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

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.

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.

Graphical abstract

Keywords

Rare taxa / Biogeography / Community assembly / Bacterioplankton / The Yangtze River

References

[1] 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

[2] 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

[3] 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

[4] 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

[5] 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

[6] 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. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37(8): 852–857

[7] 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

[8] 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

[9] 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

[10] 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

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

[12] 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

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

[14] 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

[15] 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

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

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

[18] 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

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

[20] 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

[21] 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

[22] 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

[23] 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

[24] 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

[25] 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

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

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

[28] 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

[29] 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

[30] 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

[31] 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

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

[33] 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

[34] 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

[35] 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

[36] 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

[37] 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

[38] 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

[39] 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

[40] 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

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

[42] 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

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

[44] 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

[45] 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

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

[47] 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

[48] 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

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

[50] 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

[51] 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

[52] 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

[53] 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

[54] 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

[55] 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

[56] 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

[57] 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

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

[59] 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

[60] 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

[61] 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

[62] 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

[63] 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

[64] 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

[65] 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, . (2019). Global diversity and biogeography of bacterial communities in wastewater treatment plants. Nature Microbiology, 4: 1183–1195

[66] 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

[67] 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

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

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.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-021-1513-4 and is accessible for authorized users.

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