Abstract
Elucidating the bacterioplankton spatial distribution patterns and its determinants is a central topic in ecological research. However, research on the distribution patterns of bacterioplankton community composition (BCC) within a small-sized, highly dynamic freshwater lake remains unclear. In this study, we collected surface water samples from West Lake to investigate the spatiotemporal variation of BCC by 16S rRNA gene high-throughput sequencing. Clear spatial heterogeneity in BCC was identified both in summer and winter. The relatively high abundant taxa exhibited greater correlations with environmental factors and other abundant species in summer than in winter. Variation partitioning analysis was used to unravel the relative importance of environmental factors and spatial processes and further explore the underlying mechanism of BCC successions. Our results showed the predominant shared effect of environmental and spatial factors on BCC in summer (68.41%) and winter (57.37%), indicating that spatially structured environmental factors were the key determinants of structuring BCC spatial heterogeneity in West Lake in the two seasons. Furthermore, environmental factors alone explained a higher proportion of the variation in summer whereas spatial factors explained a higher proportion in winter. These divergences may be related to seasonal environmental changes and anthropogenic disturbances. Our study provided knowledge on BCC spatial heterogeneity in small freshwater habitats and their underlying determinants in different seasons.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Astorga A, Oksanen J, Luoto M, Soininen J, Virtanen R, Muotka T (2012) Distance decay of similarity in freshwater communities: do macro- and microorganisms follow the same rules? Glob Ecol Biogeogr 21(3):365–375. https://doi.org/10.1111/j.1466-8238.2011.00681.x
Azam F, Frenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263. https://doi.org/10.3354/meps010257
Bergman B, Gallon J, Rai A, Stal L (1997) N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiology Reviews 19(3):13–185. https://doi.org/10.1016/S0168-6445(96)00028-9
Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89(9):2623–2632. https://doi.org/10.1890/07-0986.1
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich KJ, Gordon IJ, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Clercin NA, Druschel GK (2019) Influence of environmental factors on the production of MIB and Geosmin metabolites by bacteria in a eutrophic reservoir. Water Resources Research 55(7):5413–5430. https://doi.org/10.1029/2018WR023651
Committee of Compiling Records of Hangzhou (CCRH) (2017) Hangzhou statistical yearbook 2017. http://tjj.hangzhou.gov.cn/art/2017/11/6/art_1653175_35022587html Accessed 6 July 2019 (in Chinese)
Dai W, Zhang J, Tu Q, Deng Y, Qiu Q, Xiong J (2017) Bacterioplankton assembly and interspecies interaction indicating increasing coastal eutrophication. Chemosphere 177:317–325. https://doi.org/10.1016/j.chemosphere.2017.03.034
Daniel B, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68. https://doi.org/10.1016/S0304-3800(01)00501-4
DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL (2006a) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34(suppl_2):W394–W399. https://doi.org/10.1093/nar/gkl244
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006b) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072. https://doi.org/10.1128/AEM.03006-05
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Science 320(5879):1034–1039. https://doi.org/10.1126/science.1153213
Fodelianakis S, Papageorgiou N, Pitta P, Kasapidis P, Karakassis I, Ladoukakis ED (2014) The pattern of change in the abundances of specific bacterioplankton groups is consistent across different nutrient-enriched habitats in Crete. Appl Environ Microbiol 80(13):3784–3792. https://doi.org/10.1128/AEM.00088-14
Koopman KR, Collas FP, Breure AM, Lenders RHJ, Velde G, Leuven RS (2018) Predicting effects of ship-induced changes in flow velocity on native and alien molluscs in the littoral zone of lowland rivers. 13(4):481–490. doi:https://doi.org/10.3391/ai.2018.13.4.06
Langenheder S, Lindström ES (2019) Factors influencing aquatic and terrestrial bacterial community assembly. Environ Microbiol Rep 11(3):306–315. https://doi.org/10.1111/1758-2229.12731
Lear G, Washington V, Neale M, Case B, Buckley H, Lewis G (2013) The biogeography of stream bacteria. Glob Ecol Biogeogr 22(5):544–554. https://doi.org/10.1111/geb.12046
Lear G, Bellamy J, Case BS, Lee JE, Buckley HL (2014) Fine-scale spatial patterns in bacterial community composition and function within freshwater ponds. ISME J 8(8):1715–1726. https://doi.org/10.1038/ismej.2014.21
Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69(1):1–24. https://doi.org/10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2
Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunityconcept: a framework for multi-scale community ecology. Ecol Lett 7:601–613. https://doi.org/10.1111/j.1461-0248.2004.00608.x
Lima MS, da Motta MD, They NH, McMahon KD, Rodrigues LR, de Souza CL, Crossetti LO (2016) Contrasting factors drive within-lake bacterial community composition and functional traits in a large shallow subtropical lake. Hydrobiologia 778(1):105–120. https://doi.org/10.1007/s10750-015-2610-9
Liu L, Yang J, Yu X, Chen G, Yu Z (2013) Patterns in the composition of microbial communities from a subtropical river: effects of environmental, spatial and temporal factors. PLoS One 8(11):e81232. https://doi.org/10.1371/journal.pone.0081232
Logue JB, Lindström ES (2008) Biogeography of bacterioplankton in inland waters. Fr Rev 1(1):99–115. https://doi.org/10.1608/FRJ-1.1.9
Lucas J, Wichels A, Gerdts G (2016) Spatiotemporal variation of the bacterioplankton community in the German Bight: from estuarine to offshore regions. Helgoland Mar Res 70(1):16–15. https://doi.org/10.1186/s10152-016-0464-9
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Glavina del Rio T, Robert C, Edgar RC, Thiloeickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90. https://doi.org/10.1038/nature11237
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Meot A, Legendre P, Borcard D (1998) Partialling out the spatial component of ecological variation: questions and propositions in the linear modelling framework. Environ Ecol Stat 5(1):1–27. https://doi.org/10.1023/a:1009693501830
Mikhailov IS, Zakharova YR, Bukin YS, Galachyants YP, Petrova DP, Sakirko MV, Likhoshway YV (2019) Co-occurrence networks among bacteria and microbial eukaryotes of Lake Baikal during a spring phytoplankton bloom. Microb Ecol 77(1):96–109. https://doi.org/10.1007/s00248-018-1212-2
Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75(1):14–49. https://doi.org/10.1128/MMBR.00028-10
O’brien RM (2007) A caution regarding rules of thumb for variance inflation factors. Qual Quant 41(5):673–690. https://doi.org/10.1007/s11135-006-9018-6
Salcher MM, Pernthaler J, Posch T (2011) Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria ‘that rule the waves’ (LD12). ISME J 5(8):1242–1252. https://doi.org/10.1038/ismej.2011.8
Sommaruga R, Casamayor EO (2008) Bacterial ‘cosmopolitanism’ and importance of local environmental factors for community composition in remote high-altitude lakes. Freshw Biol 54:994–1005. https://doi.org/10.1111/j.1365-2427.2008.02146.x
Souffreau CK, van der Gucht I, van Gremberghe S, Kosten G, Lacerot LM, Lobaõ VL, de Moraes Huszar F, Roland E, Jeppesen W, Vyverman L, Meester D (2015) Environmental rather than spatial factors structure bacterioplankton communities in shallow lakes along a > 6000 km latitudinal gradient in South America. Environ Microbiol 17:2336–2351. https://doi.org/10.1111/1462-2920.12692
Tang X, Xie G, Shao K, Dai J, Chen Y, Xu Q, Gao G (2015) Bacterial community composition in Oligosaline Lake Bosten: low overlap of Betaproteobacteria and Bacteroidetes with freshwater ecosystems. Microbes Environ 30(2):180–188. https://doi.org/10.1264/jsme2.ME14177
Teira E, Martínez-García S, Calvo-Díaz A, Morán XAG (2010) Effects of inorganic and organic nutrient inputs on bacterioplankton community composition along a latitudinal transect in the Atlantic Ocean. Aquat Microb Ecol 60(3):299–313. https://doi.org/10.3354/ame01435
Venohr M, Langhans SD, Peters O, Hölker F, Arlinghaus R, Mitchell L, Wolter C (2018) The underestimated dynamics and impacts of water-based recreational activities on freshwater ecosystems. Environ Rev 26(2):199–213. https://doi.org/10.1139/er-2017-0024
Wang J, Shen J, Wu Y, Tu C, Soininen J, Stegen JC, He JZ, Liu XQ, Zhang L, Zhang E (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7(7):1310–1321. https://doi.org/10.1038/ismej.2013.30
Wang K, Ye XS, Chen HP, Zhao QF, Hu CJ, He JY, Qian YX, Xiong JB, Zhu JL, Zhang DM (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):3898–3913. https://doi.org/10.1111/1462-2920.12884
Wang Y, Liu L, Chen H, Yang J (2015b) Spatiotemporal dynamics and determinants of planktonic bacterial and microeukaryotic communities in a Chinese subtropical river. Appl Microbiol Biotechnol 99(21):9255–9266. https://doi.org/10.1007/s00253-015-6773-0
Wang J, Pan F, Soininen J, Heino J, Shen J (2016) Nutrient enrichment modifies temperature-biodiversity relationships in large-scale field experiments. Nat Commun 7:13960. https://doi.org/10.1038/ncomms13960
Wang K, Razzano M, Mou XZ (2020) Cyanobacterial blooms alter the relative importance of neutral and selective processes in assembling freshwater bacterioplankton community. Sci Total Environ 706. https://doi.org/10.1016/j.scitotenv.2019.135724
Wilson DS (1992) Complex interactions in metacommunities, with implications for biodiversity and higher levels of selection. Ecology 73(6):1984–2000. https://doi.org/10.2307/1941449
Wu QL, Zwart G, Wu JF, Kamst-van Agterveld MP, Liu SJ, Hahn MW (2007) Submersed macrophytes play a key role in structuring bacterioplankton community composition in the large, shallow, subtropical Taihu Lake, China. Environ Microbiol 9(11):2765–2774. https://doi.org/10.1111/j.1462-2920.2007.01388.x
Xiong J, Chen H, Hu C, Ye X, Kong D, Zhang D (2015) Evidence of bacterioplankton community adaptation in response to long-term mariculture disturbance. Sci Rep 5:15274. https://doi.org/10.1038/srep15274
Yang J, Wu ZY, Xu J, Yao SP, Chen Y, Cai TT, Ding XY (2014) Analysis of the nutrient characteristics and eutrophication status in different areas of West Lake. Environmental Science Survey 33(3):8–12 (in Chinese)
Yang W, Zheng C, Zheng ZM, Wei YM, Lu KH, Zhu JY (2018) Nutrient enrichment during shrimp cultivation alters bacterioplankton assemblies and destroys community stability. Ecotoxicol Environ Saf 156:366–374. https://doi.org/10.1016/j.ecoenv.2018.03.043
You AJ, Wu ZY, Han ZC, Yang J, Hua L (2015) Spatial and temporal distributions and variations of nutrients in the West Lake, Hangzhou, after the implementation of integrated water management program (1985–2013). Lake Science 27(3):371–377 (in Chinese)
Yu S, He R, Song A, Huang YD, Jin ZJ, Liang YM, Li Q, Wang XH, Müller WEG, Cao JH (2019) Spatial and temporal dynamics of bacterioplankton community composition in a subtropical dammed karst river of southwestern China. Microbiology Open 2. https://doi.org/10.1002/mbo3.849
Zhang HJ, Huang XL, Huang L, Bao FJ, Xiong SL, Wang K, Zhang DM (2018) Microeukaryotic biogeography in the typical subtropical coastal waters with multiple environmental gradients. Sci Total Environ 635:618–628. https://doi.org/10.1016/j.scitotenv.2018.04.142
Zhao DY, Xu HM, Zeng J, Cao XY, Huang R, Shen F, Yu ZB (2017) Community composition and assembly processes of the free living and particle-attached bacteria in Taihu Lake. FEMS Microbiol Ecol 293:fix062. https://doi.org/10.1093/femsec/fix062
Zhu CM, Zhang JY, Nawaz MZ, Mahboob S, Al-Ghanim KA, Khan IA, Lu ZH, Chen T (2019) Seasonal succession and spatial distribution of bacterial community structure in a eutrophic freshwater Lake, Lake Taihu. Sci Total Environ 669:29–40. https://doi.org/10.1016/j.scitotenv.2019.03.087
Funding
Our work was supported by the Zhejiang Provincial Natural Science Foundation of China (No. LY17C190004, LQ20C190003), Zhejiang Province Public Welfare Technology Application Research Project (LGN19C200010), and Ningbo Municipal Natural Science Foundation (2019A610443, 2019A610421) and also sponsored by the K.C. Wong Magna Fund in Ningbo University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Diane Purchase
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 640 kb)
Rights and permissions
About this article
Cite this article
Du, Y., Yang, W., Ding, X. et al. High heterogeneity of bacterioplankton community shaped by spatially structured environmental factors in West Lake, a typical urban lake in eastern China. Environ Sci Pollut Res 27, 42283–42293 (2020). https://doi.org/10.1007/s11356-020-08818-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-08818-w