Abstract
At certain nutrient concentrations, shallow freshwater lakes are generally characterized by two contrasting ecological regimes with disparate patterns of biodiversity and biogeochemical cycles: a macrophyte-dominated regime (MDR) and a phytoplankton-dominated regime (PDR). To reveal ecological mechanisms that affect bacterioplankton along the regime shift, Illumina MiSeq sequencing of the 16S rRNA gene combined with a novel network clustering tool (Manta) were used to identify patterns of bacterioplankton community composition across the regime shift in Taihu Lake, China. Marked divergence in the composition and ecological assembly processes of bacterioplankton community was observed under the regime shift. The alpha diversity of the bacterioplankton community consistently and continuously decreased with the regime shift from MDR to PDR, while the beta diversity presents differently. Moreover, as the regime shifted from MDR to PDR, the contribution of deterministic processes (such as environmental selection) to the assembly of bacterioplankton community initially decreased and then increased again as regime shift from MDR to PDR, most likely as a consequence of differences in nutrient concentration. The topological properties, including modularity, transitivity and network diameter, of the bacterioplankton co-occurrence networks changed along the regime shift, and the co-occurrences among species changed in structure and were significantly shaped by the environmental variables along the regime transition from MDR to PDR. The divergent environmental state of the regimes with diverse nutritional status may be the most important factor that contributes to the dissimilarity of bacterioplankton community composition along the regime shift.
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Data Availability
The raw reads were deposited into the NCBI Sequence Read Archive (SRA) database (BioProject: PRJNA511603).
Code Availability
Not applicable.
References
Scheffer M, van Nes EH (2007) Shallow lakes theory revisited: various alternative regimes driven by climate, nutrients, depth and lake size. Hydrobiologia 584:455–466. https://doi.org/10.1007/s10750-007-0616-7
Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279. https://doi.org/10.1016/0169-5347(93)90254-M
Wang Y, Cao X et al (2020) Distinct shifts in bacterioplankton community composition and functional gene structure between macrophyte-and phytoplankton-dominated regimes in a large shallow lake. Limnol Oceanogr 65:S208–S219. https://doi.org/10.1002/lno.11373
Van der Gucht K, Sabbe K et al (2010) Contrasting bacterioplankton community composition and seasonal dynamics in two neighbouring hypertrophic freshwater lakes. Environ Microbiol 3:680–690. https://doi.org/10.1046/j.1462-2920.2001.00242.x
Haukka K, Kolmonen E et al (2006) Effect of nutrient loading on bacterioplankton community composition in lake mesocosms. Microb Ecol 51:137–146. https://doi.org/10.1007/s00248-005-0049-7
Dakos V, Matthews B et al (2019) Ecosystem tipping points in an evolving world. Nat Ecol Evol 3:355–362. https://doi.org/10.1038/s41559-019-0797-2
Wang H, Wang H, Liang X, Wu S (2014) Total phosphorus thresholds for regime shifts are nearly equal in subtropical and temperate shallow lakes with moderate depths and areas. Freshw Biol 59:1659–1671. https://doi.org/10.1111/fwb.12372
Wetzel RG, 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, New York, pp 133–148
González Sagrario MA, Jeppesen E et al (2005) Does high nitrogen loading prevent clear-water conditions in shallow lakes at moderately high phosphorus concentrations? Freshw Biol 50:27–41. https://doi.org/10.1111/j.1365-2427.2004.01290.x
Zimmer KD, Hanson MA, Herwig BR, Konsti ML (2009) Thresholds and stability of alternative regimes in shallow Prairie-Parkland Lakes of Central North America. Ecosystems 12:843–852. https://doi.org/10.1007/s10021-009-9262-4
Hanashiro FTT, Mukherjee S et al (2019) Freshwater bacterioplankton metacommunity structure along urbanization gradients in Belgium. Front Microbiol 10:743. https://doi.org/10.3389/fmicb.2019.00743
Khazaei T, Williams RL et al (2020) Metabolic multistability and hysteresis in a model aerobe-anaerobe microbiome community. Sci Adv 6:eaba353. https://doi.org/10.1126/sciadv.aba0353
Hillebrand H, Langenheder S et al (2018) Decomposing multiple dimensions of stability in global change experiments. Ecol Lett 21:21–30. https://doi.org/10.1111/ele.12867
Gonze D, Lahti L, Raes J, Faust K (2017) Multi-stability and the origin of microbial community types. ISME J 11:2159–2166. https://doi.org/10.1038/ismej.2017.60
Jeppesen E, Jensen JP et al (1997) Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 342:151–164. https://doi.org/10.1023/a:1017046130329
Han X, Schubert CJ, Fiskal A, Dubois N, Lever MA (2020) Eutrophication as a driver of microbial community structure in lake. Environ Microbiol 22:3446–3462. https://doi.org/10.1111/1462-2920.15115
Corno G, Caravati E, Callieri C, Bertoni R (2008) Effects of predation pressure on bacterial abundance, diversity, and size-structure distribution in an oligotrophic system. J Limnol 67:107–119. https://doi.org/10.4081/jlimnol.2008.107
Berga M, Östman Ö, Lindström ES, Langenheder S (2014) Combined effects of zooplankton grazing and dispersal on the diversity and assembly mechanisms of bacterial metacommunities. Environ Microbiol 17:2275–2287. https://doi.org/10.1111/1462-2920.12688
Chang W, Sun J et al (2020) Effects of different habitats on the bacterial community composition in the water and sediments of Lake Taihu, China. Environ Sci Pollut Res 27:44983–44994. https://doi.org/10.1007/s11356-020-10376-0
Wu QL, Zwart G et al (2010) Submersed macrophytes play a key role in structuring bacterioplankton community composition in the large, shallow, subtropical Taihu Lake, China. Environ Microbiol 9:2765–2774. https://doi.org/10.1111/j.1462-2920.2007.01388.x
Pang X, Shen H et al (2014) Dissolved organic carbon and relationship with bacterioplankton community composition in 3 lake regions of Lake Taihu, China. Can J Microbiol 60:669–680. https://doi.org/10.1139/cjm-2013-0847
Zhou L, Zhou Y, Tang X, Zhang Y, Jeppesen E (2021) Biodegradable dissolved organic carbon shapes bacterial community structures and co-occurrence patterns in large eutrophic Lake Taihu. J Environ Sci 107:205–217. https://doi.org/10.1016/j.jes.2021.02.011
Langenheder S, Székely AJ (2011) Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J 5:1086–1094. https://doi.org/10.1038/ismej.2010.207
Stegen JC, Lin X, Fredrickson JK, Konopka AE (2015) Estimating and mapping ecological processes influencing microbial community assembly. Front Microbiol 6:370. https://doi.org/10.3389/fmicb.2015.00370
Zhou J, Ning D (2017) Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol Rev. https://doi.org/10.1128/mmbr.00002-17
Stegen JC, Lin X et al (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079. https://doi.org/10.1038/ismej.2013.93
Wang J, Shen J et al (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7:1310–1321. https://doi.org/10.1038/ismej.2013.30
Röttjers L, Faust K (2020) manta: a clustering algorithm for weighted ecological networks. Msystems. https://doi.org/10.1128/mSystems.00903-19
Röttjers L, Faust K (2018) From hairballs to hypotheses–biological insights from microbial networks. FEMS Microbiol Rev 42:761–780. https://doi.org/10.1093/femsre/fuy030
Ma B, Wang Y et al (2020) Earth microbial co-occurrence network reveals interconnection pattern across microbiomes. Microbiome 8:1–12. https://doi.org/10.1186/s40168-020-00857-2
Lima-Mendez G, Faust K et al (2015) Determinants of community structure in the global plankton interactome. Science 348:1262073. https://doi.org/10.1126/science.1262073
Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219. https://doi.org/10.3389/fmicb.2014.00219
Qin B, Liu Z, Havens K (2007) Eutrophication of Shallow Lakes with Special Reference to Lake Taihu, China. Springer, Netherlands
Janssen AB, de Jager VC et al (2017) Spatial identification of critical nutrient loads of large shallow lakes: implications for Lake Taihu (China). Water Res 119:276–287. https://doi.org/10.1016/j.watres.2017.04.045
Qin B, Xu P, Wu Q, Luo L, Zhang Y (2007) Environmental issues of Lake Taihu, China. Hydrobiologia 581:3–14. https://doi.org/10.1007/s10750-006-0521-5
Caporaso JG, Lauber CL et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. Isme J Multidiscip J Microbial Ecol 6:1621–1624. https://doi.org/10.1038/ismej.2012.8
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
Oksanen J, Blanchet FG et al (2013) vegan: Community Ecology Package. R package version 2: http://CRAN.R-project.org/package=vegan
Zapala MA, Schork NJ (2006) Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proc Natl Acad Sci 103:19430–19435. https://doi.org/10.1073/pnas.0609333103
Chafee M, Fernàndez-Guerra A et al (2017) Recurrent patterns of microdiversity in a temperate coastal marine environment. ISME J 12:237–252. https://doi.org/10.1038/ismej.2017.165
Legendre P, Legendre LF (2012) Numerical ecology, vol 24, 3rd edn. Elsevier Science, Oxford
Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. https://doi.org/10.1371/journal.pone.0009490
Dini-Andreote F, Stegen JC, Van Elsas JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci 112:E1326–E1332. https://doi.org/10.1073/pnas.1414261112
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Kembel SW, Cowan PD et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Stegen JC, Lin X, Konopka AE, Fredrickson JK (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6:1653–1664. https://doi.org/10.1038/ismej.2012.22
Weiss S, Treuren WV et al (2016) Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J 10:1669–1681. https://doi.org/10.1038/ismej.2015.235
Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550. https://doi.org/10.1038/nrmicro2832
Ognyanova K (2016) Network Analysis and Visualization with R and igraph
Shannon P, Markiel A et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Csardi G (2006) The igraph software package for complex network research 1695
Guimerà R, Amaral LAN (2005) Functional cartography of complex metabolic networks. Nature 433:895–900. https://doi.org/10.1038/nature03288
Guimerà R, Sales-Pardo M, Amaral LAN (2007) Classes of complex networks defined by role-to-role connectivity profiles. Nat Phys 3:63–69. https://doi.org/10.1038/nphys489
Deng Y, Jiang Y et al (2012) Molecular ecological network analyses. BMC Bioinformatics. https://doi.org/10.1186/1471-2105-13-113
Zhao D, Cao X et al (2017) The heterogeneity of composition and assembly processes of the microbial community between different nutrient loading lake zones in Taihu Lake. Appl Microbiol Biotechnol 101:1–11. https://doi.org/10.1007/s00253-017-8327-0
Ren L, Song X et al (2017) Contrasting patterns of freshwater microbial metabolic potentials and functional gene interactions between an acidic mining lake and a weakly alkaline lake. Limnol Oceanogr 63:S354–S366. https://doi.org/10.1002/lno.10744
Brothers SM, Hilt S et al (2013) A regime shift from macrophyte to phytoplankton dominance enhances carbon burial in a shallow, eutrophic lake. Ecosphere 4:1–17. https://doi.org/10.1890/ES13-00247.1
Xu H, Zhao D et al (2020) Distinct successional patterns and processes of free-living and particle-attached bacterial communities throughout a phytoplankton bloom. Freshw Biol 65:1363–1375. https://doi.org/10.1111/fwb.13505
Zeng J, Jiao CC et al (2019) Patterns and assembly processes of planktonic and sedimentary bacterial community differ along a trophic gradient in freshwater lakes. Ecol Ind. https://doi.org/10.1016/j.ecolind.2019.105491
Carpenter SR, Lathrop RC (2008) Probabilistic estimate of a threshold for eutrophication. Ecosystems 11:601–613. https://doi.org/10.1007/S10021-008-9145-0
Qin B, Chen W, Hu W (2004) Succession of ecological environment and its mechanism in Lake Taihu (in Chinese). China Science Press, Beijing
Molinos-Senante M, Hernández-Sancho F, Sala-Garrido R, Garrido-Baserba M (2011) Economic feasibility study for phosphorus recovery processes. Ambio 40:408–416. https://doi.org/10.1007/s13280-010-0101-9
Huang L, Fang H, He G, Jiang H, Wang C (2016) Effects of internal loading on phosphorus distribution in the Taihu Lake driven by wind waves and lake currents. Environ Pollut 219:760–773. https://doi.org/10.1016/j.envpol.2016.07.049
Elser JJ, Marzolf ER, Goldman CR (1990) Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: a review and critique of experimental enrichments. Can J Fish Aquat Sci 47:1468–1477. https://doi.org/10.1139/f90-165
Wu L, Ge G, Gong S, Li S, Wan J (2012) Diversity and composition of the bacterial community of Poyang Lake (China) as determined by 16S rRNA gene sequence analysis. World J Microbiol Biotechnol 28:233–244. https://doi.org/10.1007/s11274-011-0812-5
Zeng J, Bian YQ, Xing P, Wu QL (2012) Macrophyte species drive the variation of bacterioplankton community composition in a shallow freshwater lake. Appl Environ Microbiol 78:177–184. https://doi.org/10.1128/AEM.05117-11
Su X, Steinman AD et al (2017) Response of bacterial communities to cyanobacterial harmful algal blooms in Lake Taihu, China. Harmful Algae 68:168–177. https://doi.org/10.1016/j.hal.2017.08.007
Kim B-R, Shin J et al (2017) Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol 27:2089–2093. https://doi.org/10.4014/jmb.1709.09027
Xing P, Guo L, Tian W, Wu QL (2010) Novel Clostridium populations involved in the anaerobic degradation of Microcystis blooms. ISME J 5:792–800. https://doi.org/10.1038/ismej.2010.176
Li J, Wang G et al (2017) Dynamic changes of bacterial community structure in the occurrence process of cyanobacterial bloom. J China Agric Univ 22:134–142. https://doi.org/10.11841/j.issn.1007-4333.2017.07.16
Zhou J, Deng Y et al (2014) Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proc Natl Acad Sci 111:836–845. https://doi.org/10.1073/pnas.1324044111
Zhou J, Liu W et al (2013) Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community. MBio 4:49–52. https://doi.org/10.1128/mBio.00584-12
Van der Plas F, Anderson TM, Olff H (2012) Trait similarity patterns within grass and grasshopper communities: multitrophic community assembly at work. Ecology 93:836–846. https://doi.org/10.1890/11-0975.1
Gerisch M, Dziock F (2012) More species, but all do the same: contrasting effects of flood disturbance on ground beetle functional and species diversity. Oikos 121:508–515. https://doi.org/10.1111/j.1600-0706.2011.19749.x
Chase JM (2010) Stochastic community assembly causes higher biodiversity in more productive environments. Science 328:1388–1391. https://doi.org/10.1126/science.1187820
Liu L, Yang J, Lv H, Yu Z (2014) Synchronous dynamics and correlations between bacteria and phytoplankton in a subtropical drinking water reservoir. FEMS Microbiol Ecol 90:126–138. https://doi.org/10.1111/1574-6941.12378
Berry MA, Davis TW et al (2017) Cyanobacterial harmful algal blooms are a biological disturbance to Western Lake Erie bacterial communities. Environ Microbiol 19:1149–1162. https://doi.org/10.1111/1462-2920.13640
Jiao C, Zhao D, Huang R, He F, Yu Z (2021) Habitats and seasons differentiate the assembly of bacterial communities along a trophic gradient of freshwater lakes. Freshw Biol 66:1515–1529. https://doi.org/10.1111/fwb.13735
Jiao C, Zhao D, Zeng J, Guo L, Yu Z (2020) Disentangling the seasonal co-occurrence patterns and ecological stochasticity of planktonic and benthic bacterial communities within multiple lakes. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2020.140010
Chaffron S, Rehrauer H, Pernthaler J, Mering CV (2010) A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Res 20:947–959. https://doi.org/10.1007/s002890050103
Tilman D (2007) Interespecific competition and multispecies coexistence. In: May RM, McLean A (eds) Theoretical ecology principles and applications. University Press, Oxford, pp 84–97
Li H, Xing P, Wu QL (2017) Genus-specific relationships between the phytoplankton and bacterioplankton communities in Lake Taihu, China. Hydrobiologia 795:281–294. https://doi.org/10.1007/s10750-017-3141-3
Cao X, Zhao D et al (2018) Heterogeneity of interactions of microbial communities in regions of Taihu Lake with different nutrient loadings: a network analysis. Sci Rep 8:1–11. https://doi.org/10.1038/s41598-018-27172-z
Newman MEJ (2006) Modularity and community structure in networks. Proc Natl Acad Sci 103:8577–8582. https://doi.org/10.1073/pnas.0601602103
Acknowledgements
We are especially grateful to Qinglong Wu for his experimental design of this study, Yujing Wang for her assistance in the sample collection and the measurement of physicochemical parameters. This work was supported by the National Natural Science Foundation of China (41871096, 32171563); the Natural Science Foundation of Jiangsu Province, China (BK20181311); the Fundamental Research Funds for the Central Universities (B210202009, B200203051); and the China Scholarship Council (No. 201906710009).
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This work was supported by the National Natural Science Foundation of China (41871096, 32171563); the Natural Science Foundation of Jiangsu Province, China (BK20181311); the Fundamental Research Funds for the Central Universities (B210202009, B200203051); and the China Scholarship Council (No. 201906710009).
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Conceptualization: DZ, XC; Methodology: LR, KF, XC; Formal analysis and investigation: XC, LR, KF; Writing—original draft preparation: XC, HZ; Writing—review and editing: XC, LR, KF, DZ, C:L; Funding acquisition: DZ; Supervision: DZ.
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Cao, X., Zhao, D., Li, C. et al. Regime transition Shapes the Composition, Assembly Processes, and Co-occurrence Pattern of Bacterioplankton Community in a Large Eutrophic Freshwater Lake. Microb Ecol 84, 336–350 (2022). https://doi.org/10.1007/s00248-021-01878-6
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DOI: https://doi.org/10.1007/s00248-021-01878-6