Cite this paper:
ANG Yujing, LI Huabing, XING Peng, WU Qinglong. Contrasting patterns of free-living bacterioplankton diversity in macrophyte-dominated versus phytoplankton blooming regimes in Dianchi Lake, a shallow lake in China[J]. Journal of Oceanology and Limnology, 2017, 35(2): 336-349

Contrasting patterns of free-living bacterioplankton diversity in macrophyte-dominated versus phytoplankton blooming regimes in Dianchi Lake, a shallow lake in China

ANG Yujing1,2, LI Huabing1, XING Peng1, WU Qinglong1,3
1 State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China;
2 University of Chinese Academy of Sciences, Beijing 100039, China;
3 Sino-Danish Center for Science and Education, Beijing 100039, China
Abstract:
Freshwater shallow lakes typically exhibit two alternative stable states under certain nutrient loadings:macrophyte-dominated and phytoplankton-dominated water regimes. An ecosystem regime shift from macrophytes to phytoplankton blooming typically reduces the number of species of invertebrates and fishes and results in the homogenization of communities in freshwater lakes. We investigated how microbial biodiversity has responded to a shift of the ecosystem regime in Dianchi Lake, which was previously fully covered with submerged macrophytes but currently harbors both ecological states. We observed marked divergence in the diversity and community composition of bacterioplankton between the two regimes. Although species richness, estimated as the number of operational taxonomic units and phylogenetic diversity (PD), was higher in the phytoplankton dominated ecosystem after this shift, the dissimilarity of bacterioplankton community across space decreased. This decrease in beta diversity was accompanied by loss of planktonic bacteria unique to the macrophyte-dominated ecosystem. Mantel tests between bacterioplankton community distances and Euclidian distance of environmental parameters indicated that this reduced bacterial community differentiation primarily reflected the loss of environmental niches, particularly in the macrophyte regime. The loss of this small-scale heterogeneity in bacterial communities should be considered when assessing long-term biodiversity changes in response to ecosystem regime conversions in freshwater lakes.
Key words:    bacterioplankton biodiversity|regime shift|macrophyte|phytoplankton   
Received: 2015-10-13   Revised: 2015-12-07
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Articles by LI Huabing
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References:
Balata D, Piazzi L, Benedetti-Cecchi L. 2007. Sediment disturbance and loss of beta diversity on subtidal rocky reefs. Ecology, 88(10):2 455-2 461.
Brunberg A K. 1999. Contribution of bacteria in the mucilage of Microcystis spp. (Cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiol. Ecol., 29(1):13-22.
Caporaso J G, Lauber C L, Walters W A et al. 2012. Ultra-highthroughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J., 6(8):1 621-1 624.
Chase J M, Kraft N J B, Smith K G, Vellend M, Inouye B D. 2011. Using null models to disentangle variation in community dissimilarity from variation in α-diversity.Ecosphere, 2(2):1-11.
Crump B C, Amaral-Zettler L A, Kling G W. 2012. Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils. ISME J., 6(9):1 629-1 639.
Donohue I, Jackson A L, Pusch M T, Irvine K. 2009. Nutrient enrichment homogenizes lake benthic assemblages at local and regional scales. Ecology, 90(12):3 470-3 477.
Dudgeon D, Arthington A H, Gessner M O et al. 2006.Freshwater biodiversity:importance, threats, status and conservation challenges. Biol. Rev., 81(2):163-182.
Edgar R C. 2013. UPARSE:highly accurate OTU sequences from microbial amplicon reads. Nat. Methods, 10(10):996-998.
Eiler A, Bertilsson S. 2004. Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ. Microbiol., 6(12):1 228-1 243.
Faith D P. 1992. Conservation evaluation and phylogenetic diversity. Biol. Conserv., 61(1):1-10.
Gallego I, Davidson T A, Jeppesen E, Pérez-Martínez C, Fuentes-Rodríguez F, Juan M, Casas J J. 2014. Disturbance from pond management obscures local and regional drivers of assemblages of primary producers. Freshwater Biol., 59(7):1 406-1 422.
Good I J. 1953. The population frequencies of species and the estimation of population parameters. Biometrika, 40(3-4):237-264.
Haukka K, Kolmonen E, Hyder R, Hietala J, Vakkilainen K, Kairesalo T, Haario H, Sivonen K. 2006. Effect of nutrient loading on bacterioplankton community composition in lake mesocosms. Microb. Ecol., 51(2):137-146.
He D, Ren L J, Wu Q L. 2012. Epiphytic bacterial communities on two common submerged macrophytes in Taihu Lake:diversity and host-specificity. Chin. J. Oceanol. Limnol., 30(2):237-247.
He D, Ren L J, Wu Q L. 2014. Contrasting diversity of epibiotic bacteria and surrounding bacterioplankton of a common submerged macrophyte, Potamogeton crispus, in freshwater lakes. FEMS Microbiol. Ecol., 90(3):551-562.
Horner-Devine M C, Leibold M A, Smith V H, Bohannan B J M. 2003. Bacterial diversity patterns along a gradient of primary productivity. Ecol. Lett., 6(7):613-622.
Jeppesen E, Jensen J P, Søndergaard M, Lauridsen T, Pedersen L J, Jensen L. 1997. Top-down control in freshwater lakes:the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia, 342-343:151-164.
Jespersen A M, Christoffersen K. 1987. Measurements of chlorophyll a from phytoplankton using ethanol as extraction solvent. Archiv für Hydrobiologie, 109(3):445-454.
Jones S E, Cadkin T A, Newton R J, McMahon K D. 2012.Spatial and temporal scales of aquatic bacterial beta diversity. Front Microbiol., 3:318.
Legendre P, Legendre L F. 2012. Numerical Ecology. 3rd ed.Elsevier Science, Amsterdam.
Lindström E S, Bergström A K. 2004. Influence of inlet bacteria on bacterioplankton assemblage composition in lakes of different hydraulic retention time. Limnol.Oceanogr., 49(1):125-136.
Liu L M, Yang J, Lv H, Yu Z. 2014. Synchronous dynamics and correlations between bacteria and phytoplankton in a subtropical drinking water reservoir. FEMS Microbiol.Ecol., 90(1):126-138.
Logares R, Lindström E S, Langenheder S, Logue J B, Paterson H, Laybourn-Parry J, Rengefors K, Tranvik L, Bertilsson S. 2013. Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J., 7(5):937-948.
Ludwig W, Strunk O, Westram R et al. 2004. ARB:a software environment for sequence data. Nucl. Acids Res., 32(4):1 363-1 371.
Maloney K O, Munguia P, Mitchell R M. 2011. Anthropogenic disturbance and landscape patterns affect diversity patterns of aquatic benthic macroinvertebrates. Journal of the North American Benthological Society, 30(1):284-295.
Newton R J, Jones S E, Eiler A, McMahon K D, Bertilsson S. 2011. A guide to the natural history of freshwater lake bacteria. Microbiol. Mol. Biol. Rev., 75(1):14-49.
Oksanen J, Blanchet F G, Kindt R, Legendre P, Minchin P R, O'Hara R, Simpson G L, Solymos P, Stevens M H H, Wagner H. 2013. vegan:community ecology package. R package version 2, http://CRAN.R-project.org/package=vegan. Accessed on 2015-01-01.
Olden J D, Poff N L. 2004. Ecological processes driving biotic homogenization:testing a mechanistic model using fish faunas. Ecology, 85(7):1 867-1 875.
Passy S I, Blanchet F G. 2007. Algal communities in humanimpacted stream ecosystems suffer beta-diversity decline.Diversity and Distributions, 13(6):670-679.
Price M N, Dehal P S, Arkin A P. 2010. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One, 5(3):e9490.
Rice E W, Baird R B, Eaton A D, Clesceri L S. 2012. Standard Methods for the Examination of Water and Wastewater.American Public Health Association, Washington DC.
Rodrigues J L M, Pellizari V H, Mueller R, et al. 2013.Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities.Proc. Natl. Acad. Sci. U. S. A., 110(3):988-993.
Roesch L F, Fulthorpe R R, Riva A, Casella G, Hadwin A K, Kent A D, Daroub S H, Camargo F A, Farmerie W G, Triplett E W. 2007. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J., 1(4):283-290.
Scheffer M, Hosper S H, Meijer M L, Moss B, Jeppesen E. 1993. Alternative equilibria in shallow lakes. Trends Ecol.Evol., 8(8):275-279.
Simek K, Kasalický V, Horňák K, Hahn M W, Weinbauer M G. 2010. Assessing niche separation among coexisting Limnohabitans strains through interactions with a competitor, viruses, and a bacterivore. Appl. Environ.Microbiol., 76(5):1 406-1 416.
Van der Gucht K, Cottenie K, Muylaert K et al. 2007. The power of species sorting:local factors drive bacterial community composition over a wide range of spatial scales. Proc. Natl. Acad. Sci. U. S. A., 104(51):20 404-20 409.
Van der Gucht K, Sabbe K, de Meester L, Vloemans N, Zwart G, Gillis M, Vyverman W. 2001. Contrasting bacterioplankton community composition and seasonal dynamics in two neighbouring hypertrophic freshwater lakes. Environ. Microbiol., 3(11):680-690.
Wang L Z, Liu Y D, Chen L, Xiao B D, Liu J T, Wu Q L. 2007a. Benthic macroinvertebrate communities in Dianchi Lake Yunnan and assessment of its water. Acta Hydrob. Sin., 31(4):590-593. (in Chinese with English abstract)
Wang Q, Garrity G M, Tiedje J M, Cole J R. 2007b. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ.Microbiol., 73(16):5 261-5 267.
Wang S M, Dou H S. 1998. Lakes in China. Science Press, Beijing, China. (in Chinese)
Wetzel R G, Søndergaard M. 1998. Role of submerged macrophytes for the microbial community and dynamics of dissolved organic carbon in aquatic ecosystems. In:Jeppesen E, Søndergaard M, Søndergaard M, Christoffersen K eds. The Structuring Role of Submerged Macrophytes in Lakes. Springer Press, New York. p.133-148.
Wu Q L, Zwart G, Schauer M, Kamst-van Agterveld M P, Hahn M W. 2006. Bacterioplankton community composition along a salinity gradient of sixteen highmountain lakes located on the Tibetan Plateau, China.Appl. Environ. Microbiol., 72(8):5 478-5 485.
Wu Q L, Zwart G, Wu J, Kamst-van Agterveld M P, Liu S J, Hahn M W. 2007. Submersed macrophytes play a key role in structuring bacterioplankton community composition in the large, shallow, subtropical Taihu Lake, China.Environ. Microbiol., 9(11):2 765-2 774.
Yuan Y, Chen C, Liang B et al. 2014. Fine-tuning key parameters of an integrated reactor system for the simultaneous removal of COD, sulfate and ammonium and elemental sulfur reclamation. J. Hazard. Mater., 269:56-67.
Zapala M A, Schork N J. 2006. Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proc. Natl.Acad. Sci. U. S. A., 103(51):19 430-19 435.
Zeng J, Bian Y Q, Xing P, Wu Q L. 2012. Macrophyte species drive the variation of bacterioplankton community composition in a shallow freshwater lake. Appl. Environ.Microbiol., 78(1):177-184.
Zhao D Y, Liu P, Fang C, Sun Y M, Zeng J, Wang J Q, Ma T, Xiao Y H, Wu Q L. 2013. Submerged macrophytes modify bacterial community composition in sediments in a large, shallow, freshwater lake. Canadian Journal of Microbiology, 59(4):237-244.
Zhu G B, Wang S Y, Wang W D et al. 2013. Hotspots of anaerobic ammonium oxidation at land-freshwater interfaces. Nat. Geosci., 6(2):103-107.
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