Abstract
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.
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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: 357–365
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: 1185
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
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: 1741–1743
Arnosti C. 2014. Patterns of microbially driven carbon cycling in the ocean: Links between extracellular enzymes and microbial communities. Adv Oceanogr, 2014: 1–12
Austin B, Zhang X H. 2006. Vibrio harveyi: A significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol, 43: 119–124
Baker-Austin C, Trinanes J, Gonzalez-Escalona N, Martinez-Urtaza J. 2017. Non-cholera Vibrios: The microbial barometer of climate change. Trends Microbiol, 25: 76–84
Azam F, Malfatti F. 2007. Microbial structuring of marine ecosystems. Nat Rev Microbiol, 5: 782–791
Beijerinck M W. 1889. Le Photobacterium luminosum, bactérie lumineuse de la Mer du Nord. Archives Néerlandaises des Sciences Exactes et Naturelles, 23: 401–427
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
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: 7263–7270
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
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
Chi W J, Chang Y K, Hong S K. 2012. Agar degradation by microorganisms and agar-degrading enzymes. Appl Microbiol Biotechnol, 94: 917–930
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: 2272
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
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: e01147–17
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: 3164–3169
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: 1581–1592
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: 6399–6401
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: 38–46
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: 3044–3051
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: 6004–6011
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
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: 477–479
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: 915–922
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
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: 1373–1382
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: 1958–1962
Gilbert J A, Dupont C L. 2011. Microbial metagenomics: Beyond the genome. Annu Rev Mar Sci, 3: 347–371
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: 298–308
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: 210–218
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
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: 447–460
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: 350–357
Hamdan L, Fulmer P. 2011. Effects of COREXIT® EC9500A on bacteria from a beach oiled by the Deepwater Horizon spill. Aquat Microb Ecol, 63: 101–109
Hickey M E, Lee J L. 2017. A comprehensive review of Vibrio (Listonella) anguillarum: Ecology, pathology and prevention. Rev Aquacult, 161
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: 627–634
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: 1099–1107
Joseph S W, Colwell R R, Kaper J B. 1982. Vibrio Parahaemolyticus and related halophilic vibrios. Crit Rev Microbiol, 10: 77–124
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: 357–365
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: 118–122
Keyhani N O, Roseman S. 1996. The chitin catabolic cascade in the Marine Bacterium Vibrio furnissii. J Biol Chem, 271: 33414–33424
Kirchman D, White J. 1999. Hydrolysis and mineralization of chitin in the Delaware Estuary. Aquat Microb Ecol, 18: 187–196
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: 949–957
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: 646–656
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: 55–81
Lehmann K B, Neumann R. 1896. Atlas und Grundriss der Bakteriologie und Lehrbuch der speziellen bakteriologischen Diagnostik. 1st ed. J F Lehmann,München
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: 627–631
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: 1
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: 7077–7079
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: 135
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: 492–504
Lukjancenko O, Ussery D W. 2014. Vibrio chromosome-specific families. Front Microbiol, 5: 73
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: 5703–5713
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, 4
Machado H, Gram L. 2015. The fur gene as a new phylogenetic marker for Vibrionaceae species identification. Appl Environ Microbiol, 81: 2745–2752
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: 14181–14184
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: 543–551
Oliver J D. 2010. Recent findings on the viable but nonculturable state in pathogenic bacteria. Fems Microbiol Rev, 34: 415–425
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: 109–121
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: 154–165
Phillips K E, Satchell K J F. 2017. Vibrio vulnificus: From oyster colonist to human pathogen. PLoS Pathog, 13: e1006053
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: 129–136
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: 131–138
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: 1794–1807
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: 3004–3009
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
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: 460
Simu K, Hagström A. 2004. Oligotrophic bacterioplankton with a novel single-cell life strategy. Appl Environ Microbiol, 70: 2445–2451
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: 242–250
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
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: 40
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: 171–180
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
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: 38
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: 1713–1724
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: 109–116
Thompson F L, Austin B, Swings J. 2006. The Biology of Vibrios. Washington D C: American Society for Microbiology
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: 5107–5115
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
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: 4103–4110
Turner J W, Good B, Cole D, Lipp E K. 2009. Plankton composition and environmental factors contribute to Vibrio seasonality. ISME J, 3: 1082–1092
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: 2148–2163
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: 21–30
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–E5071
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: 734–738
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: 808–818
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
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: 2517–2523
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: fiv087
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
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: 5964–5969
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: 313–323
Zhang W, Sun L. 2007. Cloning, characterization, and molecular application of a beta-agarase gene from Vibrio sp. strain V134. Appl Environ Microbiol, 73: 2825–2831
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: 330–337
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: 1140–1147
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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).
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Zhang, X., Lin, H., Wang, X. et al. Significance of Vibrio species in the marine organic carbon cycle—A review. Sci. China Earth Sci. 61, 1357–1368 (2018). https://doi.org/10.1007/s11430-017-9229-x
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DOI: https://doi.org/10.1007/s11430-017-9229-x