bacteria, that are ubiquitous in marine environments, especially in coastal areas. In particular, vibrios dominate, i.e. up to 10% of the readily culturable marine bacteria in these habitats. The distribution of Vibrio spp. is shaped by various environmental parameters, notably temperature, salinity and dissolved organic carbon. Vibriospp. may utilize a wide range of organic carbon compounds, including chitin (this may be metabolized by most Vibrio spp.), alginic acid and agar. Many Vibrio spp. have very short replication times (as short as ~10 min), which could facilitate them developing into high biomass content albeit for relatively short durations. Although Vibriospp. usually comprise a minor portion (typically ~1% of the total bacterioplankton in coastal waters) of the total microbial population, they have been shown to proliferate explosively in response to various nutrient pulses, e.g., organic nutrients from algae blooms and iron (Fe+) from Saharan dust. Thus, Vibrio spp. may exert large impacts on marine organic carbon cycling especially in marginal seas. Genomics and related areas of investigation will reveal more about the molecular components and mechanisms involved in Vibrio-mediated biotransformation and remineralization processes.


Vibrio Ecology Carbon cycle Marine Organic carbon 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



This work was supported by the National Natural Science Foundation of China (Grant Nos. 91751202, 41521064 & 41506154) and the National Key Research and Development Program of China (Grant No. 2016YFA0601303).


  1. Amaral G R S, Dias G M, Wellington-Oguri M, Chimetto L, Campeão M E, Thompson F L, Thompson C C. 2014. Genotype to phenotype: Identification of diagnostic vibrio phenotypes using whole genome sequences. Int J Syst Evol Microbiol, 64: 357–365CrossRefGoogle Scholar
  2. Amin A K M R, Feng G, Al-saari N, Meirelles P M, Yamazaki Y, Mino S, Thompson F L, Sawabe T, Sawabe T. 2016. The first temporal and spatial assessment of vibrio diversity of the surrounding seawater of coral reefs in ishigaki, Japan. Front Microbiol, 7: 1185CrossRefGoogle Scholar
  3. Araki T, Hayakawa M, Lu Z, Karita S, Morishita T. 1998. Purification and characterization of agarases from a marine bacterium, Vibrio sp. PO-303. J Mar Biotechnol, 6: 260–265Google Scholar
  4. Araki T, Hashikawa S, Morishita T. 2000. Cloning, sequencing, and expression in Escherichia coli of the new gene encoding beta -1,3-Xylanase from a marine bacterium, Vibrio sp. strain XY-214. Appl Environ Microbiol, 66: 1741–1743CrossRefGoogle Scholar
  5. Arnosti C. 2014. Patterns of microbially driven carbon cycling in the ocean: Links between extracellular enzymes and microbial communities. Adv Oceanogr, 2014: 1–12CrossRefGoogle Scholar
  6. Austin B, Zhang X H. 2006. Vibrio harveyi: A significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol, 43: 119–124CrossRefGoogle Scholar
  7. Baker-Austin C, Trinanes J, Gonzalez-Escalona N, Martinez-Urtaza J. 2017. Non-cholera Vibrios: The microbial barometer of climate change. Trends Microbiol, 25: 76–84CrossRefGoogle Scholar
  8. Azam F, Malfatti F. 2007. Microbial structuring of marine ecosystems. Nat Rev Microbiol, 5: 782–791CrossRefGoogle Scholar
  9. Beijerinck M W. 1889. Le Photobacterium luminosum, bactérie lumineuse de la Mer du Nord. Archives Néerlandaises des Sciences Exactes et Naturelles, 23: 401–427Google Scholar
  10. Benner R. 2002. Chemical composition and reactivity. In: Hansell D A, Carlson C A, eds. Biogeochemistry of Marine Dissolved Organic Matter. New York: Academic. 59–90CrossRefGoogle Scholar
  11. Bruhn J B, Nielsen K F, Hjelm M, Hansen M, Bresciani J, Schulz S, Gram L. 2005. Ecology, inhibitory activity, and morphogenesis of a marine antagonistic bacterium belonging to the Roseobacter Clade. Appl Environ Microbiol, 71: 7263–7270CrossRefGoogle Scholar
  12. Chan K, Woo M, Lo K, French G. 1986. Occurrence and distribution of halophilic vibrios in subtropical coastal waters of Hong Kong. Appl Environ Microbiol, 52: 1407–1411Google Scholar
  13. Chao Y, Wang S, Wu S, Wei J, Chen H. 2017. Cloning and characterization of an alginate lyase from marine Vibrio. sp. QD-5. PreprintsGoogle Scholar
  14. Chi W J, Chang Y K, Hong S K. 2012. Agar degradation by microorganisms and agar-degrading enzymes. Appl Microbiol Biotechnol, 94: 917–930CrossRefGoogle Scholar
  15. Chimetto Tonon L A, Thompson J R, Moreira A P B, Garcia G D, Penn K, Lim R, Berlinck R G S, Thompson C C, Thompson F L. 2017. Quantitative detection of active vibrios associated with white plague disease in Mussismilia braziliensis corals. Front Microbiol, 8: 2272CrossRefGoogle Scholar
  16. Connell T D, Metzger D J, Lynch J, Folster J P. 1998. Endochitinase is transported to the extracellular milieu by the eps-encoded general secretory pathway of Vibrio cholerae. J Bacteriol, 180: 5591–5600Google Scholar
  17. Davis B J K, Jacobs J M, Davis M F, Schwab K J, DePaola A, Curriero F C. 2017. Environmental determinants of Vibrio parahaemolyticus in the Chesapeake Bay. Appl Environ Microbiol, 83: e01147–17CrossRefGoogle Scholar
  18. Doi H, Chinen A, Fukuda H, Usuda Y. 2016. Vibrio algivorus sp. nov., an alginate- and agarose-assimilating bacterium isolated from the gut flora of a turban shell marine snail. Int J Syst Evol Microbiol, 1: 3164–3169Google Scholar
  19. Doi H, Tokura Y, Mori Y, Mori K, Asakura Y, Usuda Y, Fukuda H, Chinen A. 2017. Identification of enzymes responsible for extracellular alginate depolymerization and alginate metabolism in Vibrio algivorus. Appl Microbiol Biotechnol, 101: 1581–1592CrossRefGoogle Scholar
  20. Dong J, Hashikawa S, Konishi T, Tamaru Y, Araki T. 2006. Cloning of the novel gene encoding-agarase C from a marine bacterium, Vibrio sp. strain PO-303, and characterization of the gene product. Appl Environ Microbiol, 72: 6399–6401CrossRefGoogle Scholar
  21. Dong J, Tamaru Y, Araki T. 2007. Molecular cloning, expression, and characterization of a β-agarase gene, agaD, from a marine bacterium, Vibrio sp. strain PO-303. Biosci Biotech Biochem, 71: 38–46CrossRefGoogle Scholar
  22. Eilers H, Pernthaler J, Glockner F O, Amann R. 2000. Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol, 66: 3044–3051CrossRefGoogle Scholar
  23. 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 Microbiol, 72: 6004–6011CrossRefGoogle Scholar
  24. Farmer J J, Janda J M, Brenner F W, Cameron D N, Birkhead K M. 2005. Genus I. Vibrio Pacini 1854. In: Brenner D J, Kreig N R, Staley J T, eds. Bergey’s Manual of Systematic Bacteriology. 2nd ed. New York: Springer Science Business Media. 494–546Google Scholar
  25. Feller G, Narinx E, Arpigny J L, Zekhnini Z, Swings J, Gerday C. 1994. Temperature dependence of growth, enzyme secretion and activity of psychrophilic Antarctic bacteria. Appl Microbiol Biotechnol, 41: 477–479CrossRefGoogle Scholar
  26. Fu W, Han B, Duan D, Liu W, Wang C. 2008. Purification and characterization of agarases from a marine bacterium Vibrio sp. F-6. J Ind Microbiol Biotechnol, 35: 915–922CrossRefGoogle Scholar
  27. Fujino T, Okuno Y, Nakada D, Aoyama A, Fukai K, Mukai T, Ueha T. 1951. On the bacteriological examination of shirasu food poisoning (in Japanese). J Jpn Assoc Inf Dis, 25: 11Google Scholar
  28. Gao Z, Ruan L, Chen X, Zhang Y, Xu X. 2010. A novel salt-tolerant endo-β-1,4-glucanase Cel5A in Vibrio sp. G21 isolated from mangrove soil. Appl Microbiol Biotechnol, 87: 1373–1382CrossRefGoogle Scholar
  29. Gao Z M, Xiao J, Wang X N, Ruan L W, Chen X L, Zhang Y Z. 2012. Vibrio xiamenensis sp. nov., a cellulase-producing bacterium isolated from mangrove soil. Int J Syst Evol Microbiol, 62: 1958–1962CrossRefGoogle Scholar
  30. Gilbert J A, Dupont C L. 2011. Microbial metagenomics: Beyond the genome. Annu Rev Mar Sci, 3: 347–371CrossRefGoogle Scholar
  31. Gilbert J A, Steele J A, Caporaso J G, Steinbrück L, Reeder J, Temperton B, Huse S, McHardy A C, Knight R, Joint I, Somerfield P, Fuhrman J A, Field D. 2012. Defining seasonal marine microbial community dynamics. ISME J, 6: 298–308CrossRefGoogle Scholar
  32. Girard L, Peuchet S, Servais P, Henry A, Charni-Ben-Tabassi N, Baudart J. 2017. Spatiotemporal dynamics of total viable Vibrio spp. in a NW Mediterranean coastal area. Microbes Environ, 32: 210–218CrossRefGoogle Scholar
  33. Gomez-Gil B, Thompson C C, Matsumura Y, Sawabe T, Iida T, Christen R. 2014. Family Vibrionaceae (Chapter 225). In: Rosenberg E, DeLong E, Thompson F L, Lory S, Stackebrandt E, eds. The Prokaryotes. 4th ed. New York: Springer. 88Google Scholar
  34. Grimes D J, Johnson C N, Dillon K S, Flowers A R, Noriea N F, Berutti T. 2009. What genomic sequence information has revealed about Vibrio ecology in the ocean—A Review. Microb Ecol, 58: 447–460CrossRefGoogle Scholar
  35. Guerinot M L, West P A, Lee J V, Colwell R R. 1982. Vibrio diazotrophicus sp. nov., a Marine Nitrogen-Fixing Bacterium. Int J Systatic Bacteriology, 32: 350–357CrossRefGoogle Scholar
  36. Hamdan L, Fulmer P. 2011. Effects of COREXIT® EC9500A on bacteria from a beach oiled by the Deepwater Horizon spill. Aquat Microb Ecol, 63: 101–109CrossRefGoogle Scholar
  37. Hickey M E, Lee J L. 2017. A comprehensive review of Vibrio (Listonella) anguillarum: Ecology, pathology and prevention. Rev Aquacult, 161Google Scholar
  38. Honda Y, Taniguchi H, Kitaoka M. 2008. A reducing-end-acting chitinase from Vibrio proteolyticus belonging to glycoside hydrolase family 19. Appl Microbiol Biotechnol, 78: 627–634CrossRefGoogle Scholar
  39. Itoi S, Kanomata Y, Koyama Y, Kadokura K, Uchida S, Nishio T, Oku T, Sugita H. 2007. Identification of a novel endochitinase from a marine bacterium Vibrio proteolyticus strain No. 442. BBA-Proteins Proteom, 1774: 1099–1107CrossRefGoogle Scholar
  40. Joseph S W, Colwell R R, Kaper J B. 1982. Vibrio Parahaemolyticus and related halophilic vibrios. Crit Rev Microbiol, 10: 77–124CrossRefGoogle Scholar
  41. Kadokura K, Rokutani A, Yamamoto M, Ikegami T, Sugita H, Itoi S, Hakamata W, Oku T, Nishio T. 2007. Purification and characterization of Vibrio parahaemolyticus extracellular chitinase and chitin oligosaccharide deacetylase involved in the production of heterodisaccharide from chitin. Appl Microbiol Biotechnol, 75: 357–365CrossRefGoogle Scholar
  42. Kauffman K M, Hussain F A, Yang J, Arevalo P, Brown J M, Chang W K, VanInsberghe D, Elsherbini J, Sharma R S, Cutler M B, Kelly L, Polz M F. 2018. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Nature, 554: 118–122CrossRefGoogle Scholar
  43. Keyhani N O, Roseman S. 1996. The chitin catabolic cascade in the Marine Bacterium Vibrio furnissii. J Biol Chem, 271: 33414–33424CrossRefGoogle Scholar
  44. Kirchman D, White J. 1999. Hydrolysis and mineralization of chitin in the Delaware Estuary. Aquat Microb Ecol, 18: 187–196CrossRefGoogle Scholar
  45. Kiyohara M, Sakaguchi K, Yamaguchi K, Araki T, Nakamura T, Ito M. 2005. Molecular cloning and characterization of a novel β-1,3-xylanase possessing two putative carbohydrate-binding modules from a marine bacterium Vibrio sp. strain AX-4. Biochem J, 388: 949–957CrossRefGoogle Scholar
  46. Kopprio G A, Streitenberger M E, Okuno K, Baldini M, Biancalana F, Fricke A, Martínez A, Neogi S B, Koch B P, Yamasaki S, Lara R J. 2017. Biogeochemical and hydrological drivers of the dynamics of Vibrio species in two Patagonian estuaries. Sci Total Environ, 579: 646–656CrossRefGoogle Scholar
  47. Lapota D, Galt C, Losee J R, Huddell H D, Orzech J K, Nealson K H. 1988. Observations and measurements of planktonic bioluminescence in and around a milky sea. J Exp Mar Biol Ecol, 119: 55–81CrossRefGoogle Scholar
  48. Lehmann K B, Neumann R. 1896. Atlas und Grundriss der Bakteriologie und Lehrbuch der speziellen bakteriologischen Diagnostik. 1st ed. J F Lehmann,MünchenGoogle Scholar
  49. Li X, Roseman S. 2004. The chitinolytic cascade in Vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/ kinase. Proc Natl Acad Sci USA, 101: 627–631CrossRefGoogle Scholar
  50. Li S, Wang L, Hao J, Xing M, Sun J, Sun M. 2016. Purification and characterization of a new alginate lyase from marine bacterium Vibrio sp. SY08. Mar Drugs, 15: 1CrossRefGoogle Scholar
  51. Liao L, Xu X W, Jiang X W, Cao Y, Yi N, Huo Y Y, Wu Y H, Zhu X F, Zhang X Q, Wu M. 2011. Cloning, expression, and characterization of a new β-Agarase from Vibrio sp. strain CN41. Appl Environ Microbiol, 77: 7077–7079CrossRefGoogle Scholar
  52. Lin H, Yu M, Wang X, Zhang X H. 2018. Comparative genomic analysis reveals the evolution and environmental adaptation strategies of vibrios. BMC Genomics, 19: 135CrossRefGoogle Scholar
  53. Liu Z, Liu J. 2013. Evaluating bacterial community structures in oil collected from the sea surface and sediment in the northern Gulf of Mexico after the Deepwater Horizon oil spill. Microbiol Open, 2: 492–504CrossRefGoogle Scholar
  54. Lukjancenko O, Ussery D W. 2014. Vibrio chromosome-specific families. Front Microbiol, 5: 73CrossRefGoogle Scholar
  55. Main C R, Salvitti L R, Whereat E B, Coyne K J. 2015. Community-level and species-specific associations between phytoplankton and particleassociated Vibrio species in Delaware’s Inland Bays. Appl Environ Microbiol, 81: 5703–5713CrossRefGoogle Scholar
  56. Martínez A, Ventouras L A, Wilson S T, Karl D M, DeLong E F. 2013. Metatranscriptomic and functional metagenomic analysis of methylphosphonate utilization by marine bacteria. Front Microbiol, 4Google Scholar
  57. Machado H, Gram L. 2015. The fur gene as a new phylogenetic marker for Vibrionaceae species identification. Appl Environ Microbiol, 81: 2745–2752CrossRefGoogle Scholar
  58. Miller S D, Haddock S H D, Elvidge C D, Lee T F. 2005. Detection of a bioluminescent milky sea from space. Proc Natl Acad Sci USA, 102: 14181–14184CrossRefGoogle Scholar
  59. Oberbeckmann S, Fuchs B M, Meiners M, Wichels A, Wiltshire K H, Gerdts G. 2012. Seasonal dynamics and modeling of a Vibrio community in coastal waters of the North Sea. Microb Ecol, 63: 543–551CrossRefGoogle Scholar
  60. Oliver J D. 2010. Recent findings on the viable but nonculturable state in pathogenic bacteria. Fems Microbiol Rev, 34: 415–425CrossRefGoogle Scholar
  61. Øvreås L, Bourne D, Sandaa R, Casamayor E, Benlloch S, Goddard V, Smerdon G, Heldal M, Thingstad T. 2003. Response of bacterial and viral communities to nutrient manipulations in seawater mesocosms. Aquat Microb Ecol, 31: 109–121CrossRefGoogle Scholar
  62. Pascual J, Macián M C, Arahal D R, Garay E, Pujalte M J. 2010. Multilocus sequence analysis of the central clade of the genus Vibrio by using the 16S rRNA, recA, pyrH, rpoD, gyrB, rctB and toxR genes. Int J Syst Evol Microbiol, 60: 154–165CrossRefGoogle Scholar
  63. Phillips K E, Satchell K J F. 2017. Vibrio vulnificus: From oyster colonist to human pathogen. PLoS Pathog, 13: e1006053CrossRefGoogle Scholar
  64. Rizzo L, Fraschetti S, Alifano P, Tredici M S, Stabili L. 2016. Association of Vibrio community with the Atlantic Mediterranean invasive alga Caulerpa cylindracea. J Exp Mar Biol Ecol, 475: 129–136CrossRefGoogle Scholar
  65. Rubio-Portillo E, Gago J F, Martínez-García M, Vezzulli L, Rosselló-Móra R, Antón J, Ramos-Esplá A A. 2018. Vibrio communities in scleractinian corals differ according to health status and geographic location in the Mediterranean Sea. Syst Appl Microbiol, 41: 131–138CrossRefGoogle Scholar
  66. Rubio-Portillo E, Yarza P, Peñalver C, Ramos-Esplá A A, Antón J. 2014. New insights into Oculina patagonica coral diseases and their associated Vibrio spp. communities. ISME J, 8: 1794–1807CrossRefGoogle Scholar
  67. Ruby E G, Urbanowski M, Campbell J, Dunn A, Faini M, Gunsalus R, Lostroh P, Lupp C, McCann J, Millikan D, Schaefer A, Stabb E, Stevens A, Visick K, Whistler C, Greenberg E P. 2005. Complete genome sequence of Vibrio fischeri: A symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci USA, 102: 3004–3009CrossRefGoogle Scholar
  68. Sakazaki R, Iwanami S, Fukumi H. 1963. Studies on the enteropathogenic facultatively halophilic bacteria Vibrio parahaemolyticus. I. Morphological, cultural and biochemical properties and its taxonomical position. Jpn J Med Sci Biol, 16: 161–188CrossRefGoogle Scholar
  69. Siboni N, Balaraju V, Carney R, Labbate M, Seymour J R. 2016. Spatiotemporal dynamics of Vibrio spp. within the Sydney harbour estuary. Front Microbiol, 7: 460CrossRefGoogle Scholar
  70. Simu K, Hagström A. 2004. Oligotrophic bacterioplankton with a novel single-cell life strategy. Appl Environ Microbiol, 70: 2445–2451CrossRefGoogle Scholar
  71. Sneha K G, Anas A, Jayalakshmy K V, Jasmin C, Das P V V, Pai S S, Pappu S, Nair M, Muraleedharan K R, Sudheesh K, Nair S. 2016. Distribution of multiple antibiotic resistant Vibrio spp. across Palk Bay. Region Stud Mar Sci, 3: 242–250CrossRefGoogle Scholar
  72. Sugano Y, Matsumoto T, Kodama H, Noma M. 1993. Cloning and sequencing of agaA, a unique agarose 0107 gene from a marine bacterium, Vibrio sp. strain JT0107. Appl Environ Microbiol, 59: 3750–3756Google Scholar
  73. Suginta W, Chuenark D, Mizuhara M, Fukamizo T. 2010. Novel β-Nacetylglucosaminidases from Vibrio harveyi 650: Cloning, expression, enzymatic properties, and subsite identification. BMC Biochem, 11: 40CrossRefGoogle Scholar
  74. Suginta W, Vongsuwan A, Songsiriritthigul C, Prinz H, Estibeiro P, Duncan R R, Svasti J, Fothergill-Gilmore L A. 2004. An endochitinase A from Vibrio carchariae: Cloning, expression, mass and sequence analyses, and chitin hydrolysis. Archives Biochem Biophys, 424: 171–180CrossRefGoogle Scholar
  75. Svitil A L, Chadhain S, Moore J A, Kirchman D L. 1997. Chitin degradation proteins produced by the marine bacterium Vibrio harveyi growing on different forms of chitin. Appl Environ Microbiol, 63: 408–413Google Scholar
  76. Takemura A F, Chien D M, Polz M F. 2014. Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level. Front Microbiol, 5: 38CrossRefGoogle Scholar
  77. Tall A, Hervio-Heath D, Teillon A, Boisset-Helbert C, Delesmont R, Bodilis J, Touron-Bodilis A. 2013. Diversity of Vibrio spp. isolated at ambient environmental temperature in the Eastern English Channel as determined by pyrH sequencing. J Appl Microbiol, 114: 1713–1724CrossRefGoogle Scholar
  78. Tanaka M, Umemoto Y, Okamura H, Nakano D, Tamaru Y, Araki T. 2009. Cloning and characterization of a β-1,4-mannanase 5C possessing a family 27 carbohydrate-binding module from a marine bacterium, Vibrio sp. strain MA-138. Biosci Biotech Biochem, 73: 109–116CrossRefGoogle Scholar
  79. Thompson F L, Austin B, Swings J. 2006. The Biology of Vibrios. Washington D C: American Society for MicrobiologyCrossRefGoogle Scholar
  80. Thompson F L, Gevers D, Thompson C C, Dawyndt P, Naser S, Hoste B, Munn C B, Swings J. 2005. Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis. Appl Environ Microbiol, 71: 5107–5115CrossRefGoogle Scholar
  81. Thompson J R, Polz M F. 2006. Dynamics of Vibrio populations and their role in environmental nutrient cycling. In: Thompson F L, Austin B, Swings J, eds. The Biology of Vibrios. Washington D C: ASM Press. 190–203CrossRefGoogle Scholar
  82. Thompson J R, Randa M A, Marcelino L A, Tomita-Mitchell A, Lim E, Polz M F. 2004. Diversity and dynamics of a north atlantic coastal Vibrio community. Appl Environ Microbiol, 70: 4103–4110CrossRefGoogle Scholar
  83. Turner J W, Good B, Cole D, Lipp E K. 2009. Plankton composition and environmental factors contribute to Vibrio seasonality. ISME J, 3: 1082–1092CrossRefGoogle Scholar
  84. Thurber R V, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards R A, Angly F, Dinsdale E, Kelly L, Rohwer F. 2009. Metagenomic analysis of stressed coral holobionts. Environ Microbiol, 11: 2148–2163CrossRefGoogle Scholar
  85. Vezzulli L, Brettar I, Pezzati E, Reid P C, Colwell R R, Höfle M G, Pruzzo C. 2012. Long-term effects of ocean warming on the prokaryotic community: Evidence from the vibrios. ISME J, 6: 21–30CrossRefGoogle Scholar
  86. Vezzulli L, Grande C, Reid P C, Hélaouët P, Edwards M, Höfle M G, Brettar I, Colwell R R, Pruzzo C. 2016. Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic. Proc Natl Acad Sci USA, 113: E5062–E5071CrossRefGoogle Scholar
  87. Vezzulli L, Grande C, Tassistro G, Brettar I, Höfle M G, Pereira R P A, Mushi D, Pallavicini A, Vassallo P, Pruzzo C. 2017. Whole-genome enrichment provides deep insights into Vibrio cholerae Metagenome from an African River. Microb Ecol, 73: 734–738CrossRefGoogle Scholar
  88. Vezzulli L, Pezzati E, Moreno M, Fabiano M, Pane L, Pruzzo C, Pruzzo C. 2009. Benthic ecology of Vibrio spp. and pathogenic Vibrio species in a coastal Mediterranean environment (La Spezia Gulf, Italy). Microb Ecol, 58: 808–818CrossRefGoogle Scholar
  89. Wang H, Liu J, Wang Y, Zhang X H. 2011. Vibrio marisflavi sp. nov., a novel marine bacterium isolated from seawater near the Yellow Sea Cold Water Mass, China. Int J Syst Evol Microbiol, 61: 568–573CrossRefGoogle Scholar
  90. Wang Y, Zhang X H, Yu M, Wang H, Austin B. 2010. Vibrio atypicus sp. nov., isolated from the digestive tract of the Chinese prawn (Penaeus chinensis O’sbeck). Int J Syst Evol Microbiol, 60: 2517–2523CrossRefGoogle Scholar
  91. Wang Z, Robertson K L, Liu C, Liu J L, Johnson B J, Leary D H, Compton J R, Vuddhakul V, Legler P M, Vora G J. 2015. A novel Vibrio betaglucosidase (LamN) that hydrolyzes the algal storage polysaccharide laminarin. Fems Microbiol Ecol, 91: fiv087CrossRefGoogle Scholar
  92. West P A, Okpokwasili G C, Brayton P R, Grimes D J, Colwell R R. 1984. Numerical taxonomy of phenanthrene-degrading bacteria isolated from the Chesapeake Bay. Appl Environ Microbiol, 48: 988–993Google Scholar
  93. Westrich J R, Ebling A M, Landing W M, Joyner J L, Kemp K M, Griffin D W, Lipp E K. 2016. Saharan dust nutrients promote Vibrio bloom formation in marine surface waters. Proc Natl Acad Sci USA, 113: 5964–5969CrossRefGoogle Scholar
  94. Xu H S, Roberts N, Singleton F L, Attwell R W, Grimes D J, Colwell R R. 1982. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb Ecol, 8: 313–323CrossRefGoogle Scholar
  95. Zhang W, Sun L. 2007. Cloning, characterization, and molecular application of a beta-agarase gene from Vibrio sp. strain V134. Appl Environ Microbiol, 73: 2825–2831CrossRefGoogle Scholar
  96. Zhu B, Tan H, Qin Y, Xu Q, Du Y, Yin H. 2015. Characterization of a new endo-type alginate lyase from Vibrio sp. W13. Int J Biol Macromol, 75: 330–337CrossRefGoogle Scholar
  97. Zhu B, Sun Y, Ni F, Ning L, Yao Z. 2018. Characterization of a new endotype alginate lyase from Vibrio sp. NJU-03. Int J Biol Macromol, 108: 1140–1147CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Xiaohua Zhang
    • 1
    • 2
    Email author
  • Heyu Lin
    • 1
  • Xiaolei Wang
    • 1
  • Brian Austin
    • 3
  1. 1.College of Marine Life SciencesOcean University of ChinaQingdaoChina
  2. 2.Laboratory for Marine Ecology and Environmental ScienceQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.Institute of AquacultureUniversity of StirlingStirlingUK

Personalised recommendations