Cite this paper:
HE Jiaying, WANG Kai, XIONG Jinbo, GUO Annan, ZHANG Demin, FEI Yuejun, YE Xiansen. Drivers of coastal bacterioplankton community diversity and structure along a nutrient gradient in the East China Sea[J]. Journal of Oceanology and Limnology, 2018, 36(2): 329-340

Drivers of coastal bacterioplankton community diversity and structure along a nutrient gradient in the East China Sea

HE Jiaying1,2, WANG Kai1,2, XIONG Jinbo1,2, GUO Annan1, ZHANG Demin1,2, FEI Yuejun3, YE Xiansen3
1 School of Marine Sciences, Ningbo University, Ningbo 315211, China;
2 Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture, Ningbo 315200, China;
3 Marine Environmental Monitoring Center of Ningbo, State Oceanic Administration(SOA), Ningbo 315211, China
Abstract:
Anthropogenic nutrient discharge poses widespread threats to coastal ecosystems and has increased environmental gradients from coast to sea. Bacterioplankton play crucial roles in coastal biogeochemical cycling, and a variety of factors affect bacterial community diversity and structure. We used 16S rRNA gene pyrosequencing to investigate the spatial variation in bacterial community composition (BCC) across five sites on a coast-offshore gradient in the East China Sea. Overall, bacterial alpha-diversity did not differ across sites, except that richness and phylogenetic diversity were lower in the offshore sites, and the highest alpha-diversity was found in the most landward site, with Chl-a being the main factor. BCCs generally clustered into coastal and offshore groups. Chl-a explained 12.3% of the variation in BCCs, more than that explained by either the physicochemical (5.7%) or spatial (8.5%) variables. Nutrients (particularly nitrate and phosphate), along with phytoplankton abundance, were more important than other physicochemical factors, co-explaining 20.0% of the variation in BCCs. Additionally, a series of discriminant families (primarily affiliated with Gammaproteobacteria and Alphaproteobacteria), whose relative abundances correlated with Chl-a, DIN, and phosphate concentrations, were identified, implying their potential to indicate phytoplankton blooms and nutrient enrichment in this marine ecosystem. This study provides insight into bacterioplankton response patterns along a coast-offshore gradient, with phytoplankton abundance increasing in the offshore sites. Time-series sampling across multiple transects should be performed to determine the seasonal and spatial patterns in bacterial diversity and community structure along this gradient.
Key words:    bacterioplankton|pyrosequencing|nutrient gradient|phytoplankton abundance|dominant factor|bioindicator   
Received: 2016-04-17   Revised:
Tools
PDF (539 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by HE Jiaying
Articles by WANG Kai
Articles by XIONG Jinbo
Articles by GUO Annan
Articles by ZHANG Demin
Articles by FEI Yuejun
Articles by YE Xiansen
References:
Abed R M M, Al-Kindi S, Al-Kharusi S. 2015. Diversity of bacterial communities along a petroleum contamination gradient in desert soils. Microb. Ecol., 69(1):95-105.
Adams H E, Crump B C, Kling G W. 2014. Metacommunity dynamics of bacteria in an arctic lake:the impact of species sorting and mass effects on bacterial production and biogeography. Front. Microbiol., 5:82.
Alonso C, Warnecke F, Amann R, Pernthaler J. 2007. High local and global diversity of Flavobacteria in marine plankton. Environ. Mivrobiol., 9(5):1 253-1 266.
Anderson M J. 2004. DISTLM v.5:A FORTRAN Computer Program to Calculate A Distance-Based Multivariate Analysis for A Linear Model. Department of Statistics, University of Auckland, New Zealand. 10p.
Barberán A, Casamayor E O. 2010. Global phylogenetic community structure and β-diversity patterns in surface bacterioplankton metacommunities. Aquat. Microb. Ecol., 59(1):1-10.
Baumann B, Snozzi M, Zehnder A J B, Van Meer J R D. 1996.Dynamics of denitrification activity of Paracoccus denitrificans in continuous culture during aerobicanaerobic changes. J. Bacteriol., 178(15):4 367-4 374.
Behrenfeld M J, Boss E, Siegel D A, Shea D M. 2005. Carbonbased ocean productivity and phytoplankton physiology from space. Global Biogeochem. Cycles, 19(1):GB1006.
Behrenfeld M J, O'Malley R T, Siegel D A, McClain C R, Sarmiento J L, Feldman G C, Milligan A J, Falkowski P G, Letelier R M, Boss E S. 2006. Climate-driven trends in contemporary ocean productivity. Nature, 444(7120):752-755.
Bryant D A, Frigaard N U. 2006. Prokaryotic photosynthesis and phototrophy illuminated. Trends Micribiol., 14(11):488-496.
Buchan A, LeCleir G R, Gulvik C A, González J M. 2014.Master recyclers:features and functions of bacteria associated with phytoplankton blooms. Nat. Rev.Microbiol., 12(10):686-698.
Caporaso J G, Bittinger K, Bushman F D, DeSantis T Z, Andersen G L, Knight R. 2010a. PyNAST:a flexible tool for aligning sequences to a template alignment.Bioinformatics, 26(2):266-267.
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. 2010b. QⅡME allows analysis of high-throughput community sequencing data. Nat.Methods, 7(5):335-336.
Chase J M. 2007. Drought mediates the importance of stochastic community assembly. Proc. Natl. Acad. Sci.USA., 104(44):17 430-17 434.
Chen H P, Zhang H J, Xiong J B, Zhu J L, Zhu X Y, Zhou X Y, Zhang D M. 2016. Successional trajectories of bacterioplankton community over the complete cycle of a sudden phytoplankton bloom in the Xiangshan Bay, East China Sea. Environ. Pollut., 219:750-759, https://doi.org/10.1016/j.envpol.2016.07.035.
Chow C E T, Sachdeva R, Cram J A, Steele J A, Needham D M, Patel A, Parada A E, Fuhrman J A. 2013. Temporal variability and coherence of euphotic zone bacterial communities over a decade in the Southern California Bight. ISME J., 7(12):2 259-2 273.
Clarke K R, Gorley R N. Primer V5 (Plymouth routines in multivariate ecological research):user manual/tutorial[M]. Primer-E, 2001.
Cole J J. 1982. Interactions between bacteria and algae in aquatic ecosystems. Annu. Rev. Ecol. Evol. Syst., 13:291-314.
Cram J A, Chow C E T, Sachdeva R, Needham D M, Parada A E, Steele J A, Fuhrman J A. 2015. Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years. ISME J., 9(3):563-580.
Daufresne T, Lacroix G, Benhaim D, Loreau M. 2008.Coexistence of algae and bacteria:a test of the carbon hypothesis. Aquat. Microb. Ecol., 53(3):323-332.
De'ath G. 2002. Multivariate regression trees:a new technique for modeling species-environment relationships. Ecology, 83(4):1 105-1 117.
DeSantis T Z, Hugenholtz P, Larsen N, Rojas M, Brodie E L, Keller K, Huber T, Dalevi D, Hu P, Andersen G L. 2006.Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Aquat. Environ.Microbiol., 72(7):5 069-5 072.
Ducklow H W, Kirchman D L, Quinby H L, Carlson C A, Dam H G. 1993. Stocks and dynamics of bacterioplankton carbon during the spring bloom in the eastern north Atlantic Ocean. Deep Sea Res., Part Ⅱ Top. Studies Oceanogr., 40(1-2):245-263.
Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011.UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16):2 194-2 200.
Edgar R C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26(19):2 460-2 461.
El-Swais H, Dunn K A, Bielawski J P, Li W K W, Walsh D A. 2014. Seasonal assemblages and short-lived blooms in coastal north-west Atlantic Ocean bacterioplankton.Environ. Microbiol., 17(10):3 642-3 661.
Foesel B U, Drake H L, Schramm A. 2011. Defluviimonas denitrificans gen. nov., sp. nov., and Pararhodobacter aggregans gen. nov., sp. nov., non-phototrophic Rhodobacteraceae from the biofilter of a marine aquaculture. Syst. Appl. Microbiol., 34(7):498-502.
General Administration of Quality Supervision, Inspection and Quarantine of the People's Republic of China (AQSIQ), Standardization Administration of the People's Republic of China. GB 17378.4-2007 The specification for marine monitoring of China-Part 4:seawater analysis. China Standard Press, Beijing. 2007. (in Chinese)
Gilbert J A, Field D, Swift P, Newbold L, Oliver A, Smyth T, Somerfield P J, Huse S, Joint I. 2009. The seasonal structure of microbial communities in the Western English Channel. Environ. Microbiol., 11(12):3 132-3 139.
Glaeser S P, Kämpfer P. 2014. The family sphingomonadaceae.In:Rosenberg E, DeLong E F, Lory S, Stackebrandt E, Thompson F eds. The Prokaryotes. Springer, Berlin Heidelberg. p.641-707.
Griffith D A, Peres-Neto P R. 2006. Spatial modeling in ecology:the flexibility of eigenfunction spatial analyses.Ecology, 87(10):2 603-2 613.
Halpern B S, Walbridge S, Selkoe K A, Kappel C V, Micheli F, D'Agrosa C, Bruno J F, Casey K S, Ebert C, Fox H E, Fujita R, Heinemann D, Lenihan H S, Madin E M P, Perry M T, Selig E R, Spalding M, Steneck R, Watson R. 2008.A global map of human impact on marine ecosystems.Science, 319(5865):948-952.
Hansen M M, Olivieri I, Waller D M, Nielsen E E. 2012.Monitoring adaptive genetic responses to environmental change. Mol. Ecol., 21(6):1 311-1 312.
Hanson C A, Fuhrman J A, Horner-Devine M C, Martiny J B H. 2012. Beyond biogeographic patterns:processes shaping the microbial landscape. Nat. Rev. Microbiol., 10(7):497-506.
Herlemann D P R, Labrenz M, Jürgens K, Bertilsson S, Waniek J J, Andersson A F. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J., 5(10):1 571-1 579.
Howarth R, Chan F, Conley D J, Garnier J, Doney S C, Marino R, Billen G. 2011. Coupled biogeochemical cycles:eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front. Ecol. Environ., 9(1):18-26.
Hu A Y, Yang X Y, Chen N W, Hou L Y, Ma Y, Yu C P. 2014. Response of bacterial communities to environmental changes in a mesoscale subtropical watershed, Southeast China. Sci. Total. Environ., 472:746-756.
Huang W, Li B, Zhang C, Zhang Z Y, Lei Z F, Lu B, Zhou B B. 2015. Effect of algae growth on aerobic granulation and nutrients removal from synthetic wastewater by using sequencing batch reactors. Bioresour. Technol., 175:187-192.
Kuczynski J, Stombaugh J, Walters W A, González A, Caporaso J G, Knight R. 2012. Using QⅡME to analyze 16S rRNA gene sequences from microbial communities.Curr. Protoc. Bioinformatics., https://doi.org/10.1002/0471250953.bi1007s36.
Langenheder S, Ragnarsson H. 2007. The role of environmental and spatial factors for the composition of aquatic bacterial communities. Ecology, 88(9):2 154-2 161.
León M J, Sánchez-Porro C, de la Haba R R, Llamas I, Ventosa A. 2014. Larsenia salina gen. nov., sp. nov., a new member of the family Halomonadaceae based on multilocus sequence analysis. Syst. Appl. Microbiol., 37(7):480-487.
Li D J, Daler D. 2004. Ocean pollution from land-based sources:East China Sea, China. AMBIO., 33(1):107-113.
Li H M, Tang H J, Shi X Y, Zhang C S, Wang X L. 2014.Increased nutrient loads from the Changjiang (Yangtze)River have led to increased harmful algal blooms. Harmful Algae, 39:92-101.
Lomas M W, Bonachela J A, Levin S A, Martiny A C. 2014.Impact of ocean phytoplankton diversity on phosphate uptake. Proc. Natl. Acad. Sci. U. S. A., 111(49):17 540-17 545.
Lozupone C A, Knight R. 2007. Global patterns in bacterial diversity. Proc. Natl. Acad. Sci. U. S. A., 104(27):11 436-11 440.
Martiny J B, Eisen J A, Penn K, Allison S D, Horner-Devine M C. 2011. Drivers of bacterial β-diversity depend on spatial scale. Proc. Natl. Acad. Sci. U. S. A., 108(19):7 850-7 854.
McBride M J. 2014. The family flavobacteriaceae. In:Rosenberg E, DeLong E F, Lory S, Stackebrandt E, Thompson F eds. The Prokaryotes. Springer, Berlin Heidelberg. p.643-676.
Nelson C E, Carison C A, Ewart C S, Halewood E R. 2014.Community differentiation and population enrichment of Sargasso Sea bacterioplankton in the euphotic zone of a mesoscale mode-water eddy. Environ. Microbiol., 16(3):871-887.
Nie N H, Bent D H, Hull C H. SPSS:1970. Statistical Package for the Social Sciences[M]. New York:McGraw-Hill.
Nogales B, Aguiló-Ferretjans M M, Martín-Cardona C, Lalucat J, Bosch R. 2007. Bacterial diversity, composition and dynamics in and around recreational coastal areas.Environ. Microbiol., 9(8):1 913-1 929.
Nogales B, Lanfranconi M P, Piña-Villalonga J M, Bosch R. 2011. Anthropogenic perturbations in marine microbial communities. FEMS Microbiol. Rev., 35(2):275-298.
Paerl H W. 2006. Assessing and managing nutrient-enhanced eutrophication in estuarine and coastal waters:interactive effects of human and climatic perturbations. Ecol. Eng., 26(1):40-54.
Partensky F, Blanchot J, Vaulot D. 1999. Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters:a review. Bulletin de l'Institut Océanographique, 19(19):457-476.
Pujalte M J, Lucena T, Ruvir M A, Arahal D R, Macián M. 2014. The family Rhodobacteraceae. In:Rosenberg E, DeLong E F, Lory S, Stackebrandt E, Thompson F eds.The Prokaryotes. Springer-Verlag, Berlin Heidelberg.p.439-512.
Teeling H, Fuchs B M, Becher D, Klockow C, Gardebrecht A, Bennke C M, Kassabgy M, Huang S, Mann A J, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann F D, Callies U, Gerdts G, Wichels A, Wiltshire K H, Glockner F O, Schweder T, Amann R. 2012. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science, 336(6081):608-611.
Thompson F L, Bruce T, Gonzalez A, Cardoso A, Clementino M, Costagliola M, Hozbor C, Otero E, Piccini C, Peressutti S, Schmieder R, Edwards R, Smith M, Takiyama L R, Vieira R, Paranhos R, Artigas L F. 2011. Coastal bacterioplankton community diversity along a latitudinal gradient in Latin America by means of V6 tag pyrosequencing. Arch. Microbiol., 193(2):105-114.
Verreydt D, De Meester L, Decaestecker E, Villena M J, Van Der Gucht K, Vannormelingen P, Vyverman W, Declerck S A. 2012. Dispersal-mediated trophic interactions can generate apparent patterns of dispersal limitation in aquatic metacommunities. Ecol. Lett., 15(3):218-226.
Wang K, Ye X S, Chen H P, Zhao Q F, Hu C J, He J Y, Qian Y X, Xiong J B, Zhu J L, Zhang D M. 2015a. Bacterial biogeography in the coastal waters of northern Zhejiang, East China Sea is highly controlled by spatially structured environmental gradients. Environ. Microbiol., 17(10):3 898-3 913.
Wang K, Zhang D M, Xiong J B, Chen X X, Zheng J L, Hu C J, Yang Y N, Zhu J L. 2015b. Response of bacterioplankton communities to cadmium exposure in coastal water microcosms with high temporal variability. Appl. Environ Microb., 81(1):231-240.
Xiong J B, Ye X S, Wang K, Chen H P, Hu C J, Zhu J L, Zhang D M. 2014. Biogeography of the sediment bacterial community responds to a nitrogen pollution gradient in the East China Sea. Appl. Environ. Microbiol., 80(6):1 919-1 925.
Copyright © Haiyang Xuebao