Molecular analyses of bacterioplankton communities with highly abundant <i>Vibrio</i> clades: a case study in Bohai Sea coastal waters -- Journal of Oceanology and Limnology,2019,37(5):1638-1648

	Cite this paper:
	WANG Shuping, ZHANG Yuan, HE Jia, JIA Xiaobo, LIN Jianing, LI Meng, WANG Qinglin. Molecular analyses of bacterioplankton communities with highly abundant Vibrio clades: a case study in Bohai Sea coastal waters[J]. Journal of Oceanology and Limnology, 2019, 37(5): 1638-1648

Molecular analyses of bacterioplankton communities with highly abundant Vibrio clades: a case study in Bohai Sea coastal waters

WANG Shuping¹, ZHANG Yuan¹, HE Jia¹, JIA Xiaobo¹, LIN Jianing¹, LI Meng², WANG Qinglin³

1 State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China;
2 Institute for Advanced Study, Shenzhen University, Shenzhen 518000, China;
3 College of Animal Science and Technology, Hebei Normal University of Science and Technology, Qinhuangdao 066000, China

Abstract:

We investigated the bacterioplankton abundance, community composition and the associated Vibrio clades of natural seawater in Bohai Sea coastal waters. Seawater samples (10 L in triplicate) were collected at 0.5, 3, and 5 m depths near the coastal aquaculture zone of the Bohai Sea on May 12, 2016. Real-time PCR and 16S rRNA gene amplicon high-throughput sequencing methods were employed by which 485 operational taxonomic units (OTUs) at a 97% sequence similarity level were generated. Gammaproteobacteria, Alphaproteobacteria, and Bacteroidetes were the most abundant groups, accounting for 49.5%, 23.5%, and 18.9% of the total assemblage, respectively. Obvious variations in Pseudoalteromonas, Vibrio, and Octadecabacter, which were the most abundant genera, could be observed among different samples. Notably, the results of Vibrio-specific real-time PCR indicated that Vibrio had extremely high 16S rRNA gene copy numbers. The 16S rRNA gene sequencing results across all the samples also indicated that they occupied a large proportion of the total assemblage. Both the alpha diversity and major bacterioplankton group Pseudoalteromonas had significant correlations with the concentration of PO₄^3-. Overall, studies on bacterioplankton communities with highly abundant Vibrio clades can provide interesting insight into the microbial function and health assessment of the Bohai Sea coastal ecosystem.

Key words: Bohai Sea|bacterioplankton|Vibrio|16S rRNA|Illumina MiSeq

Received: 2018-08-19 Revised: 2018-12-13

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References:
Abell G C J, Bowman J P. 2005. Ecological and biogeographic relationships of class Flavobacteria in the Southern Ocean. FEMS Microbiology Ecology, 51(2):265-277.
Acinas S G, Marcelino L A, Klepac-Ceraj V, Polz M F. 2004.Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. Journal of Bacteriology, 186(9):2 629-2 635.
Bowman J P. 2007. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Marine Drugs, 5(4):220-241.
Brinkhoff T, Giebel H A, Simon M. 2008. Diversity, ecology, and genomics of the Roseobacter clade:a short overview.Archives of Microbiology, 189(6):531-539.
Campbell A M, Fleisher J, Sinigalliano C, White J R, Lopez J V. 2015. Dynamics of marine bacterial community diversity of the coastal waters of the reefs, inlets, and wastewater outfalls of southeast Florida. Microbiology Open, 4(3):390-408.
Canfora L, Bacci G, Pinzari F, Lo Papa G, Dazzi C, Benedetti A. 2014. Salinity and bacterial diversity:to what extent does the concentration of salt affect the bacterial community in a saline soil? PLoS One, 9(9):e106662, https://doi.org/10.1371/journal.pone.0106662.
Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Peña A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge B D, Pirrung M, Reeder J, Sevinsky J R, Turnbaugh P J, Walters W A, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QⅡME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5):335-336.
Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Huntley J, Fierer N, Owens S M, Betley J, Fraser L, Bauer M, Gormley N, Gilbert J A, Smith G, Knight R. 2012.Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal, 6(8):1 621-1 624.
Cottrell M T, Kirchman D L. 2000. Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization.Applied and Environmental Microbiology, 66(12):5 116-5 122.
Dang H Y, Zhou H X, Zhang Z N, Yu Z S, Hua E, Liu X S, Jiao N Z. 2013. Molecular detection of Candidatus Scalindua pacifica and environmental responses of sediment anammox bacterial community in the Bohai Sea, China.PLoS One, 8(4):e61330.
DeLong E F, Franks D G, Alldredge A L. 1993. Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnology and Oceanography, 38(5):924-934.
DeLorenzo M E, Brooker J, Chung K W, Kelly M, Martinez J, Moore J G, Thomas M. 2016. Exposure of the grass shrimp, Palaemonetes pugio, to antimicrobial compounds affects associated Vibrio bacterial density and development of antibiotic resistance. Environmental Toxicology, 31(4):469-477.
Ding J J, Zhang Y G, Deng Y, Cong J, Lu H, Sun X, Yang C Y, Yuan T, Van Nostrand J D, Li D Q, Zhou J Z, Yang Y F. 2015. Integrated metagenomics and network analysis of soil microbial community of the forest timberline.Scientific Reports, 5:7 994.
Eiler A, Johansson M, Bertilsson S. 2006. Environmental influences on Vibrio populations in northern temperate and boreal coastal waters (Baltic and Skagerrak Seas).Applied and Environmental Microbiology, 72(9):6 004-6 011.
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. 2^nd edn. Springer, New York.p.494-546.
Fernández-Gómez B, Richter M, Schüler M, Pinhassi J, Acinas S G, González J M, Pedrós-Alió C. 2013. Ecology of marine Bacteroidetes:a comparative genomics approach.The ISME Journal, 7(5):1 026-1 037.
Fukami K, Simidu U, Taga N. 1985. Microbial decomposition of phyto-and zooplankton in seawater. I. Changes in organic matter. Marine Ecology Progress Series, 21:1-5.
Gao X L, Zhou F X, Chen C T A. 2014. Pollution status of the Bohai Sea:an overview of the environmental quality assessment related trace metals. Environment International, 62:12-30.
Ghosh A, Bhadury P. 2018. Exploring biogeographic patterns of bacterioplankton communities across global estuaries.MicrobiologyOpen, e741, https://doi.org/10.1002/mbo3.741.
Gifford S M, Sharma S, Moran M A. 2014. Linking activity and function to ecosystem dynamics in a coastal bacterioplankton community. Frontiers in Microbiology, 5:185.
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. The ISME Journal, 6(2):298-308.
Goodwin K D, Thompson L R, Duarte B, Kahlke T, Thompson A R, Marques J C, Caçador I. 2017. DNA sequencing as a tool to monitor marine ecological status. Frontiers in Marine Science, 4:107.
Gosink J J, Herwig R P, Staley J T. 1997. Octadecabacter arcticus gen. nov., sp. nov., and O. antarcticus, sp. nov., nonpigmented, psychrophilic gas vacuolate bacteria from polar sea ice and water. Systematic and Applied Microbiology, 20(3):356-365.
Grimes D J, Johnson C N, Dillon K S, Flowers A R, Noriea Ⅲ N F, Berutti T. 2009. What genomic sequence information has revealed about Vibrio ecology in the ocean-a review.Microbial Ecology, 58(3):447-460.
Grimes D J, Singleton F L, Colwell R R. 1984. Allogenic succession of marine bacterial communities in response to pharmaceutical waste. Journal of Applied Microbiology, 57(2):247-261.
Hoffmann M, Fischer M, Ottesen A, McCarthy P J, Lopez J V, Brown E W, Monday S R. 2010. Population dynamics of Vibrio spp. associated with marine sponge microcosms.The ISME Journal, 4(12):1 608-1 612.
Lin X P, Xie S P, Chen X P, Xu L L. 2006. A well-mixed warm water column in the central Bohai Sea in summer:effects of tidal and surface wave mixing. Journal of Geophysical Research:Oceans, 111(C11):C11017, https://doi.org/10.1029/2006JC003504.
Lydon K A, Glinski D A, Westrich J R, Henderson W M, Lipp E K. 2017. Effects of triclosan on bacterial community composition and Vibrio populations in natural seawater microcosms. Elementa:Science of the Anthropocene, 5:22.
McArthur J V. 2006. Microbial Ecology:An Evolutionary Approach. Elsevier, Amsterdam. 432p.
Oberbeckmann S, Wichels A, Maier T, Kostrzewa M, Raffelberg S, Gerdts G. 2011. A polyphasic approach for the differentiation of environmental Vibrio isolates from temperate waters. FEMS Microbiology Ecology, 75(1):145-162.
Paillard C, Le Roux F, Borrego J J. 2004. Bacterial disease in marine bivalves, a review of recent studies:trends and evolution. Aquatic Living Resources, 17(4):477-498.
Peng Z Q, Zhuang Z X, Huang R F, Lu Z Q. 2010. Distribution of pathogen in the Bohai sea in spring and summer.African Journal of Microbiology Research, 4(13):1 383-1 390.
Pruzzo C, Gallo G, Canesi L. 2005. Persistence of vibrios in marine bivalves:the role of interactions with haemolymph components. Environmental Microbiology, 7(6):761-772.
Rotini A, Manfra L, Spanu F, Pisapia M, Cicero A M, Migliore L. 2017. Ecotoxicological method with marine bacteria Vibrio anguillarum to evaluate the acute toxicity of environmental contaminants. Journal of Visualized Experiments, (123):e55211.
Shendure J, Ji H. 2008. Next-generation DNA sequencing.Nature Biotechnology, 26(10):1 135-1 145.
Sinkko H, Lukkari K, Jama A S, Sihvonen L M, Sivonen K, Leivuori M, Rantanen M, Paulin L, Lyra C. 2011.Phosphorus chemistry and bacterial community composition interact in brackish sediments receiving agricultural discharges. PLoS One, 6(6):e21555, https://doi.org/10.1371/journal.pone.0021555.
Stackebrandt E, Goebel B M. 1994. Taxonomic note:a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology.International Journal of Systematic and Evolutionary Microbiology, 44(4):846-849.
Stackebrandt E, Goodfellow M. 1991. Nucleic acid Techniques in Bacterial Systematics. Wiley, New York. 329p.
Sun Y H, De Vos P, Heylen K. 2016. Nitrous oxide emission by the non-denitrifying, nitrate ammonifier Bacillus licheniformis. BMC Genomics, 17:68.
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. Frontiers in Microbiology, 5:38.
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. ASM Press, Washington, DC. p.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. Applied and Environmental Microbiology, 70(7):4 103-4 110.
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.Proceedings of the National Academy of Sciences of the United States of America, 113(34):E5 062-E5 071.
Vollmers J, Voget S, Dietrich S, Gollnow K, Smits M, Meyer K, Brinkhoff T, Simon M, Daniel R. 2013. Poles apart:Arctic and Antarctic Octadecabacter strains share high genome plasticity and a new type of Xanthorhodopsin.PLoS One, 8(5):e63422, https://doi.org/10.1371/journal.pone.0063422.
Wear E K, Wilbanks E G, Nelson C E, Carlson C A. 2018.Primer selection impacts specific population abundances but not community dynamics in a monthly time-series 16S rRNA gene amplicon analysis of coastal marine bacterioplankton. Environmental Microbiology, 20(8):2 709-2 726.
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.Proceedings of the National Academy of Sciences of the United States of America, 113(21):5 964-5 969.
Westrich J R, Griffin D W, Westphal D L, Lipp E K. 2018.Vibrio population dynamics in Mid-Atlantic surface waters during Saharan dust events. Frontiers in Marine Science, 5:12, https://doi.org/10.3389/fmars.2018.00012.
Williams T J, Wilkins D, Long E, Evans F, DeMaere M Z, Raftery M J, Cavicchioli R. 2013. The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environmental Microbiology, 15(5):1 302-1 317.
Worden A Z, Seidel M, Smriga S, Wick A, Malfatti F, Bartlett D, Azam F. 2006. Trophic regulation of Vibrio cholerae in coastal marine waters. Environmental Microbiology, 8(1):21-29.
Wu Z X, Yu Z M, Song X X, Yuan Y Q, Cao X H, Liang Y B. 2013. Application of an integrated methodology for eutrophication assessment:a case study in the Bohai Sea.Chinese Journal of Oceanology and Limnology, 31(5):1 064-1 078.
Yang C Y, Li Y, Zhou B, Zhou Y Y, Zheng W, Tian Y, Van Nostrand J D, Wu L Y, He Z L, Zhou J Z, Zheng T L. 2015. Illumina sequencing-based analysis of free-living bacterial community dynamics during an Akashiwo sanguine bloom in Xiamen sea, China. Scientific Reports, 5:8476.
Yilmaz P, Parfrey L W, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glöckner F O. 2014. The SILVA and "All-species Living Tree Project (LTP)" taxonomic frameworks. Nucleic Acids Research, 42(D1):D643-D648.
Yu S X, Pang Y L, Wang Y C, Li J L, Qin S. 2018. Distribution of bacterial communities along the spatial and environmental gradients from Bohai Sea to northern Yellow Sea. PeerJ, 6:e4272, https://doi.org/10.7717/peerj.4272.
Zhang X H, Lin H Y, Wang X L, Austin B. 2018. Significance of Vibrio species in the marine organic carbon cycle-a review. Science China Earth Sciences, 61(10):1 357-1 368.
Zhang Y Q, Lin X, Shi X G, Lin L X, Luo H, Li L, Lin S J. 2019. Metatranscriptomic signatures associated with phytoplankton regime shift from diatom dominance to a dinoflagellate bloom. Frontiers in Microbiology, 10:590.
Zhao H P, Tao J H, Li Q X, Yuan D K, Gao Q C. 2013.Microbial ecological characteristics in the Red TideMonitoring area of Bohai Bay. Journal of Hydroenvironment Research, 7(2):141-151.