Threshold effects of soil pH regulate the biogeography of bacterial communities in inland wetlands across eastern China

Highlights

	● Distinct biogeographic patterns of bacterial abundant and rare taxa were detected.
	● Determinism governed bacterial community assemblages especially for abundant one.
	● Soil pH threshold effects imposed strong effects on shaping bacterial distribution.
	● Niche-based exclusion (overlap) of bacterial communities intensified at pH > 8.31.

Abstract

Biogeographic patterns of microbial communities in wetland soils at broad scales remain underexplored compared to those in well-drained soils, particularly regarding abundant and rare taxa. Here, we investigated the ecological distributions and assembly mechanisms of abundant and rare bacterial sub-communities and explored their underlying environmental drivers in inland wetland soils across eastern China. Both bacterial sub-communities exhibited significant distance-decay relationships (DDR), with a stronger DDR observed for abundant sub-communities due to more pronounced environmental filtering and dispersal limitation. Deterministic processes predominantly governed bacterial communities (62%‒97%), while stochasticity played a larger role in rare sub-communities (38%) compared to abundant ones (4.0%). Soil pH emerged as a dominant factor influencing bacterial communities and mediated the assembly of both sub-communities. The diversity of overall and rare taxa increased with pH and peaked at pH of 8.31, followed by an abrupt decline, suggesting a threshold effect on their ecological distributions. When pH exceeded 8.31, bacterial communities rapidly converged to more deterministic assemblages (especially for abundant taxa), with decreased species coexistence and increased negative cohesion (i.e., reflecting the degree of competition), suggesting intensified niche-based exclusion among bacterial communities. Collectively, this broad-scale study provides new insights into pH-related rules governing wetland bacterial biospheres and underscores the distinct biogeographic patterns between abundant and rare bacteria. The abrupt threshold of soil bacteria identified can inform effective adaptation and conservation efforts to sustain wetland ecosystem functioning.

Graphical abstract

Keywords

pH threshold / microbial biogeography / community assembly / deterministic process / rare biosphere

References

[1] An, J.X., Liu, C., Wang, Q., Yao, M.J., Rui, J.P., Zhang, S.H., Li, X.Z., 2019. Soil bacterial community structure in Chinese wetlands. Geoderma337, 290–299.

[2] Bahram, M., Hildebrand, F., Forslund, S.K., Anderson, J.L., Soudzilovskaia, N.A., Bodegom, P.M., Bengtsson-Palme, J., Anslan, S., Coelho, L.P., Harend, H., Huerta-Cepas, J., Medema, M.H., Maltz, M.R., Mundra, S., Olsson, P.A., Pent, M., Põlme, S., Sunagawa, S., Ryberg, M., Tedersoo, L., Bork, P., 2018. Structure and function of the global topsoil microbiome. Nature560, 233–237.

[3] Baker, M.E., King, R.S., 2010. A new method for detecting and interpreting biodiversity and ecological community thresholds. Methods in Ecology and Evolution1, 25–37.

[4] Bell, G., 2001. Neutral macroecology. Science293, 2413–2418.

[5] Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods,7, 335–336.

[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 America108, 4516–4522.

[7] Chen, B.B., Jiao, S., Luo, S.W., Ma, B.B., Qi, W., Cao, C.D., Zhao, Z.G., Du, G.Z., Ma, X.J., 2021. High soil pH enhances the network interactions among bacterial and archaeal microbiota in alpine grasslands of the Tibetan Plateau. Environmental Microbiology23, 464–477.

[8] Chen, W.D., Ren, K.X., Isabwe, A., Chen, H.H., Liu, M., Yang, J., 2019. Stochastic processes shape microeukaryotic community assembly in a subtropical river across wet and dry seasons. Microbiome7, 138.

[9] Chesson, P., 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology, Evolution, and Systematics31, 343–366.

[10] Dray, S., Bauman, D., Blanchet, G., Borcard, D., Clappe, S., Guenard, G., Jombart, T., Larocque, G., Legendre, P., Madi, N., Wagner, H.H., Siberchicot, A., 2020. adespatial: multivariate multiscale spatial analysis [Online]. available at the website of The Comprehensive R Archive Network.

[11] Edgar, R.C., 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods10, 996–998.

[12] Fan, K.K., Weisenhorn, P., Gilbert, J.A., Shi, Y., Bai, Y., Chu, H.Y., 2018. Soil pH correlates with the co-occurrence and assemblage process of diazotrophic communities in rhizosphere and bulk soils of wheat fields. Soil Biology and Biochemistry121, 185–192.

[13] 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 America100, 8916–8920.

[14] Feng, K., Zhang, Y.G., He, Z.L., Ning, D.L., Deng, Y., 2019. Interdomain ecological networks between plants and microbes. Molecular Ecology Resources19, 1565–1577.

[15] Feng, Y.Z., Zhang, J.W., Berdugo, M., Guirado, E., Guerra, C.A., Egidi, E., Wang, J.T., Singh, B.K., Delgado-Baquerizo, M., 2022. Temperature thresholds drive the global distribution of soil fungal decomposers. Global Change Biology28, 2779–2789.

[16] Fierer, N., 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nature Reviews Microbiology15, 579–590.

[17] Fierer, N., Jackson, R.B., 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America103, 626–631.

[18] Gao, G.F., Peng, D., Zhang, Y.H., Li, Y.T., Fan, K.K., Tripathi, B.M., Adams, J.M., Chu, H.Y., 2021. Dramatic change of bacterial assembly process and co-occurrence pattern in Spartina alterniflora salt marsh along an inundation frequency gradient. Science of the Total Environment755, 142546.

[19] Guo, J.J., Ling, N., Chen, Z.J., Xue, C., Li, L., Liu, L.S., Gao, L.M., Wang, M., Ruan, J.Y., Guo, S.W., Vandenkoornhuyse, P., Shen, Q.R., 2020. Soil fungal assemblage complexity is dependent on soil fertility and dominated by deterministic processes. New Phytologist226, 232–243.

[20] Herren, C.M., McMahon, K.D., 2017. Cohesion: a method for quantifying the connectivity of microbial communities. The ISME Journal11, 2426–2438.

[21] Hou, J.Y., Wu, L.H., Liu, W.X, Ge, Y.Y., Mu, T.T., Zhou, T., Li, Z., Zhou, J.W., Sun, X., Luo, Y.M., Christie, P., 2020. Biogeography and diversity patterns of abundant and rare bacterial communities in rice paddy soils across China. Science of the Total Environment730, 139116.

[22] Huang, H.Y., 2021. linkET: everything is linkable. R package version 0.0.3 [Online]. available at the website of Github.

[23] Ji, M.K., Kong, W.D., Stegen, J., Yue, L.Y., Wang, F., Dong, X.B., 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 Microbiology22, 2261–2272.

[24] Jia, X., Dini-Andreote, F., Falcão Salles, J., 2018. Community assembly processes of the microbial rare biosphere. Trends in Microbiology26, 738–747.

[25] Jiao, S., Chen, W.M., Wei, G.H., 2017. Biogeography and ecological diversity patterns of rare and abundant bacteria in oil-contaminated soils. Molecular Ecology26, 5305–5317.

[26] Jiao, S., Lu, Y.H., 2020. Soil pH and temperature regulate assembly processes of abundant and rare bacterial communities in agricultural ecosystems. Environmental Microbiology22, 1052–1065.

[27] Jiao, S., Lu, Y.H., Wei, G.H., 2022. Soil multitrophic network complexity enhances the link between biodiversity and multifunctionality in agricultural systems. Global Change Biology28, 140–153.

[28] Jurburg, S.D., Natal-da-Luz, T., Raimundo, J., Morais, P.V., Sousa, J.P., van Elsas, J.D., Salles, J.F., 2018. Bacterial communities in soil become sensitive to drought under intensive grazing. Science of the Total Environment618, 1638–1646.

[29] Kassambara, A., 2023. ggpubr: ‘ggplot2’ based publication ready plots. R package version 0.6.0 [Online].available at the website ofThe Comprehensive R Archive Network.

[30] Kerfahi, D., Dong, K., Tripathi, B., Adams, J.M., 2024. Global comparison shows that soil bacterial communities in extreme pH soils are more structured by deterministic processes. Science of the Total Environment942, 173662.

[31] King, A.J., Freeman, K.R., McCormick, K.F., Lynch, R.C., Lozupone, C., Knight, R., Schmidt, S.K., 2010. Biogeography and habitat modelling of high-alpine bacteria. Nature Communications1, 53.

[32] Kou, Y.P., Wei, K., Li, C.N., Wang, Y.S., Tu, B., Wang, J.M., Li, X.Z., Yao, M.J., 2020. Deterministic processes dominate soil methanotrophic community assembly in grassland soils. Geoderma359, 114004.

[33] Krulwich, T.A., Sachs, G., Padan, E., 2011. Molecular aspects of bacterial pH sensing and homeostasis. Nature Reviews Microbiology9, 330–343.

[34] Lai, J.S., Zou, Y., Zhang, J.L., Peres‐Neto, P.R., 2022. Generalizing hierarchical and variation partitioning in multiple regression and canonical analyses using the rdacca. hp R package. Methods in Ecology and Evolution13, 782–788.

[35] Lauber, C.L., Hamady, M., Knight, R., Fierer, N., 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and Environmental Microbiology75, 5111–5120.

[36] Li, W.T., Kuzyakov, Y., Zheng, Y.L., Li, P.F., Li, G.L., Liu, M., Alharbi, H.A., Li, Z.P., 2022. Depth effects on bacterial community assembly processes in paddy soils. Soil Biology and Biochemistry165, 108517.

[37] Liang, Y.T., Xiao, X., Nuccio, E.E., Yuan, M.T., Zhang, N., Xue, K., Cohan, F.M., Zhou, J.Z., Sun, B., 2020. Differentiation strategies of soil rare and abundant microbial taxa in response to changing climatic regimes. Environmental Microbiology22, 1327–1340.

[38] Liu, L.M., Yang, J., Yu, Z., Wilkinson, D.M., 2015. The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. The ISME Journal9, 2068–2077.

[39] Liu, X., Zhang, L., Wang, Y.C., Hu, S., Zhang, J., Huang, X.L., Li, R.W., Hu, Y.X., Yao, H.Y., Wang, Z., 2024a. Microbiome analysis in Asia’s largest watershed reveals inconsistent biogeographic pattern and microbial assembly mechanisms in river and lake systems. iScience27, 110053.

[40] Liu, Z.H., Fang, J., He, Y.C., Bending, G.D., Song, B., Guo, Y.P., Wang, X.J., Fang, Z.M., Adams, J.M., 2024b. Distinct biogeographic patterns in Glomeromycotinian and Mucoromycotinian arbuscular mycorrhizal fungi across China: a meta-analysis. Science of the Total Environment912, 168907.

[41] Liu, Z.H., Fang, J., Song, B., Yang, Y., Yu, Z., Hu, J.L., Dong, K., Takahashi, K., Adams, J.M., 2023. Stochastic processes dominate soil arbuscular mycorrhizal fungal community assembly along an elevation gradient in central Japan. Science of the Total Environment855, 158941.

[42] Lozupone, C.A., Knight, R., 2007. Global patterns in bacterial diversity. Proceedings of the National Academy of Sciences of the United States of America104, 11436–11440.

[43] Luan, L., Shi, G.P., Zhu, G.F., Zheng, J., Fan, J.B., Dini-Andreote, F., Sun, B., Jiang, Y.J., 2023. Biogeographical patterns of abundant and rare bacterial biospheres in paddy soils across East Asia. Environmental Microbiology25, 294–305.

[44] Ma, B., Wang, Y.L., Ye, S.D., Liu, S., Stirling, E., Gilbert, J.A., Faust, K., Knight, R., Jansson, J.K., Cardona, C., Röttjers, L., Xu, J.M., 2020. Earth microbial co-occurrence network reveals interconnection pattern across microbiomes. Microbiome8, 82.

[45] Meng, W.Q., Feagin, R.A., Hu, B.B., He, M.X., Li, H.Y., 2019. The spatial distribution of blue carbon in the coastal wetlands of China. Estuarine, Coastal and Shelf Science222, 13–20.

[46] Meng, W.Q., He, M.X., Hu, B.B., Mo, X.Q., Li, H.Y., Liu, B.Q., Wang, Z.L., 2017. Status of wetlands in China: a review of extent, degradation, issues and recommendations for improvement. Ocean & Coastal Management146, 50–59.

[47] Muggeo, V.M.R., 2008. Segmented: an R package to fit regression models with broken-line relationships. R News8, 20–25.

[48] Ni, Y.Y., Yang, T., Ma, Y.Y., Zhang, K.P., Soltis, P.S., Soltis, D.E., Gilbert, J.A., Zhao, Y.P., Fu, C.X., Chu, H.Y., 2021. Soil pH determines bacterial distribution and assembly processes in natural mountain forests of Eastern China. Global Ecology and Biogeography30, 2164–2177.

[49] Ning, D.L., Deng, Y., Tiedje, J.M., Zhou, J.Z., 2019. A general framework for quantitatively assessing ecological stochasticity. Proceedings of the National Academy of Sciences of the United States of America116, 16892–16898.

[50] Pedrós-Alió, C., 2006. Marine microbial diversity: can it be determined? Trends in Microbiology 14, 257–263.

[51] Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glockner, F.O., 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research41, D590–D596.

[52] Shen, X.J., Jiang, M., Lu, X.G., Thompson, J.R., 2024. Protect and restore small wetlands. Science384, 1415–1415.

[53] Shi, Y., Li, Y.T., Yang, T., Chu, H.Y., 2021. Threshold effects of soil pH on microbial co-occurrence structure in acidic and alkaline arable lands. Science of the Total Environment800, 149592.

[54] ter Horst, A.M., Fudyma, J.D., Sones, J.L., Emerson, J.B., 2023. Dispersal, habitat filtering, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography. The ISME Journal17, 2079–2089.

[55] 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. The ISME Journal12, 1072–1083.

[56] Villarino, E., Watson, J.R., Jönsson, B., Gasol, J.M., Salazar, G., Acinas, S.G., Estrada, M., Massana, R., Logares, R., Giner, C.R., Pernice, M.C., Olivar, M.P., Citores, L., Corell, J., Rodríguez-Ezpeleta, N., Acuña, J.L., Molina-Ramírez, A., González-Gordillo, J.I., Cózar, A., Martí, E., Cuesta, J.A., Agustí, S., Fraile-Nuez, E., Duarte, C.M., Irigoien, X., Chust, G., 2018. Large-scale ocean connectivity and planktonic body size. Nature Communications9, 142.

[57] Wagg, C., Schlaeppi, K., Banerjee, S., Kuramae, E.E., van der Heijden, M.G.A., 2019. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nature Communications10, 4841.

[58] Wang, B., Chen, C., Xiao, Y.M., Chen, K.Y., Wang, J., Zhou, G.Y., 2023. Temperature thresholds drive the biogeographic pattern of root endophytic fungal diversity in the Qinghai-Tibet Plateau. Science of the Total Environment889, 164270.

[59] Wang, J.M., Li, M.X., Li, J.W., 2021. Soil pH and moisture govern the assembly processes of abundant and rare bacterial communities in a dryland montane forest. Environmental Microbiology Reports13, 862–870.

[60] Wang, Y.S., Li, C.N., Kou, Y.P., Wang, J.J., Tu, B., Li, H., Li, X.Z., Wang, C.T., Yao, M.J., 2017. Soil pH is a major driver of soil diazotrophic community assembly in Qinghai-Tibet alpine meadows. Soil Biology and Biochemistry115, 547–555.

[61] Wu, H., Yang, J.J., Fu, W., Rillig, M.C., Cao, Z.J., Zhao, A.H., Hao, Z.P., Zhang, X., Chen, B.D., Han, X.G., 2023. Identifying thresholds of nitrogen enrichment for substantial shifts in arbuscular mycorrhizal fungal community metrics in a temperate grassland of Northern China. New Phytologist237, 279–294.

[62] Xiao, D.R., Deng, L., Kim, D.G., Huang, C.B., Tian, K., 2019. Carbon budgets of wetland ecosystems in China. Global Change Biology25, 2061–2076.

[63] Xun, W.B., Li, W., Xiong, W., Ren, Y., Liu, Y.P., Miao, Y.Z., Xu, Z.H., Zhang, N., Shen, Q.R., Zhang, R.F., 2019. Diversity-triggered deterministic bacterial assembly constrains community functions. Nature Communications10, 3833.

[64] Yang, W., Jeelani, N., Zhu, Z.H., Luo, Y.Q., Cheng, X.L., An, S.Q., 2019. Alterations in soil bacterial community in relation to Spartina alterniflora Loisel. invasion chronosequence in the Eastern Chinese coastal wetlands. Applied Soil Ecology135, 38–43.

[65] Yang, Y., Shi, Y., Fang, J., Chu, H.Y., Adams, J.M., 2022. Soil microbial network complexity varies with pH as a continuum, not a threshold, across the North China Plain. Frontiers in Microbiology13, 895687.

[66] Yuan, M.M., Guo, X., Wu, L.W., Zhang, Y., Xiao, N.J., Ning, D.L., Shi, Z., Zhou, X.S., Wu, L.Y., Yang, Y.F., Tiedje, J.M., Zhou, J.Z., 2021. Climate warming enhances microbial network complexity and stability. Nature Climate Change11, 343–348.

[67] Zhang, Q., Han, Y.L., Chen, W.Q., Guo, Y.L., Wu, M.Y., Wang, Y.L., Li, H., 2022. Soil type and pH mediated arable soil bacterial compositional variation across geographic distance in North China Plain. Applied Soil Ecology169, 104220.

[68] Zhou, J., Song, X., Zhang, C.Y., Chen, G.F., Lao, Y.M., Jin, H., Cai, Z.H., 2018. Distribution patterns of microbial community structure along a 7000-mile latitudinal transect from the Mediterranean Sea across the Atlantic Ocean to the Brazilian Coastal Sea. Microbial Ecology76, 592–609.

[69] Zhou, X.G., Rahman, M.K.U., Liu, J.J., Wu, F.Z., 2021. Soil acidification mediates changes in soil bacterial community assembly processes in response to agricultural intensification. Environmental Microbiology23, 4741–4755.

[70] Zhou, Z.B., Zhang, Y.J., Zhang, F.G., 2022. Abundant and rare bacteria possess different diversity and function in crop monoculture and rotation systems across regional farmland. Soil Biology and Biochemistry171, 108742.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant No. 32372058), Provincial Policy Guidance Program‒Jiangsu “100 Foreign Experts Program” (Grant No. SBX2020010098) and Jiangsu Agricultural Biodiversity Cultivation and Utilization Research Center (Grant No. 0270756100ZX).

CRediT authorship contribution statement

Jie Fang: Methodology, Formal analysis, Visualization, Writing -original draft. Zihao Liu: Conceptualization, Methodology, Visualization, Writing‒original draft. Yongcui Deng: Investigation, Writing‒review & editing. Bin Song: Conceptualization, Writing‒ review &editing. Xiangzhen Li: Resources, Investigation. Jonathan M. Adams: Conceptualization, Supervision, Funding acquisition, Writing‒review & editing.

Declaration of competing interest

The authors have no relevant financial or non-financial interests to disclose.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-024-0274-y and is accessible for authorized users.

RIGHTS & PERMISSIONS

2024 Higher Education Press