
Microbial diversity loss and plant genotype modulates rhizosphere microbial β-diversity to constrain soil functioning
Luyao Lai, Chuanfa Wu, Haoqing Zhang, Zhenke Zhu, Jian Yang, Yakov Kuzyakov, Jianpin Chen, Tida Ge
Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (3) : 250308.
Microbial diversity loss and plant genotype modulates rhizosphere microbial β-diversity to constrain soil functioning
● β-diversity (community structure) of bacterial and fungal communities is a stronger predictor of ecosystem functions. | |
● Plant genotypes regulate the relationship between microbial diversity and ecosystem functions, with a significant link in different wheat genotypes. | |
● Biodiversity loss influenced the enrichment of keystone taxa ( Burkholderia and Altemaria ), which are related to specialized functions and crucial for network cohesion. |
Soil microbial alpha diversity is essential for driving ecosystem functions and processes. However, little is known about the beta-diversity affect community functions. Here, we combine distinct community inocula using the dilution-to-extinction approach with two wheat genotypes to study the effect of microbial diversity loss on rhizosphere community assembly processes, which are related to beta-diversity (between-habitat diversity), and the consequences for ecosystem functions within greenhouse experiment. Compared with alpha-diversity, the bacterial and fungal community beta-diversity are stronger predictors of ecosystem functions (organic matter degradation, phosphorus supply capacity and nitrogen supply capacity), plant genotypes regulated the relationship between microbial diversity and ecosystem functions, with ecosystem functions being significant link to microbial diversity under different wheat genotypes. Loss of microbial diversity decreased the abundance of Bacterial_ASV6 (Burkholderia) and increased Fungal_11 (Altemaria) within the restored rhizosphere soil. Null modeling analysis showed that the deterministic assembly processes are dominant in bacterial community and fungal high-diversity (alpha-diversity) community, associating with the change of specialized functions (organic matter degradation, phosphorus supply capacity and nitrogen supply capacity) that are correlated with microbial diversity and specific microbial taxa. In addition, these two species were key role for regulating to the network cohesion. Overall, our study pointed out that the regulation of community assembly by microbial diversity loss limits the development of soil ecological functions and weakens the stability of rhizosphere microbial network, highlighting the potential regulatory effect of microbial taxa distribution on microbial community stability and changes of specific ecological functions.
microbial diversity loss / community assembly / rhizosphere microbes / soil functions / plant genotype
[1] |
Alori, E.T., Dare, M.O., Babalola, O.O., 2017. Microbial inoculants for soil quality and plant health, In: Lichtfouse, E., ed. Sustainable Agriculture Reviews. Cham: Springer281–307.
CrossRef
Google scholar
|
[2] |
Badri, D.V., Vivanco, J.M., 2009. Regulation and function of root exudates. Plant, Cell & Environment32, 666–681.
CrossRef
Google scholar
|
[3] |
Chen, G., Zhu, H.L., Zhang, Y., 2003. Soil microbial activities and carbon and nitrogen fixation. Research in Microbiology154, 393–398.
CrossRef
Google scholar
|
[4] |
Chen, Q.L., Ding, J., Zhu, Y.G., He, J.Z., Hu, H.W., 2020. Soil bacterial taxonomic diversity is critical to maintaining the plant productivity. Environment International140, 105766.
CrossRef
Google scholar
|
[5] |
Collado, J., Platas, G., Paulus, B., Bills, G.F., 2007. High-throughput culturing of fungi from plant litter by a dilution-to-extinction technique. FEMS Microbiology Ecology60, 521–533.
CrossRef
Google scholar
|
[6] |
Coyte, K.Z., Schluter, J., Foster, K.R., 2015. The ecology of the microbiome: networks, competition, and stability. Science350, 663–666.
CrossRef
Google scholar
|
[7] |
Dai, Z.M., Su, W.Q., Chen, H.H., Barberán, A., Zhao, H.C., Yu, M.J., Yu, L., Brookes, P.C., Schadt, C.W., Chang, S.X., Xu, J.M., 2018. Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agro-ecosystems across the globe. Global Change Biology24, 3452–3461.
CrossRef
Google scholar
|
[8] |
Djemiel, C., Dequiedt, S., Karimi, B., Cottin, A., Horrigue, W., Bailly, A., Boutaleb, A., Sadet-Bourgeteau, S., Maron, P.A., Chemidlin Prévost-Bouré, N., Ranjard, L., Terrat, S., 2022. Potential of meta-omics to provide modern microbial indicators for monitoring soil quality and securing food production. Frontiers in Microbiology13, 889788.
CrossRef
Google scholar
|
[9] |
Duan, C.W., Li, X.L., Li, C.Y., Yang, P.N., Chai, Y., Xu, W.Y., 2023a. Positive effects of fungal β diversity on soil multifunctionality mediated by pH in the natural restoration succession stages of alpine meadow patches. Ecological Indicators148, 110122.
CrossRef
Google scholar
|
[10] |
Duan, P.P., Fu, R.T., Nottingham, A.T., Domeignoz-Horta, L.A., Yang, X.Y., Du, H., Wang, K.L., Li, D.J., 2023b. Tree species diversity increases soil microbial carbon use efficiency in a subtropical forest. Global Change Biology29, 7131–7144.
CrossRef
Google scholar
|
[11] |
Eskelinen, A., Stark, S., Männistö, M., 2009. Links between plant community composition, soil organic matter quality and microbial communities in contrasting tundra habitats. Oecologia161, 113–123.
CrossRef
Google scholar
|
[12] |
Fernandez, C.W., Mielke, L., Stefanski, A., Bermudez, R., Hobbie, S.E., Montgomery, R.A., Reich, P.B., Kennedy, P.G., 2023. Climate change–induced stress disrupts ectomycorrhizal interaction networks at the boreal–temperate ecotone. Proceedings of the National Academy of Sciences of the United States of America120, e2221619120.
CrossRef
Google scholar
|
[13] |
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.
CrossRef
Google scholar
|
[14] |
Gan, D.Y., Zeng, H., Zhu, B., 2022. The rhizosphere effect on soil gross nitrogen mineralization: a meta-analysis. Soil Ecology Letters4, 144–154.
CrossRef
Google scholar
|
[15] |
Gotelli, N.J., 2000. Null model analysis of species co-occurrence patterns. Ecology81, 2606–2621.
CrossRef
Google scholar
|
[16] |
Hartmann, M., Frey, B., Mayer, J., Mäder, P., Widmer, F., 2015. Distinct soil microbial diversity under long-term organic and conventional farming. The ISME Journal9, 1177–1194.
CrossRef
Google scholar
|
[17] |
Hayat, R., Ali, S., Amara, U., Khalid, R., Ahmed, I., 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology60, 579–598.
CrossRef
Google scholar
|
[18] |
Hayatsu, M., Tago, K., Saito, M., 2008. Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Science and Plant Nutrition54, 33–45.
CrossRef
Google scholar
|
[19] |
Hernandez, D.J., David, A.S., Menges, E.S., Searcy, C.A., Afkhami, M.E., 2021. Environmental stress destabilizes microbial networks. The ISME Journal15, 1722–1734.
CrossRef
Google scholar
|
[20] |
Herren, C.M., McMahon, K.D., 2017. Cohesion: a method for quantifying the connectivity of microbial communities. The ISME Journal11, 2426–2438.
CrossRef
Google scholar
|
[21] |
Huet, S., Romdhane, S., Breuil, M.C., Bru, D., Mounier, A., Spor, A., Philippot, L., 2023. Experimental community coalescence sheds light on microbial interactions in soil and restores impaired functions. Microbiome11, 42.
CrossRef
Google scholar
|
[22] |
Hussain, S., Siddique, T., Saleem, M., Arshad, M., Khalid, A., 2009. Impact of pesticides on soil microbial diversity, enzymes, and biochemical reactions. Advances in Agronomy102, 159–200.
CrossRef
Google scholar
|
[23] |
IUSS Working Group WRB, 2006. World reference base for soil resources 2006: a framework for international classification, correlation and communication. Rome: FAO, 145.
|
[24] |
Jing, X., Classen, A.T., Li, D.J., Lin, L.T., Lu, M.Z., Sanders, N.J., Wang, Y.G., Feng, W.T., 2024. Unraveling microbial community structure–function relationships in the horizontal and vertical spatial dimensions in extreme environments. Ecography2024, e07118.
CrossRef
Google scholar
|
[25] |
Karimi, B., Maron, P.A., Chemidlin-Prevost Boure, N., Bernard, N., Gilbert, D., Ranjard, L., 2017. Microbial diversity and ecological networks as indicators of environmental quality. Environmental Chemistry Letters15, 265–281.
CrossRef
Google scholar
|
[26] |
Kowalchuk, G.A., Stephen, J.R., 2001. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annual Review of Microbiology55, 485–529.
CrossRef
Google scholar
|
[27] |
Lavecchia, A., Curci, M., Jangid, K., Whitman, W.B., Ricciuti, P., Pascazio, S., Crecchio, C., 2015. Microbial 16S gene-based composition of a sorghum cropped rhizosphere soil under different fertilization managements. Biology and Fertility of Soils51, 661–672.
CrossRef
Google scholar
|
[28] |
Li, J.W., Dong, L.B., Liu, Y.L., Wu, J.Z., Wang, J., Shangguan, Z.P., Deng, L., 2022a. Soil organic carbon variation determined by biogeographic patterns of microbial carbon and nutrient limitations across a 3,000-km humidity gradient in China. CATENA209, 105849.
CrossRef
Google scholar
|
[29] |
Li, P., Wu, G.G., Li, Y.J., Hu, C., Ge, L., Zheng, X.Q., Zhang, J.Q., Chen, J., Zhang, H.L., Bai, N.L., Zhang, H.Y., Song, L.L., Sun, Y., Jiang, W., Jia, J.W., Chen, Y.F., Wang, C., Lv, B.B., Wu, X., Pan, A.H., Li, S.X., Lv, W.G., 2022b. Long-term rice-crayfish-turtle co-culture maintains high crop yields by improving soil health and increasing soil microbial community stability. Geoderma413, 115745.
CrossRef
Google scholar
|
[30] |
Liaw, A., Wiener, M., 2002. Classification and Regression by randomForest. R News2, 18–22.
|
[31] |
Luo, J.P., Liao, G.C., Banerjee, S., Gu, S.H., Liang, J.B., Guo, X.Y., Zhao, H.P., Liang, Y.C., Li, T.Q., 2023. Long-term organic fertilization promotes the resilience of soil multifunctionality driven by bacterial communities. Soil Biology and Biochemistry177, 108922.
CrossRef
Google scholar
|
[32] |
Martinez-Almoyna, C., Thuiller, W., Chalmandrier, L., Ohlmann, M., Foulquier, A., Clément, J.C., Zinger, L., Münkemüller, T., 2019. Multi‐trophic β‐diversity mediates the effect of environmental gradients on the turnover of multiple ecosystem functions. Functional Ecology33, 2053–2064.
CrossRef
Google scholar
|
[33] |
Mori, A.S., Isbell, F., Seidl, R., 2018. β-diversity, community assembly, and ecosystem functioning. Trends in Ecology & Evolution33, 549–564.
CrossRef
Google scholar
|
[34] |
Pang, Z.Q., Mao, X.Y., Zhou, S.Q., Yu, S., Liu, G.Z., Lu, C.K., Wan, J.P., Hu, L.F., Xu, P., 2023. Microbiota-mediated nitrogen fixation and microhabitat homeostasis in aerial root-mucilage. Microbiome11, 85.
CrossRef
Google scholar
|
[35] |
Paśmionka, I.B., Bulski, K., Boligłowa, E., 2021. The participation of microbiota in the transformation of nitrogen compounds in the soil—a review. Agronomy11, 977.
CrossRef
Google scholar
|
[36] |
Peter, P.C., Enemo, D.C., Uzoh, I.M., 2021. Soil microbes and food security nexus: imperativeness of microbial biotechnology, In: Babalola, O.O., ed. Food Security and Safety. Cham: Springer545–561.
CrossRef
Google scholar
|
[37] |
Philippot, L., Chenu, C., Kappler, A., Rillig, M.C., Fierer, N., 2024. The interplay between microbial communities and soil properties. Nature Reviews Microbiology22, 226–239.
CrossRef
Google scholar
|
[38] |
Philippot, L., Spor, A., Hénault, C., Bru, D., Bizouard, F., Jones, C.M., Sarr, A., Maron, P.A., 2013. Loss in microbial diversity affects nitrogen cycling in soil. The ISME Journal,7, 1609–1619.
CrossRef
Google scholar
|
[39] |
Rudrappa, T., Czymmek, K.J., Paré, P.W., Bais, H.P., 2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiology148, 1547–1556.
CrossRef
Google scholar
|
[40] |
Sabir, M.S., Shahzadi, F., Ali, F., Shakeela, Q., Niaz, Z., Ahmed, S., 2021. Comparative effect of fertilization practices on soil microbial diversity and activity: an overview. Current Microbiology78, 3644–3655.
CrossRef
Google scholar
|
[41] |
Salih, H.M., Yahya, A.I., Abdul-Rahem, A.M., Munam, B.H., 1989. Availability of phosphorus in a calcareous soil treated with rock phosphate or superphosphate as affected by phosphate-dissolving fungi. Plant and Soil120, 181–185.
CrossRef
Google scholar
|
[42] |
Stegen, J.C., Lin, X.J., Fredrickson, J.K., Chen, X.Y., Kennedy, D.W., Murray, C.J., Rockhold, M.L., Konopka, A., 2013. Quantifying community assembly processes and identifying features that impose them. The ISME Journal,7, 2069–2079.
CrossRef
Google scholar
|
[43] |
Tao, C.X., Wang, Z., Liu, S.S., Lv, N.N., Deng, X.H., Xiong, W., Shen, Z.Z., Zhang, N., Geisen, S., Li, R., Shen, Q.R., Kowalchuk, G.A., 2023. Additive fungal interactions drive biocontrol of Fusarium wilt disease. New Phytologist238, 1198–1214.
CrossRef
Google scholar
|
[44] |
Wang, L.Y., Liao, D., Rengel, Z., Shen, J.B., 2025. Soil–plant–microbe interactions in the rhizosphere: incremental amplification induced by localized fertilization. Frontiers of Agricultural Science and Engineering12, 57–68.
CrossRef
Google scholar
|
[45] |
Wang, Y., Chen, G.W., Sun, Y.F., Zhu, K., Jin, Y., Li, B.G., Wang, G., 2022. Different agricultural practices specify bacterial community compositions in the soil rhizosphere and root zone. Soil Ecology Letters4, 18–31.
CrossRef
Google scholar
|
[46] |
Webb, C.O., Ackerly, D.D., Kembel, S.W., 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics24, 2098–2100.
CrossRef
Google scholar
|
[47] |
Wen, Z., 2021. Bacterial composition, function and the enrichment of plant growth promoting rhizobacteria (PGPR) in differential rhizosphere compartments of Al-tolerant soybean in acidic soil. Hereditas (Beijing)43, 487–507.
CrossRef
Google scholar
|
[48] |
Wu, L.W., Zhang, Y., Guo, X., Ning, D.L., Zhou, X.S., Feng, J.J., Yuan, M.M., Liu, S., Guo, J.J., Gao, Z.P., Ma, J., Kuang, J.L., Jian, S.Y., Han, S., Yang, Z.F., Ouyang, Y., Fu, Y., Xiao, N.J., Liu, X.D., Wu, L.Y., Zhou, A.F., Yang, Y., Tiedje, J.M., Zhou, J.Z., 2022. Reduction of microbial diversity in grassland soil is driven by long-term climate warming. Nature Microbiology7, 1054–1062.
CrossRef
Google scholar
|
[49] |
Xie, S.Y., Tran, H.T., Pu, M.J., Zhang, T., 2023. Transformation characteristics of organic matter and phosphorus in composting processes of agricultural organic waste: research trends. Materials Science for Energy Technologies6, 331–342.
CrossRef
Google scholar
|
[50] |
Xu, L., He, N.P., Li, X.Z., Cao, H.L., Li, C.N., Wang, R.L., Wang, C.H., Yao, M.J., Zhou, S.G., Wang, J.M., 2021. Local community assembly processes shape β-diversity of soil phoD-harbouring communities in the northern Hemisphere steppes. Global Ecology and Biogeography30, 2273–2285.
CrossRef
Google scholar
|
[51] |
Xun, W.B., Liu, Y.P., Li, W., Ren, Y., Xiong, W., Xu, Z.H., Zhang, N., Miao, Y.Z., Shen, Q.R., Zhang, R.F., 2021. Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome9, 35.
CrossRef
Google scholar
|
[52] |
Yan, Y., Kuramae, E.E., De Hollander, M., Klinkhamer, P.G.L., van Veen, J.A., 2017. Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere. The ISME Journal,11, 56–66.
CrossRef
Google scholar
|
[53] |
Zhang, M., Liang, Y.C., Song, A.L., Yu, B., Zeng, X.B., Chen, M.S., Yin, H.Q., Zhang, X.X., Sun, B.L., Fan, F.L., 2017. Loss of soil microbial diversity may increase insecticide uptake by crop. Agriculture, Ecosystems & Environment240, 84–91.
CrossRef
Google scholar
|
[54] |
Zhao, X.F., Shu, W.S., Hao, Y.Q., 2022. Seasonal climate variations promote bacterial α-Diversity in soil. Microbial Ecology83, 513–517.
CrossRef
Google scholar
|
/
〈 |
|
〉 |