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Distinct community assembly processes underlie significant spatiotemporal dynamics of abundant and rare bacterioplankton in the Yangtze River

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Abstract

The rare microbial biosphere provides broad ecological services and resilience to various ecosystems. Nevertheless, the biogeographical patterns and assembly processes of rare bacterioplankton communities in large rivers remain uncertain. In this study, we investigated the biogeography and community assembly processes of abundant and rare bacterioplankton taxa in the Yangtze River (China) covering a distance of 4300 km. The results revealed similar spatiotemporal patterns of abundant taxa (AT) and rare taxa (RT) at both taxonomic and phylogenetic levels, and analysis of similarities revealed that RT was significantly influenced by season and landform than AT. Furthermore, RT correlated with more environmental factors than AT, whereas environmental and spatial factors explained a lower proportion of community shifts in RT than in AT. The steeper distance-decay slopes in AT indicated higher spatial turnover rates of abundant subcommunities than rare subcommunities. The null model revealed that both AT and RT were mainly governed by stochastic processes. However, dispersal limitation primarily governed the AT, whereas the undominated process accounted for a higher fraction of stochastic processes in RT. River flow and suspended solids mediated the balance between the stochastic and deterministic processes in RT. The spatiotemporal dynamics and assembly processes of total taxa were more similar as AT than RT. This study provides new insights into both significant spatiotemporal dynamics and inconsistent assembly processes of AT and RT in large rivers.

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References

  • Amir A, McDonald D, Navas-Molina J A, Kopylova E, Morton J T, Zech Xu Z, Kightley E P, Thompson L R, Hyde E R, Gonzalez A, Knight R (2017). Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems, 2(2): e00191–16

    Article  Google Scholar 

  • 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? Global Ecology and Biogeography, 21(3): 365–375

    Article  Google Scholar 

  • Aufdenkampe A K, Mayorga E, Raymond P A, Melack J M, Doney S C, Alin S R, Aalto R E, Yoo K (2011). Riverine coupling of biogeochemical cycles between land, oceans, and atmosphere. Frontiers in Ecology and the Environment, 9(1): 53–60

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B. Methodological, 57(1): 289–300

    Google Scholar 

  • Bokulich N A, Kaehler B D, Rideout J R, Dillon M, Bolyen E, Knight R, Huttley G A, Gregory Caporaso J (2018). Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome, 6(1): 90

    Article  Google Scholar 

  • Bolyen E, Rideout J R, Dillon M R, Bokulich N A, Abnet C C, Al-Ghalith G A, Alexander H, Alm E J, Arumugam M, Asnicar F et al. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37(8): 852–857

    Article  CAS  Google Scholar 

  • Caron D A, Countway P D (2009). Hypotheses on the role of the protistan rare biosphere in a changing world. Aquatic Microbial Ecology, 57: 227–238

    Article  Google Scholar 

  • Chen W, Ren K, Isabwe A, Chen H, Liu M, Yang J (2019). Stochastic processes shape microeukaryotic community assembly in a subtropical river across wet and dry seasons. Microbiome, 7(1): 138

    Article  Google Scholar 

  • Cottrell M T, David K L (2003). Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary. Limnology and Oceanography, 48(1): 168–178

    Article  Google Scholar 

  • Evans S, Martiny J B H, Allison S D (2017). Effects of dispersal and selection on stochastic assembly in microbial communities. ISME Journal, 11(1): 176–185

    Article  Google Scholar 

  • Falkowski P G, Fenchel T, Delong E F (2008). The microbial engines that drive earth’s biogeochemical cycles. Science, 320(5879): 1034–1039

    Article  CAS  Google Scholar 

  • Gao Q, Yang Y, Feng J, Tian R, Guo X, Ning D, Hale L, Wang M, Cheng J, Wu L, Zhao M, Zhao J, Wu L, Qin Y, Qi Q, Liang Y, Sun B, Chu H, Zhou J (2019). The spatial scale dependence of diazotrophic and bacterial community assembly in paddy soil. Global Ecology and Biogeography, 28: 1093–1105

    Google Scholar 

  • Gilbert B, Bennett J R (2010). Partitioning variation in ecological communities: Do the numbers add up? Journal of Applied Ecology, 47(5): 1071–1082

    Article  Google Scholar 

  • Guidi L, Chaffron S, Bittner L, Eveillard D, Larhlimi A, Roux S, Darzi Y, Audic S, Berline L, Brum J, Coelho L P, Espinoza J C I, Malviya S, Sunagawa S, Dimier C, Kandels-Lewis S, Picheral M, Poulain J, Searson S, Stemmann L, Not F, Hingamp P, Speich S, Follows M, Karp-Boss L, Boss E, Ogata H, Pesant S, Weissenbach J, Wincker P, Acinas S G, Bork P, de Vargas C, Iudicone D, Sullivan M B, Raes J, Karsenti E, Bowler C, Gorsky G, the Tara Oceans coordinators (2016). Plankton networks driving carbon export in the oligotrophic ocean. Nature, 532(7600): 465–470

    Article  CAS  Google Scholar 

  • Hanson C A, Fuhrman J A, Horner-Devine M C, Martiny J B H (2012). Beyond biogeographic patterns: Processes shaping the microbial landscape. Nature Reviews. Microbiology, 10(7): 497–506

    CAS  Google Scholar 

  • Horner-Devine M C, Bohannan B J M (2006). Phylogenetic clustering and overdispersion in bacterial communities. Ecology, 87(sp7): S100–S108

    Article  Google Scholar 

  • Jansson J K, Hofmockel K S (2020). Soil microbiomes and climate change. Nature Reviews. Microbiology, 18(1): 35–46

    CAS  Google Scholar 

  • Ji M, Kong W, Stegen J, Yue L, Wang F, Dong X, Cowan D A, Ferrari B C (2020). Distinct assembly mechanisms underlie similar biogeographical patterns of rare and abundant bacteria in Tibetan Plateau grassland soils. Environmental Microbiology, 22(6): 2261–2272

    Article  CAS  Google Scholar 

  • Jia X, Dini-Andreote F, Falcão Salles J (2018). Community assembly processes of the microbial rare biosphere. Trends in Microbiology, 26(9): 738–747

    Article  CAS  Google Scholar 

  • 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. Science of the Total Environment, 740: 140010

    Article  CAS  Google Scholar 

  • Jiao S, Lu Y (2020a). Abundant fungi adapt to broader environmental gradients than rare fungi in agricultural fields. Global Change Biology, 26(8): 4506–4520

    Article  Google Scholar 

  • Jiao S, Lu Y (2020b). Soil pH and temperature regulate assembly processes of abundant and rare bacterial communities in agricultural ecosystems. Environmental Microbiology, 22(3): 1052–1065

    Article  Google Scholar 

  • Katoh K, Standley D M (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4): 772–780

    Article  CAS  Google Scholar 

  • Kim T S, Jeong J Y, Wells G F, Park H D (2013). General and rare bacterial taxa demonstrating different temporal dynamic patterns in an activated sludge bioreactor. Applied Microbiology and Biotechnology, 97(4): 1755–1765

    Article  CAS  Google Scholar 

  • Leibold M A, Holyoak M, Mouquet N, Amarasekare P, Chase J M, Hoopes M F, Holt R D, Shurin J B, Law R, Tilman D, Loreau M, Gonzalez A (2004). The metacommunity concept: A framework for multi-scale community ecology. Ecology Letters, 7(7): 601–613

    Article  Google Scholar 

  • Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, Chaffron S, Ignacio-Espinosa J C, Roux S, Vincent F et al. (2015). Determinants of community structure in the global plankton interactome. Science, 348(6237): 1262073-1–1262073-9

    Article  Google Scholar 

  • Lindström E S, Langenheder S (2012). Local and regional factors influencing bacterial community assembly. Environmental Microbiology Reports, 4(1): 1–9

    Article  Google Scholar 

  • Liu S, Wang H, Chen L, Wang J, Zheng M, Liu S, Chen Q, Ni J (2020). Comammox Nitrospira within the Yangtze River continuum: Community, biogeography, and ecological drivers. ISME Journal, 14(10): 2488–2504

    Article  CAS  Google Scholar 

  • Liu T, Liu S, He S, Tian Z, Zheng M (2021). Minimization of N2O emission through intermittent aeration in a Sequencing Batch Reactor (SBR): main behavior and mechanism. Water, 13(2): 210

    Article  CAS  Google Scholar 

  • Liu T, Zhang A N, Wang J, Liu S, Jiang X, Dang C, Ma T, Liu S, Chen Q, Xie S, Zhang T, Ni J (2018). Integrated biogeography of planktonic and sedimentary bacterial communities in the Yangtze River. Microbiome, 6(1): 16

    Article  CAS  Google Scholar 

  • 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 Journal, 7(5): 937–948

    Article  CAS  Google Scholar 

  • Lynch M D J, Neufeld J D (2015). Ecology and exploration of the rare biosphere. Nature Reviews Microbiology, 13: 217–229

    Article  CAS  Google Scholar 

  • Ma B, Wang H, Dsouza M, Lou J, He Y, Dai Z, Brookes P C, Xu J, Gilbert J A (2016). Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. ISME Journal, 10: 1891–1901

    Article  CAS  Google Scholar 

  • Martiny J B H, Eisen J A, Penn K, Allison S D, Horner-Devine M C (2011). Drivers of bacterial β-diversity depend on spatial scale. Proceedings of the National Academy of Sciences of the United States of America, 108(19): 7850–7854

    Article  CAS  Google Scholar 

  • Mo Y, Zhang W, Yang J, Lin Y, Yu Z, Lin S (2018). Biogeographic patterns of abundant and rare bacterioplankton in three subtropical bays resulting from selective and neutral processes. ISME Journal, 12(9): 2198–2210

    Article  Google Scholar 

  • Nemergut D R, Schmidt S K, Fukami T, O’Neill S P, Bilinski T M, Stanish L F, Knelman J E, Darcy J L, Lynch R C, Wickey P, Ferrenberg S (2013). Patterns and processes of microbial community assembly. Microbiology and Molecular Biology Reviews, 77(3): 342–356

    Article  Google Scholar 

  • Ning D, Deng Y, Tiedje J M, Zhou J (2019). A general framework for quantitatively assessing ecological stochasticity. Proceedings of the National Academy of Sciences of the United States of America, 116(34): 16892–16898

    Article  CAS  Google Scholar 

  • Ning D, Yuan M, Wu L, Zhang Y, Guo X, Zhou X, Yang Y, Arkin A P, Firestone M K, Zhou J (2020). A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nature Communications, 11(1): 4717

    Article  CAS  Google Scholar 

  • Nyirabuhoro P, Liu M, Xiao P, Liu L, Yu Z, Wang L, Yang J (2020). Seasonal variability of conditionally rare taxa in the Water Column Bacterioplankton Community of Subtropical Reservoirs in China. Microbial Ecology, 80(1): 14–26

    Article  CAS  Google Scholar 

  • Payne J T, Millar J J, Jackson C R, Ochs C A (2017). Patterns of variation in diversity of the Mississippi River microbiome over 1300 kilometers. PLoS One, 12(3): e0174890

    Article  Google Scholar 

  • Pedrós-Alió C (2012). The rare bacterial biosphere. Annual Review of Marine Science, 4(1): 449–466

    Article  Google Scholar 

  • Peter H, Jeppesen E, De Meester L, Sommaruga R (2018). Changes in bacterioplankton community structure during early lake ontogeny resulting from the retreat of the Greenland Ice Sheet. ISME Journal, 12(2): 544–555

    Article  Google Scholar 

  • Price M N, Dehal P S, Arkin A P (2010). FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One, 5(3): e9490

    Article  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner F O (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(Database issue): D590–D596

    Article  CAS  Google Scholar 

  • Read D S, Gweon H S, Bowes M J, Newbold L K, Field D, Bailey M J, Griffiths R I (2015). Catchment-scale biogeography of riverine bacterioplankton. ISME Journal, 9(2): 516–526

    Article  CAS  Google Scholar 

  • Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016). VSEARCH: A versatile open source tool for metagenomics. PeerJ, 4: e2584

    Article  Google Scholar 

  • Savio D, Sinclair L, Ijaz U Z, Parajka J, Reischer G H, Stadler P, Blaschke A P, Blöschl G, Mach R L, Kirschner A K T, Farnleitner A H, Eiler A (2015). Bacterial diversity along a 2600 km river continuum. Environmental Microbiology, 17(12): 4994–5007

    Article  CAS  Google Scholar 

  • Shi Y, Li Y, Xiang X, Sun R, Yang T, He D, Zhang K, Ni Y, Zhu Y G, Adams J M, Chu H (2018). Spatial scale affects the relative role of stochasticity versus determinism in soil bacterial communities in wheat fields across the North China Plain. Microbiome, 6(1): 27

    Article  Google Scholar 

  • Smith T W, Lundholm J T (2010). Variation partitioning as a tool to distinguish between niche and neutral processes. Ecography, 33(4): 648–655

    Article  Google Scholar 

  • Sogin M L, Morrison H G, Huber J A, Welch D M, Huse S M, Neal P R, Arrieta J M, Herndl G J (2006). Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proceedings of the National Academy of Sciences of the United States of America, 103(32): 12115–12120

    Article  CAS  Google Scholar 

  • Staley C, Gould T J, Wang P, Phillips J, Cotner J B, Sadowsky M J (2015). Species sorting and seasonal dynamics primarily shape bacterial communities in the Upper Mississippi River. Science of the Total Environment, 505: 435–445

    Article  CAS  Google Scholar 

  • Stegen J C, Lin X, Fredrickson J K, Chen X, Kennedy D W, Murray C J, Rockhold M L, Konopka A (2013). Quantifying community assembly processes and identifying features that impose them. ISME Journal, 7(11): 2069–2079

    Article  Google Scholar 

  • Stegen J C, Lin X, Fredrickson J K, Konopka A E (2015). Estimating and mapping ecological processes influencing microbial community assembly. Frontiers in Microbiology, 6: 370

    Article  Google Scholar 

  • Stegen J C, Lin X, Konopka A E, Fredrickson J K (2012). Stochastic and deterministic assembly processes in subsurface microbial communities. ISME Journal, 6(9): 1653–1664

    Article  CAS  Google Scholar 

  • Sun L, Wang H, Kan Y, Wang S (2018). Distribution of phytoplankton community and its influence factors in an urban river network, East China. Frontiers of Environmental Science & Engineering, 12(6): 13

    Article  CAS  Google Scholar 

  • Sun W, Xia C, Xu M, Guo J, Sun G (2016). Application of modified water quality indices as indicators to assess the spatial and temporal trends of water quality in the Dongjiang River. Ecological Indicators, 66: 306–312

    Article  CAS  Google Scholar 

  • Tripathi B M, Stegen J C, Kim M, Dong K, Adams J M, Lee Y K (2018). Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME Journal, 12(4): 1072–1083

    Article  CAS  Google Scholar 

  • Vellend M (2010). Conceptual synthesis in community ecology. Quarterly Review of Biology, 85(2): 183–206

    Article  Google Scholar 

  • Wan W, Grossart H P, He D, Yuan W, Yang Y (2021a). Stronger environmental adaptation of rare rather than abundant bacterioplankton in response to dredging in eutrophic Lake Nanhu (Wuhan, China). Water Research, 190: 116751

    Article  CAS  Google Scholar 

  • Wan W, Liu S, Li X, Xing Y, Chen W, Huang Q (2021b). Bridging rare and abundant bacteria with ecosystem multifunctionality in salinized agricultural soils: from community diversity to environmental adaptation. mSystems, 6(2): e01221–20

    Article  CAS  Google Scholar 

  • Wang J, Shen J, Wu Y, Tu C, Soininen J, Stegen J C, He J, Liu X, Zhang L, Zhang E (2013). Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME Journal, 7(7): 1310–1321

    Article  CAS  Google Scholar 

  • Wang Y, Ye F, Wu S, Wu J, Yan J, Xu K, Hong Y (2020). Biogeographic pattern of bacterioplanktonic community and potential function in the Yangtze River: Roles of abundant and rare taxa. Science of the Total Environment, 747: 141335

    Article  CAS  Google Scholar 

  • Wei G, Li M, Li F, Li H, Gao Z (2016). Distinct distribution patterns of prokaryotes between sediment and water in the Yellow River estuary. Applied Microbiology and Biotechnology, 100(22): 9683–9697

    Article  CAS  Google Scholar 

  • Wu W, Logares R, Huang B, Hsieh C H (2017). Abundant and rare picoeukaryotic sub-communities present contrasting patterns in the epipelagic waters of marginal seas in the northwestern Pacific Ocean. Environmental Microbiology, 19(1): 287–300

    Article  CAS  Google Scholar 

  • Wu L W, Ning D, Zhang B, Li Y, Zhang P, Shan X, Zhang Qiuting, Brown M R, Li Z, Van Nostrand J D, Ling F, et al. (2019). Global diversity and biogeography of bacterial communities in wastewater treatment plants. Nature Microbiology, 4: 1183–1195

    Article  CAS  Google Scholar 

  • Zhang F, Zhang H, Yuan Y, Liu D, Zhu C, Zheng D, Li G, Wei Y, Sun D (2020). Different response of bacterial community to the changes of nutrients and pollutants in sediments from an urban river network. Frontiers of Environmental Science & Engineering, 14(2): 28

    Article  CAS  Google Scholar 

  • Zhang W, Pan Y, Yang J, Chen H, Holohan B, Vaudrey J, Lin S, McManus G B (2018). The diversity and biogeography of abundant and rare intertidal marine microeukaryotes explained by environment and dispersal limitation. Environmental Microbiology, 20(2): 462–476

    Article  CAS  Google Scholar 

  • Zhou J, Ning D (2017). Stochastic community assembly: Does it matter in microbial ecology? Microbiology and Molecular Biology Reviews, 81(4): e00002–e00017

    Article  Google Scholar 

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Acknowledgements

This work was supported by National Natural Science Foundation of China (Grant No. 41907203) and China Postdoctoral Science Foundation (2021T140010). Supports from High-performance Computing Platform of Peking University (China) and Majorbio Company (Shanghai, China) are acknowledged. The authors declared no competing financial interests.

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Correspondence to Tang Liu.

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Highlights

• Season and landform influenced spatiotemporal patterns of abundant and rare taxa.

• Different stochastic processes dominated abundant and rare subcommunity assembly.

• River flow and suspended solids regulated assembly processes of rare taxa.

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11783_2021_1513_MOESM1_ESM.pdf

Distinct community assembly processes underlie significant spatiotemporal dynamics of abundant and rare bacterioplankton in the Yangtze River

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Yi, M., Fang, Y., Hu, G. et al. Distinct community assembly processes underlie significant spatiotemporal dynamics of abundant and rare bacterioplankton in the Yangtze River. Front. Environ. Sci. Eng. 16, 79 (2022). https://doi.org/10.1007/s11783-021-1513-4

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