Soil phosphorus determines the distinct assembly strategies for abundant and rare bacterial communities during successional reforestation

Highlights

• Soil phosphorus shaped both abundant and rare bacterial communities.

• ŸBoth abundant and rare bacteria exhibited different assembly strategies with successional reforestation.

• Deterministic processes increased with succession reforestation.

Abstract

Uncovering the mechanisms underlying the diversity patterns of abundant and rare species is crucial for terrestrial biodiversity maintenance. However, the response of abundant and rare community assembly to ecological succession has not been explored, particularly considering soil profiles. Here 300 soil samples were collected from reforestation ecosystems from depths of up to 300 cm and horizontal distances of 30-90 cm from a tree. We revealed that soil phosphorus not only affected alpha diversity and community structure, but also mediated the balance of stochastic and deterministic processes for abundant and rare sub-communities, which exhibited contrasting assembly strategies. The abundant sub-community changed from variable selection to stochasticity with the increase of phosphorus, while the rare sub-community shifted from homogeneous selection to stochasticity. Dispersal limitation was the main assembly process in the abundant sub-community, while the rare sub-community was governed primarily by homogeneous selection. Moreover, the relative influence of deterministic processes increased with succession for both sub-communities. At the scale of a single tree, stochastic processes increased with soil depth in rare sub-community, while deterministic processes increased with the radius from a single tree in the abundant sub-community. Overall, our results highlight the importance of the soil phosphorus-driven assembly process in understanding the re-assembly and maintenance of soil bacterial diversity.

Graphical abstract

Keywords

Rare bacteria / Reforestation / Soil profiles / Community assembly / Soil phosphorus / Semi-arid

References

[1] Archer, E. 2016. rfPermute: Estimate permutation p-values for Random Forest importance metrics. R package version 1.

[2] Bao, S., 2000. Soil Agrochemical Analysis. China Agricultural Press, Beijing, 25–114.

[3] Barberán, A., Ramirez, K.S., Leff, J.W., Bradford, M.A., Wall, D.H., Fierer, N., 2014. Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria. Ecology Letters 17, 794–802

[4] Bardgett, R., 2005. The biology of soil: a community and ecosystem approach. Oxford university press.

[5] Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 48

[6] Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., Fierer, N., Knight, R., 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America 108, 4516–4522

[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] Cavender-Bares, J., Kozak, K.H., Fine, P.V.A., Kembel, S.W., 2009. The merging of community ecology and phylogenetic biology. Ecology Letters 12, 693–715

[9] Chang, C., HilleRisLambers, J., 2016. Integrating succession and community assembly perspectives. F1000 Research 5, 5

[10] Chang, C.C., Turner, B.L., 2019. Ecological succession in a changing world. Journal of Ecology 107, 503–509

[11] Chase, J.M., 2010. Stochastic community assembly causes higher biodiversity in more productive environments. Science 328, 1388–1391

[12] Chave, J., 2004. Neutral theory and community ecology. Ecology Letters 7, 241–253

[13] Chen, D., Saleem, M., Cheng, J., Mi, J., Chu, P., Tuvshintogtokh, I., Hu, S., Bai, Y., 2019a. Effects of aridity on soil microbial communities and functions across soil depths on the Mongolian Plateau. Functional Ecology 33, 1561–1571

[14] Chen, W., Jiao, S., Li, Q., Du, N., 2019b. Dispersal limitation relative to environmental filtering governs the vertical small-scale assembly of soil microbiomes during restoration. Journal of Applied Ecology 57, 402–412

[15] Chen, X., Daniell, T.J., Neilson, R., O’Flaherty, V., Griffiths, B.S., 2014. Microbial and microfaunal communities in phosphorus limited, grazed grassland change composition but maintain homeostatic nutrient stoichiometry. Soil Biology & Biochemistry 75, 94–101

[16] Chiquoine, L.P., Abella, S.R., Bowker, M.A., 2016. Rapidly restoring biological soil crusts and ecosystem functions in a severely disturbed desert ecosystem. Ecological Applications 26, 1260–1272

[17] Cleveland, C.C., Houlton, B.Z., Smith, W.K., Marklein, A.R., Reed, S.C., Parton, W., Del Grosso, S.J., Running, S.W., 2013. Patterns of new versus recycled primary production in the terrestrial biosphere. Proceedings of the National Academy of Sciences of the United States of America 110, 12733–12737

[18] Dai, Z., Liu, G., Chen, H., Chen, C., Wang, J., Ai, S., Wei, D., Li, D., Ma, B., Tang, C., Brookes, P.C., Xu, J., 2020. Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. ISME Journal 14, 757–770

[19] Delgado-Baquerizo, M., Maestre, F.T., Reich, P.B., Jeffries, T.C., Gaitan, J.J., Encinar, D., Berdugo, M., Campbell, C.D., Singh, B.K., 2016. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nature Communications 7, 10541

[20] Dini-Andreote, F., de Cássia Pereira e Silva, M., Triadó-Margarit, X., Casamayor, E.O., van Elsas, J.D., Salles, J.F., 2014. Dynamics of bacterial community succession in a salt marsh chronosequence: evidences for temporal niche partitioning. ISME Journal 8, 1989–2001

[21] Dini-Andreote, F., Stegen, J.C., van Elsas, J.D., Salles, J.F., 2015. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proceedings of the National Academy of Sciences of the United States of America 112, E1326–E1332

[22] Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27, 2194–2200

[23] Eilers, K.G., Debenport, S., Anderson, S., Fierer, N., 2012. Digging deeper to find unique microbial communities: The strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biology & Biochemistry 50, 58–65

[24] Evans, S., Martiny, J.B.H., Allison, S.D., 2017. Effects of dispersal and selection on stochastic assembly in microbial communities. ISME Journal 11, 176–185

[25] Fargione, J., Brown, C.S., Tilman, D., 2003. Community assembly and invasion: an experimental test of neutral versus niche processes. Proceedings of the National Academy of Sciences of the United States of America 100, 8916–8920

[26] Ferrenberg, S., O’Neill, S.P., Knelman, J.E., Todd, B., Duggan, S., Bradley, D., Robinson, T., Schmidt, S.K., Townsend, A.R., Williams, M.W., Cleveland, C.C., Melbourne, B.A., Jiang, L., Nemergut, D.R., 2013. Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME Journal 7, 1102–1111

[27] Fierer, N., Nemergut, D., Knight, R., Craine, J.M., 2010. Changes through time: integrating microorganisms into the study of succession. Research in Microbiology 161, 635–642

[28] Fierer, N., Schimel, J.P., Holden, P.A., 2003. Variations in microbial community composition through two soil depth profiles. Soil Biology & Biochemistry 35, 167–176

[29] Fukami, T., 2015. Historical contingency in community assembly: Integrating niches, species pools, and priority effects. Annual Review of Ecology, Evolution, and Systematics 46, 1–23

[30] Gao, G.F., Peng, D., Tripathi, B.M., Zhang, Y., Chu, H., 2020. Distinct community assembly processes of abundant and rare soil bacteria in coastal wetlands along an inundation gradient. mSystems 5, e01150–e01120

[31] Glassman, S.I., Wang, I.J., Bruns, T.D., 2017. Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales. Molecular Ecology 26, 6960–6973

[32] Goslee, S.C., Urban, D.L., 2007. The ecodist Package for Dissimilarity-based Analysis of Ecological Data. Journal of Statistical Software 22, 1–19

[33] Hartmann, M., Lee, S., Hallam, S.J., Mohn, W.W., 2009. Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. Environmental Microbiology 11, 3045–3062

[34] HilleRisLambers, J., Adler, P.B., Harpole, W.S., Levine, J.M., Mayfield, M.M., 2012. Rethinking Community Assembly through the Lens of Coexistence Theory. Annual Review of Ecology, Evolution, and Systematics 43, 227–248

[35] Hou, J., Wu, L., Liu, W., Ge, Y., Mu, T., Zhou, T., Li, Z., Zhou, J., Sun, X., Luo, Y., Christie, P., 2020. Biogeography and diversity patterns of abundant and rare bacterial communities in rice paddy soils across China. Science of the Total Environment 730, 139116

[36] Jangid, K., Whitman, W.B., Condron, L.M., Turner, B.L., Williams, M.A., 2013. Soil bacterial community succession during long-term ecosystem development. Molecular Ecology 22, 3415–3424

[37] Jiao, S., Chen, W., Wang, J., Du, N., Li, Q., Wei, G., 2018. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome 6, 146

[38] Jiao, S., Chen, W., Wei, G., 2017a. Biogeography and ecological diversity patterns of rare and abundant bacteria in oil-contaminated soils. Molecular Ecology 26, 5305–5317

[39] Jiao, S., Lu, Y., 2020. Abundant fungi adapt to broader environmental gradients than rare fungi in agricultural fields. Global Change Biology 26, 4506–4520

[40] Jiao, S., Lu, Y., 2020. Soil pH and temperature regulate assembly processes of abundant and rare bacterial communities in agricultural ecosystems. Environmental Microbiology 22, 1052–1065

[41] Jiao, S., Luo, Y., Lu, M., Xiao, X., Lin, Y., Chen, W., Wei, G., 2017b. Distinct succession patterns of abundant and rare bacteria in temporal microcosms with pollutants. Environmental Pollution 225, 497–505

[42] Jing, X., Sanders, N.J., Shi, Y., Chu, H., Classen, A.T., Zhao, K., Chen, L., Shi, Y., Jiang, Y., He, J.S., 2015. The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nature Communications 6, 8159

[43] Jousset, A., Bienhold, C., Chatzinotas, A., Gallien, L., Gobet, A., Kurm, V., Küsel, K., Rillig, M.C., Rivett, D.W., Salles, J.F., van der Heijden, M.G.A., Youssef, N.H., Zhang, X., Wei, Z., Hol, W.H.G., 2017. Where less may be more: how the rare biosphere pulls ecosystems strings. ISME Journal 11, 853–862

[44] Kembel, S.W., Cowan, P.D., Helmus, M.R., Cornwell, W.K., Morlon, H., Ackerly, D.D., Blomberg, S.P., Webb, C.O., 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics (Oxford, England) 26, 1463–1464

[45] Kuznetsova, A., Brockhoff, P.B., Christensen, R.H.B., 2017. lmerTest Package: Tests in linear mixed effects models. Journal of Statistical Software 82, 1–26

[46] Lennon, J.T., Jones, S.E., 2011. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nature Reviews. Microbiology 9, 119–130

[47] Li, X., Li, Y., Peng, S., Chen, Y., Cao, Y., 2019. Changes in soil phosphorus and its influencing factors following afforestation in Northern China. Land Degradation & Development 30, 1655–1666

[48] Liu, L., Yang, J., Yu, Z., Wilkinson, D.M., 2015. The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME Journal 9, 2068–2077

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

[50] Marschner, P., Yang, C.H., Lieberei, R., Crowley, D.E., 2001. Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biology & Biochemistry 33, 1437–1445

[51] 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, 2198–2210

[52] Monard, C., Gantner, S., Bertilsson, S., Hallin, S., Stenlid, J., 2016. Habitat generalists and specialists in microbial communities across a terrestrial-freshwater gradient. Scientific Reports 6, 37719

[53] Morriën, E., Hannula, S.E., Snoek, L.B., Helmsing, N.R., Zweers, H., de Hollander, M., Soto, R.L., Bouffaud, M.L., Buée, M., Dimmers, W., Duyts, H., Geisen, S., Girlanda, M., Griffiths, R.I., Jørgensen, H.B., Jensen, J., Plassart, P., Redecker, D., Schmelz, R.M., Schmidt, O., Thomson, B.C., Tisserant, E., Uroz, S., Winding, A., Bailey, M.J., Bonkowski, M., Faber, J.H., Martin, F., Lemanceau, P., de Boer, W., van Veen, J.A., van der Putten, W.H., 2017. Soil networks become more connected and take up more carbon as nature restoration progresses. Nature Communications 8, 14349

[54] Nacke, H., Goldmann, K., Schöning, I., Pfeiffer, B., Kaiser, K., Castillo-Villamizar, G.A., Schrumpf, M., Buscot, F., Daniel, R., Wubet, T., 2016. Fine spatial scale variation of soil microbial communities under European Beech and Norway Spruce. Frontiers in Microbiology 7, 2067

[55] 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, 342–356

[56] Oksanen, J.Blanchet, F. G.Kindt, R.Legendre, P.Minchin, P. R.O’hara, R. B. Simpson, G. L.Solymos, P.Stevens, M. H. H.and Wagner, H.. 2013. Package ‘vegan’. Community ecology package, version 2, 1–295.

[57] Ovaskainen, O., Tikhonov, G., Norberg, A., Guillaume Blanchet, F., Duan, L., Dunson, D., Roslin, T., Abrego, N., 2017. How to make more out of community data? A conceptual framework and its implementation as models and software. Ecology Letters 20, 561–576

[58] Pebesma, E., Heuvelink, G.J.R.J., 2016. Spatio-temporal interpolation using gstat. R Journal 8, 204–218

[59] Peng, L., Zhong, Z., Zhan-bin, L., 2004. Vertical root distribution characters of Robinia pseudoacacia on the Loess Plateau in China. Journal of Forestry Research 15, 87–92

[60] Pereira, A.P.A., Andrade, P.A.M., Bini, D., Durrer, A., Robin, A., Bouillet, J.P., Andreote, F.D., Cardoso, E.J.B.N., 2017. Shifts in the bacterial community composition along deep soil profiles in monospecific and mixed stands of Eucalyptus grandis and Acacia mangium. PLoS One 12, e0180371

[61] Prach, K., Walker, L.R., 2011. Four opportunities for studies of ecological succession. Trends in Ecology & Evolution 26, 119–123

[62] Randall, K., Brennan, F., Clipson, N., Creamer, R., Griffiths, B., Storey, S., Doyle, E., 2019. Soil bacterial community structure and functional responses across a long-term mineral phosphorus (Pi) fertilisation gradient differ in grazed and cut grasslands. Applied Soil Ecology 138, 134–143

[63] Rime, T., Hartmann, M., Brunner, I., Widmer, F., Zeyer, J., Frey, B., 2015. Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Molecular Ecology 24, 1091–1108

[64] Shi, S., Peng, C., Wang, M., Zhu, Q., Yang, G., Yang, Y., Xi, T., Zhang, T., 2016. A global meta-analysis of changes in soil carbon, nitrogen, phosphorus and sulfur, and stoichiometric shifts after forestation. Plant and Soil 407, 323–340

[65] 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, 27

[66] 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, 2069–2079

[67] Stegen, J.C., Lin, X., Konopka, A.E., Fredrickson, J.K., 2012. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME Journal 6, 1653–1664

[68] Thom, D., Seidl, R., 2016. Natural disturbance impacts on ecosystem services and biodiversity in temperate and boreal forests. Biological Reviews of the Cambridge Philosophical Society 91, 760–781

[69] 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, 1072–1083

[70] Vitousek, P.M., Porder, S., Houlton, B.Z., Chadwick, O.A., 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications 20, 5–15

[71] Walker, T.W., Adams, A.F.R., 1958. Studies on soil organic matter: I. Influence of phosphorus content of parent materials on accumulations of carbon, nitrogen, sulfur, and organic phosphorus in grassland soils. Soil Science 85, 307–318

[72] Wang, J., Wang, Y., Li, M., Xu, L., He, N., Yan, P., Chen, C., Lu, Q., Feng, Y., Li, J., 2021. Differential response of abundant and rare bacterial subcommunities to abiotic and biotic gradients across temperate deserts. Science of the Total Environment 763, 142942

[73] 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, 287–300

[74] Xue, Y., Chen, H., Yang, J.R., Liu, M., Huang, B., Yang, J., 2018. Distinct patterns and processes of abundant and rare eukaryotic plankton communities following a reservoir cyanobacterial bloom. ISME Journal 12, 2263–2277

[75] Zhang, C., Liu, G., Xue, S., Wang, G., 2016. Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biology & Biochemistry 97, 40–49

[76] Zhou, J., Deng, Y., Zhang, P., Xue, K., Liang, Y., Van Nostrand, J.D., Yang, Y., He, Z., Wu, L., Stahl, D.A., Hazen, T.C., Tiedje, J.M., Arkin, A.P., 2014. Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proceedings of the National Academy of Sciences of the United States of America 111, E836–E845

[77] Zhou, J., Ning, D., 2017. Stochastic Community Assembly: Does It Matter in Microbial Ecology? Microbiology and Molecular Biology Reviews 81, e00002–e00017

Author contributions

We are thankful to all authors for their help in this study. All authors contributed intellectual input and assistance to experiments and the manuscript preparation. Z.P. conducted the experiments, analyzed the data, and wrote the manuscript. G.W. and S.J. conceived and designed the experiments and revised the manuscript. Z.W., Y.L., M.Y., T,Y., M.C., and W.C. conducted field and laboratory work.

Acknowledgments

This work was supported by the National Science Foundation of China (Grant Nos.: 42077222, 41807030 and 41830755).

Conflict of interest

The authors have no conflicts of interest to declare.

Electronic supplementory material

Supplementary material is available in the online version of this article at http://doi.org/10.1007/s42832-021-0109-z and is accessible for authorized users.

RIGHTS & PERMISSIONS

2021 Higher Education Press