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SCIENCE CHINA Earth Sciences, Volume 61 , Issue 10 : 1357-1368(2018) https://doi.org/10.1007/s11430-017-9229-x

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

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  • ReceivedNov 3, 2017
  • AcceptedMay 29, 2018
  • PublishedAug 6, 2018

Abstract


Funded by

the National Natural Science Foundation of China(Grant,Nos.,91751202,41521064,&,41506154)


Acknowledgment

This work was supported by the National Natural Science Foundation of China (Grant Nos. 41730530, 91751202, 41476112) and the National Key Research and Development Program of China (Grant No. 2016YFA0601303).


References

[1] Amaral G R S, Dias G M, Wellington-Oguri M, Chimetto L, Campeão M E, Thompson F L, Thompson C C. Genotype to phenotype: Identification of diagnostic vibrio phenotypes using whole genome sequences. Int J Syst Evol Microbiol, 2014, 64: 357-365 CrossRef PubMed Google 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. The first temporal and spatial assessment of vibrio diversity of the surrounding seawater of coral reefs in ishigaki, Japan. Front Microbiol, 2016, 7: 1185 CrossRef Google 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: 260–265. Google Scholar

[4] Araki T, Hashikawa S, Morishita T. 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, 2000, 66: 1741-1743 CrossRef Google Scholar

[5] Arnosti C. Patterns of microbially driven carbon cycling in the ocean: Links between extracellular enzymes and microbial communities. Adv Oceanogr, 2014, 2014: 1-12 CrossRef Google Scholar

[6] Austin B, Zhang X H. Vibrio harveyi: A significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol, 2006, 43: 119-124 CrossRef PubMed Google Scholar

[7] Baker-Austin C, Trinanes J, Gonzalez-Escalona N, Martinez-Urtaza J. Non-cholera Vibrios: The microbial barometer of climate change. Trends Microbiol, 2017, 25: 76-84 CrossRef PubMed Google Scholar

[8] Azam F, Malfatti F. Microbial structuring of marine ecosystems. Nat Rev Microbiol, 2007, 5: 782-791 CrossRef PubMed Google Scholar

[9] Beijerinck M W. 1889. Le Photobacterium luminosum, bactérie lumineuse de la Mer du Nord. Archives Néerlandaises des Sciences Exactes et Naturelles, 23: 401–427. Google 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. 59–90. Google Scholar

[11] Bruhn J B, Nielsen K F, Hjelm M, Hansen M, Bresciani J, Schulz S, Gram L. Ecology, inhibitory activity, and morphogenesis of a marine antagonistic bacterium belonging to the Roseobacter Clade. Appl Environ Microbiol, 2005, 71: 7263-7270 CrossRef PubMed Google 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: 1407–1411. Google 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. Preprints. Google Scholar

[14] Chi W J, Chang Y K, Hong S K. Agar degradation by microorganisms and agar-degrading enzymes. Appl Microbiol Biotechnol, 2012, 94: 917-930 CrossRef PubMed Google 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. Quantitative detection of active vibrios associated with white plague disease in Mussismilia braziliensis corals. Front Microbiol, 2017, 8: 2272 CrossRef Google 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: 5591–5600. Google Scholar

[17] Davis B J K, Jacobs J M, Davis M F, Schwab K J, DePaola A, Curriero F C. Environmental determinants of Vibrio parahaemolyticus in the Chesapeake Bay. Appl Environ Microbiol, 2017, 83: e01147-17 CrossRef PubMed Google Scholar

[18] Doi H, Chinen A, Fukuda H, Usuda Y. 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, 2016, 1: 3164-3169 CrossRef PubMed Google Scholar

[19] Doi H, Tokura Y, Mori Y, Mori K, Asakura Y, Usuda Y, Fukuda H, Chinen A. Identification of enzymes responsible for extracellular alginate depolymerization and alginate metabolism in Vibrio algivorus. Appl Microbiol Biotechnol, 2017, 101: 1581-1592 CrossRef PubMed Google Scholar

[20] Dong J, Hashikawa S, Konishi T, Tamaru Y, Araki T. 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, 2006, 72: 6399-6401 CrossRef PubMed Google Scholar

[21] Dong J, Tamaru Y, Araki T. Molecular cloning, expression, and characterization of a β-agarase gene, agaD, from a marine bacterium, Vibrio sp. strain PO-303. Biosci Biotech Biochem, 2007, 71: 38-46 CrossRef PubMed Google Scholar

[22] Eilers H, Pernthaler J, Glockner F O, Amann R. Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol, 2000, 66: 3044-3051 CrossRef Google Scholar

[23] Eiler A, Johansson M, Bertilsson S. Environmental influences on Vibrio populations in northern temperate and boreal coastal waters (Baltic and Skagerrak Seas). Appl Environ Microbiol, 2006, 72: 6004-6011 CrossRef PubMed Google 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. 494–546. Google Scholar

[25] Feller G, Narinx E, Arpigny J L, Zekhnini Z, Swings J, Gerday C. Temperature dependence of growth, enzyme secretion and activity of psychrophilic Antarctic bacteria. Appl Microbiol Biotechnol, 1994, 41: 477-479 CrossRef Google Scholar

[26] Fu W, Han B, Duan D, Liu W, Wang C. Purification and characterization of agarases from a marine bacterium Vibrio sp. F-6. J Ind Microbiol Biotechnol, 2008, 35: 915-922 CrossRef PubMed Google 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: 11. Google Scholar

[28] Gao Z, Ruan L, Chen X, Zhang Y, Xu X. A novel salt-tolerant endo-β-1,4-glucanase Cel5A in Vibrio sp. G21 isolated from mangrove soil. Appl Microbiol Biotechnol, 2010, 87: 1373-1382 CrossRef PubMed Google Scholar

[29] Gao Z M, Xiao J, Wang X N, Ruan L W, Chen X L, Zhang Y Z. Vibrio xiamenensis sp. nov., a cellulase-producing bacterium isolated from mangrove soil. Int J Syst Evol Microbiol, 2012, 62: 1958-1962 CrossRef PubMed Google Scholar

[30] Gilbert J A, Dupont C L. Microbial metagenomics: Beyond the genome. Annu Rev Mar Sci, 2011, 3: 347-371 CrossRef PubMed ADS Google 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. Defining seasonal marine microbial community dynamics. ISME J, 2012, 6: 298-308 CrossRef PubMed Google Scholar

[32] Girard L, Peuchet S, Servais P, Henry A, Charni-Ben-Tabassi N, Baudart J. Spatiotemporal dynamics of total viable Vibrio spp. in a NW Mediterranean coastal area. Microbes Environ, 2017, 32: 210-218 CrossRef PubMed Google 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. 88. Google Scholar

[34] Grimes D J, Johnson C N, Dillon K S, Flowers A R, Noriea N F, Berutti T. What genomic sequence information has revealed about Vibrio ecology in the ocean—A Review. Microb Ecol, 2009, 58: 447-460 CrossRef PubMed Google Scholar

[35] Guerinot M L, West P A, Lee J V, Colwell R R. Vibrio diazotrophicus sp. nov., a Marine Nitrogen-Fixing Bacterium. Int J Systatic Bacteriology, 1982, 32: 350-357 CrossRef Google Scholar

[36] Hamdan L, Fulmer P. Effects of COREXIT® EC9500A on bacteria from a beach oiled by the Deepwater Horizon spill. Aquat Microb Ecol, 2011, 63: 101-109 CrossRef Google Scholar

[37] Hickey M E, Lee J L. A comprehensive review of Vibrio (Listonella) anguillarum: Ecology, pathology and prevention. Rev Aquacult, 2017, 161 CrossRef Google Scholar

[38] Honda Y, Taniguchi H, Kitaoka M. A reducing-end-acting chitinase from Vibrio proteolyticus belonging to glycoside hydrolase family 19. Appl Microbiol Biotechnol, 2008, 78: 627-634 CrossRef PubMed Google Scholar

[39] Itoi S, Kanomata Y, Koyama Y, Kadokura K, Uchida S, Nishio T, Oku T, Sugita H. Identification of a novel endochitinase from a marine bacterium Vibrio proteolyticus strain No. 442. BBA-Proteins Proteom, 2007, 1774: 1099-1107 CrossRef PubMed Google Scholar

[40] Joseph S W, Colwell R R, Kaper J B. Vibrio Parahaemolyticus and related halophilic vibrios. Crit Rev Microbiol,. 1982, 10: 77-124 CrossRef PubMed Google Scholar

[41] Kadokura K, Rokutani A, Yamamoto M, Ikegami T, Sugita H, Itoi S, Hakamata W, Oku T, Nishio T. Purification and characterization of Vibrio parahaemolyticus extracellular chitinase and chitin oligosaccharide deacetylase involved in the production of heterodisaccharide from chitin. Appl Microbiol Biotechnol, 2007, 75: 357-365 CrossRef PubMed Google 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. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Nature, 2018, 554: 118-122 CrossRef PubMed ADS Google Scholar

[43] Keyhani N O, Roseman S. The chitin catabolic cascade in the Marine Bacterium Vibrio furnissii. J Biol Chem, 1996, 271: 33414-33424 CrossRef Google Scholar

[44] Kirchman D, White J. Hydrolysis and mineralization of chitin in the Delaware Estuary. Aquat Microb Ecol, 1999, 18: 187-196 CrossRef Google Scholar

[45] Kiyohara M, Sakaguchi K, Yamaguchi K, Araki T, Nakamura T, Ito M. 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, 2005, 388: 949-957 CrossRef PubMed Google 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. Biogeochemical and hydrological drivers of the dynamics of Vibrio species in two Patagonian estuaries. Sci Total Environ, 2017, 579: 646-656 CrossRef PubMed ADS Google Scholar

[47] Lapota D, Galt C, Losee J R, Huddell H D, Orzech J K, Nealson K H. Observations and measurements of planktonic bioluminescence in and around a milky sea. J Exp Mar Biol Ecol, 1988, 119: 55-81 CrossRef Google Scholar

[48] Lehmann K B, Neumann R. 1896. Atlas und Grundriss der Bakteriologie und Lehrbuch der speziellen bakteriologischen Diagnostik. 1st ed. J F Lehmann, München. Google Scholar

[49] Li X, Roseman S. The chitinolytic cascade in Vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/kinase. Proc Natl Acad Sci USA, 2004, 101: 627-631 CrossRef ADS Google Scholar

[50] Li S, Wang L, Hao J, Xing M, Sun J, Sun M. Purification and characterization of a new alginate lyase from marine bacterium Vibrio sp. SY08. Mar Drugs, 2016, 15: 1 CrossRef PubMed Google 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. Cloning, expression, and characterization of a new β-Agarase from Vibrio sp. strain CN41. Appl Environ Microbiol, 2011, 77: 7077-7079 CrossRef PubMed Google Scholar

[52] Lin H, Yu M, Wang X, Zhang X H. Comparative genomic analysis reveals the evolution and environmental adaptation strategies of vibrios. BMC Genomics, 2018, 19: 135 CrossRef PubMed Google Scholar

[53] Liu Z, Liu J. 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, 2013, 2: 492-504 CrossRef PubMed Google Scholar

[54] Lukjancenko O, Ussery D W. Vibrio chromosome-specific families. Front Microbiol, 2014, 5: 73 CrossRef Google Scholar

[55] Main C R, Salvitti L R, Whereat E B, Coyne K J. Community-level and species-specific associations between phytoplankton and particle-associated Vibrio species in Delaware’s Inland Bays. Appl Environ Microbiol, 2015, 81: 5703-5713 CrossRef PubMed Google Scholar

[56] Martínez A, Ventouras L A, Wilson S T, Karl D M, DeLong E F. Metatranscriptomic and functional metagenomic analysis of methylphosphonate utilization by marine bacteria. Front Microbiol, 2013, 4 CrossRef Google Scholar

[57] Machado H, Gram L. The fur gene as a new phylogenetic marker for Vibrionaceae species identification. Appl Environ Microbiol, 2015, 81: 2745-2752 CrossRef PubMed Google Scholar

[58] Miller S D, Haddock S H D, Elvidge C D, Lee T F. Detection of a bioluminescent milky sea from space. Proc Natl Acad Sci USA, 2005, 102: 14181-14184 CrossRef PubMed ADS Google Scholar

[59] Oberbeckmann S, Fuchs B M, Meiners M, Wichels A, Wiltshire K H, Gerdts G. Seasonal dynamics and modeling of a Vibrio community in coastal waters of the North Sea. Microb Ecol, 2012, 63: 543-551 CrossRef PubMed Google Scholar

[60] Oliver J D. Recent findings on the viable but nonculturable state in pathogenic bacteria. Fems Microbiol Rev, 2010, 34: 415-425 CrossRef PubMed Google Scholar

[61] Øvreås L, Bourne D, Sandaa R, Casamayor E, Benlloch S, Goddard V, Smerdon G, Heldal M, Thingstad T. Response of bacterial and viral communities to nutrient manipulations in seawater mesocosms. Aquat Microb Ecol, 2003, 31: 109-121 CrossRef Google Scholar

[62] Pascual J, Macián M C, Arahal D R, Garay E, Pujalte M J. 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, 2010, 60: 154-165 CrossRef PubMed Google Scholar

[63] Phillips K E, Satchell K J F. Vibrio vulnificus: From oyster colonist to human pathogen. PLoS Pathog, 2017, 13: e1006053 CrossRef PubMed Google Scholar

[64] Rizzo L, Fraschetti S, Alifano P, Tredici M S, Stabili L. Association of Vibrio community with the Atlantic Mediterranean invasive alga Caulerpa cylindracea. J Exp Mar Biol Ecol, 2016, 475: 129-136 CrossRef Google Scholar

[65] Rubio-Portillo E, Gago J F, Martínez-García M, Vezzulli L, Rosselló-Móra R, Antón J, Ramos-Esplá A A. Vibrio communities in scleractinian corals differ according to health status and geographic location in the Mediterranean Sea. Syst Appl Microbiol, 2018, 41: 131-138 CrossRef PubMed Google Scholar

[66] Rubio-Portillo E, Yarza P, Peñalver C, Ramos-Esplá A A, Antón J. New insights into Oculina patagonica coral diseases and their associated Vibrio spp. communities. ISME J, 2014, 8: 1794-1807 CrossRef PubMed Google 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. Complete genome sequence of Vibrio fischeri: A symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci USA, 2005, 102: 3004-3009 CrossRef PubMed ADS Google 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: 161–188. Google Scholar

[69] Siboni N, Balaraju V, Carney R, Labbate M, Seymour J R. Spatiotemporal dynamics of Vibrio spp. within the Sydney harbour estuary. Front Microbiol, 2016, 7: 460 CrossRef Google Scholar

[70] Simu K, Hagström A. Oligotrophic bacterioplankton with a novel single-cell life strategy. Appl Environ Microbiol, 2004, 70: 2445-2451 CrossRef Google 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. Distribution of multiple antibiotic resistant Vibrio spp. across Palk Bay. Region Stud Mar Sci, 2016, 3: 242-250 CrossRef Google 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: 3750–3756. Google Scholar

[73] Suginta W, Chuenark D, Mizuhara M, Fukamizo T. Novel β-N-acetylglucosaminidases from Vibrio harveyi 650: Cloning, expression, enzymatic properties, and subsite identification. BMC Biochem, 2010, 11: 40 CrossRef PubMed Google Scholar

[74] Suginta W, Vongsuwan A, Songsiriritthigul C, Prinz H, Estibeiro P, Duncan R R, Svasti J, Fothergill-Gilmore L A. An endochitinase A from Vibrio carchariae: Cloning, expression, mass and sequence analyses, and chitin hydrolysis. Archives Biochem Biophys, 2004, 424: 171-180 CrossRef PubMed Google 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: 408–413. Google Scholar

[76] Takemura A F, Chien D M, Polz M F. Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level. Front Microbiol, 2014, 5: 38 CrossRef Google Scholar

[77] Tall A, Hervio-Heath D, Teillon A, Boisset-Helbert C, Delesmont R, Bodilis J, Touron-Bodilis A. Diversity of Vibrio spp. isolated at ambient environmental temperature in the Eastern English Channel as determined by pyrH sequencing. J Appl Microbiol, 2013, 114: 1713-1724 CrossRef PubMed Google Scholar

[78] Tanaka M, Umemoto Y, Okamura H, Nakano D, Tamaru Y, Araki T. 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, 2009, 73: 109-116 CrossRef PubMed Google Scholar

[79] Thompson F L, Austin B, Swings J. 2006. The Biology of Vibrios. Washington D C: American Society for Microbiology. Google Scholar

[80] Thompson F L, Gevers D, Thompson C C, Dawyndt P, Naser S, Hoste B, Munn C B, Swings J. Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis. Appl Environ Microbiol, 2005, 71: 5107-5115 CrossRef PubMed Google 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. 190–203. Google Scholar

[82] Thompson J R, Randa M A, Marcelino L A, Tomita-Mitchell A, Lim E, Polz M F. Diversity and dynamics of a north atlantic coastal Vibrio community. Appl Environ Microbiol, 2004, 70: 4103-4110 CrossRef PubMed Google Scholar

[83] Turner J W, Good B, Cole D, Lipp E K. Plankton composition and environmental factors contribute to Vibrio seasonality. ISME J, 2009, 3: 1082-1092 CrossRef PubMed Google Scholar

[84] Thurber R V, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards R A, Angly F, Dinsdale E, Kelly L, Rohwer F. Metagenomic analysis of stressed coral holobionts. Environ Microbiol, 2009, 11: 2148-2163 CrossRef PubMed Google Scholar

[85] Vezzulli L, Brettar I, Pezzati E, Reid P C, Colwell R R, Höfle M G, Pruzzo C. Long-term effects of ocean warming on the prokaryotic community: Evidence from the vibrios. ISME J, 2012, 6: 21-30 CrossRef PubMed Google Scholar

[86] Vezzulli L, Grande C, Reid P C, Hélaouët P, Edwards M, Höfle M G, Brettar I, Colwell R R, Pruzzo C. Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic. Proc Natl Acad Sci USA, 2016, 113: E5062-E5071 CrossRef PubMed Google 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. Whole-genome enrichment provides deep insights into Vibrio cholerae Metagenome from an African River. Microb Ecol, 2017, 73: 734-738 CrossRef PubMed Google Scholar

[88] Vezzulli L, Pezzati E, Moreno M, Fabiano M, Pane L, Pruzzo C, Pruzzo C. Benthic ecology of Vibrio spp. and pathogenic Vibrio species in a coastal Mediterranean environment (La Spezia Gulf, Italy). Microb Ecol, 2009, 58: 808-818 CrossRef PubMed Google 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: 568–573. Google Scholar

[90] Wang Y, Zhang X H, Yu M, Wang H, Austin B. Vibrio atypicus sp. nov., isolated from the digestive tract of the Chinese prawn (Penaeus chinensis O’sbeck). Int J Syst Evol Microbiol, 2010, 60: 2517-2523 CrossRef PubMed Google 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. A novel Vibrio beta-glucosidase (LamN) that hydrolyzes the algal storage polysaccharide laminarin. Fems Microbiol Ecol, 2015, 91: fiv087 CrossRef PubMed Google 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: 988–993. Google Scholar

[93] Westrich J R, Ebling A M, Landing W M, Joyner J L, Kemp K M, Griffin D W, Lipp E K. Saharan dust nutrients promote Vibrio bloom formation in marine surface waters. Proc Natl Acad Sci USA, 2016, 113: 5964-5969 CrossRef PubMed ADS Google Scholar

[94] Xu H S, Roberts N, Singleton F L, Attwell R W, Grimes D J, Colwell R R. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb Ecol, 1982, 8: 313-323 CrossRef PubMed Google Scholar

[95] Zhang W, Sun L. Cloning, characterization, and molecular application of a beta-agarase gene from Vibrio sp. strain V134. Appl Environ Microbiol, 2007, 73: 2825-2831 CrossRef PubMed Google Scholar

[96] Zhu B, Tan H, Qin Y, Xu Q, Du Y, Yin H. Characterization of a new endo-type alginate lyase from Vibrio sp. W13. Int J Biol Macromol, 2015, 75: 330-337 CrossRef PubMed Google Scholar

[97] Zhu B, Sun Y, Ni F, Ning L, Yao Z. Characterization of a new endo-type alginate lyase from Vibrio sp. NJU-03. Int J Biol Macromol, 2018, 108: 1140-1147 CrossRef PubMed Google Scholar

  • Figure 1

    Abundance of Vibrio spp. in different marine environments. Orange colour circles, by culture-based methods; green and dark green (unpublished data from our laboratory) colour circles, by culture-independent methods.

  • Figure 2

    Phylogenetic tree of 115 Vibrio species. Neighbor-Joining phylogeny were reconstructed based on 16S rRNA gene sequences of the type strain of each species. The tree was rooted using Shewanella denitrificans OS217T as an outgroup. The branches were estimated from 1000 bootstrap replicates, and circles at internal nodes indicate bootstrap support greater than 50%; larger circles indicate greater bootstrap values.

  • Figure 3

    Potential action mode of Vibrio species in marine organic carbon cycling. T, temperature; S, salinity; P, phosphate; N, nitrogen salt; Si, silicate; E, extracellular enzyme; POC, particulate organic carbon; DOC, dissolved organic carbon.

  • Table 1   Organic carbon substrates of spp.

    Category of organic carbon

    Specific organic carbon source*

    Polysaccharides

    Chitin, alginic acid, agar, laminarin, starch, xylan, fucoidan, mannan, cellulose and pectin

    Disaccharides

    Maltose, cellobiose, lactose, salicin, trehalose, sucrose and esculin

    Monosaccharides

    D-glucose, D-mannitol, D-fructose, D-galactose, α-D-fucose, L-arabinose, D-arabitol, D-galacturonate, D-mannitol, D-mannose, L-sorbitol, D-xylose, and myo-inositol

    Small compounds

    Glycerol, ethanol, and acetate

    Other compounds

    Polyhydroxyl alcohol, lipid, lecithin, gelatin, casein, DNA, mucin, and hydrocarbon (alkane and aromatic hydrocarbon)

    * extracted from Farmer et al. (2005); not all Vibrio cultures utilize all the organic carbons in this list

  • Table 2   Representative extracellular hydrolytic enzymes identified from spp.

    Bacterial taxon

    Enzyme and family

    Accession number

    Product

    Reference

    Vibrio sp. V134

    β-Agarase AgaV, GH16

    ABL06969

    NA4, NA6

    Zhang and Sun, 2007

    Vibrio sp. PO-303

    β-Agarase AgaB, GH50

    BAG71427

    NA2

    Araki et al., 1998

    Vibrio sp. PO-303

    β-Agarase AgaC, GH118

    BAF03590

    NA4, NA6, NA8

    Dong et al., 2006

    Vibrio sp. JT0107

    β-Agarase AgaA, GH86

    BAA03541

    NA2

    Sugano et al., 1993

    Vibrio sp. PO-303

    β-Agarase AgaD, GH16

    BAF34350

    NA2, NA

    Dong et al., 2007

    Vibrio sp. F-6

    Agarase AG-a, GH50

    EU699809

    NA4, NA6

    Fu et al., 2008

    Vibrio sp. CN41

    β-Agarase AgaACN4, GH50

    HM563685

    DP4, DP6, DP8

    Liao et al., 2011

    V. campbellii HY01

    β-glucosidase (laminarinase) LamN, GH3

    EDL69935

    Glucose

    Wang et al., 2015

    Vibrio sp. G21

    endo-β-1,4-glucanase Cel5A, GH5

    ADJ93836

    cellobiose

    Gao et al., 2010

    Vibrio sp. MA-138

    β-1,4-mannanase Man5C, GH5

    BAG69482

    M1-5

    Tanaka et al., 2009

    V. parahaemolyticus KN1699

    chitinase Pa-Chi, GH18

    BAF91600

    (GlcNAc)2

    Kadokura et al., 2007

    V. cholerae E1

    chitinase ChiA, GH18

    AAC72236

    GlcNAc

    Connell et al., 1998

    V. harveyi BB7

    chitinase ChiA, GH18

    AAC46383

    (GlcNAc)2-6

    Svitil et al., 1997

    V. proteolyticus 442

    chitinase ChiA, GH18

    BAF76068

    (GlcNAc)2

    Itoi et al., 2007

    V. proteolyticus NBRC 13287

    chitinase (reducing end-specific), GH19

    BAE86996

    (GlcNAc)2

    Honda et al., 2008

    V. furnissii NCTC 11218

    chitodextrinase EndoI, GH18

    AAC44673

    (GlcNAc)2, (GlcNAc)3

    Keyhani and Roseman, 1996

    V. harveyi 650

    β-N-acetylglucosaminidases, GH20

    HM175716

    GlcNAc

    Suginta et al., 2010

    V. carchariae (=V. harveyi) LMG7890T

    endochitinase A, GH18

    Q9AMP1

    (GlcNAc)2

    Suginta et al., 2004

    Vibrio sp. AX-4

    β-1,3-xylanase Xyl4, GH26

    BAD51934

    X1-3

    Kiyohara et al., 2005

    Vibrio sp. XY-214

    endo-1,3-β-xylanase TxyA, GH26

    BAA94698

    xylooligosaccharides

    Araki et al., 2000

    Vibrio sp. W13

    alginate lyase Algb, PL7

    KC777293

    DP2-5

    Zhu et al., 2015

    V. algivorus sp. SA2T

    polysaccharide-decomposing enzyme AlyB, PL7

    NC_007088.5

    L-Lysine

    Doi et al., 2017

    Vibrio sp. SY08

    alginate lyase AlySY08, PL7

    KY214288

    UADs

    Li et al., 2016

    Vibrio sp. NJU-03

    alginate lyase AlgNJU-03, PL7

    GAK20697.1

    DP2-4

    Zhu et al., 2018

    Vibrio. sp. QD-5

    alginate lyase Aly-IV, PL7

    PRJNA382465

    DP1-3

    Chao et al., 2017

    GH, glycosidic hydrolase; NA2, neoagarobiose; NA4, neoagarotetraose; NA6, neoagarohexaose; NA8, neoagarohexaose; GlcNAc, β-d-N-acetylglucosaminyl; M1-5: mannose, mannobiose, mannotriose, mannotetraose, and mannopentaose; X1-3: xylobiose, xylotriose and xylotetraose; PL: polysaccharide lyase family; DP: oligosaccharides with low degree of polymerization; UAD: unsaturated alginate disaccharides