Distinct effects of abundant and rare microbial communities on ecosystem multifunctionality across the soil profiles in agricultural Isohumosols

Abstract

Elucidating the intricate dynamics of microbial communities across soil profiles is essential for deciphering the mechanisms by which microorganisms regulate ecosystem functions. However, previous studies on soil microorganisms have predominantly centered on abundant taxa, neglecting the significant role of rare taxa in maintaining ecosystem functions. This study comprehensively analyzed the diversity and assembly processes of both rare and abundant microbial taxa in the profiles of Udic and Ustic Isohumosols in northeast China. We also explored the relative contribution of rare and abundant microbial taxa in maintaining ecosystem multifunctionality. Results showed that rare microbial taxa exhibited a higher diversity compared to abundant taxa, and rare microbial taxa occupied more central positions within networks. Furthermore, rare taxa displayed narrower ecological niche breadths and stronger phylogenetic signals, and their community assembly was predominantly governed by deterministic processes. In contrast, stochastic processes exert more pronounced influences on the assemblage of abundant taxa. Ecosystem multifunctionality was significantly reduced in deep soil horizons relative to the surface soil horizons. This is accompanied by close cooperation of microorganisms to cope with environmental stress in deep soils. This study highlights the pivotal role of rare microbial communities in shaping multifunctionality of ecosystems across the entire soil profiles.

Graphical abstract

Keywords

assembly processes / ecosystem functions / microbial interactions / rare taxa / soil profiles

Highlight

	● Microbial taxa living in deep soil cooperated closely with each other to cope with environmental stress.
	● Rare microbial taxa occupy more central positions within ecological networks.
	● Rare microbial community assembly was predominantly governed by deterministic processes.
	● The impact of rare microbial taxa on ecosystem multifunctionality was greater than that of abundant taxa.

References

[1] Alonso-Sáez, L., Díaz-Pérez, L., Morán, X.A.G., 2015. The hidden seasonality of the rare biosphere in coastal marine bacterioplankton. Environmental Microbiology17, 3766–3780.

[2] 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 Letters17, 794–802.

[3] Bellemain, E., Carlsen, T., Brochmann, C., Coissac, E., Taberlet, P., Kauserud, H., 2010. ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiology10, 189.

[4] Benjamini, Y., Krieger, A.M., Yekutieli, D., 2006. Adaptive linear step-up procedures that control the false discovery rate. Biometrika93, 491–507.

[5] Biddle, J.F., Fitzgibbon, S., Schuster, S.C., Brenchley, J.E., House, C.H., 2008. Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proceedings of the National Academy of Sciences of the United States of America105, 10583–10588.

[6] Blomberg, S.P., Garland, T., Ives, A.R., 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution57, 717–745.

[7] 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., Bai, Y., Bisanz, J.E., Bittinger, K., Brejnrod, A., Brislawn, C.J., Brown, C.T., Callahan, B.J., Caraballo-Rodríguez, A.M., Chase, J., Cope, E.K., Da Silva, R., Diener, C., Dorrestein, P.C., Douglas, G.M., Durall, D.M., Duvallet, C., Edwardson, C.F., Ernst, M., Estaki, M., Fouquier, J., Gauglitz, J.M., Gibbons, S.M., Gibson, D.L., Gonzalez, A., Gorlick, K., Guo, J.R., Hillmann, B., Holmes, S., Holste, H., Huttenhower, C., Huttley, G.A., Janssen, S., Jarmusch, A.K., Jiang, L.M., Kaehler, B.D., Kang, K.B., Keefe, C.R., Keim, P., Kelley, S.T., Knights, D., Koester, I., Kosciolek, T., Kreps, J., Langille, M.G.I., Lee, J., Ley, R., Liu, Y.X., Loftfield, E., Lozupone, C., Maher, M., Marotz, C., Martin, B.D., McDonald, D., McIver, L.J., Melnik, A.V., Metcalf, J.L., Morgan, S.C., Morton, J.T., Naimey, A.T., Navas-Molina, J.A., Nothias, L.F., Orchanian, S.B., Pearson, T., Peoples, S.L., Petras, D., Preuss, M.L., Pruesse, E., Rasmussen, L.B., Rivers, A., Robeson II, M.S., Rosenthal, P., Segata, N., Shaffer, M., Shiffer, A., Sinha, R., Song, S.J., Spear, J.R., Swafford, A.D., Thompson, L.R., Torres, P.J., Trinh, P., Tripathi, A., Turnbaugh, P.J., Ul-Hasan, S., Van Der Hooft, J.J.J., Vargas, F., Vázquez-Baeza, Y., Vogtmann, E., Von Hippel, M., Walters, W., Wan, Y.H., Wang, M.X., Warren, J., Weber, K.C., Williamson, C.H.D., Willis, A.D., Xu, Z.Z., Zaneveld, J.R., Zhang, Y.L., Zhu, Q.Y., Knight, R., Caporaso, J.G., 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology37, 852–857.

[8] Brown, M.V., Ostrowski, M., Grzymski, J.J., Lauro, F.M., 2014. A trait based perspective on the biogeography of common and abundant marine bacterioplankton clades. Marine Genomics15, 17–28.

[9] Buss, H.L., Mathur, R., White, A.F., Brantley, S.L., 2010. Phosphorus and iron cycling in deep saprolite, Luquillo Mountains, Puerto Rico. Chemical Geology269, 52–61.

[10] Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods13, 581–583.

[11] Chen, Q.L., Ding, J., Zhu, D., Hu, H.W., Delgado-Baquerizo, M., Ma, Y.B., He, J.Z., Zhu, Y.G., 2020. Rare microbial taxa as the major drivers of ecosystem multifunctionality in long-term fertilized soils. Soil Biology and Biochemistry141, 107686.

[12] Chen, R.R., Zhong, L.H., Jing, Z.W., Guo, Z.Y., Li, Z.P., Lin, X.G., Feng, Y.Z., 2017. Fertilization decreases compositional variation of paddy bacterial community across geographical gradient. Soil Biology and Biochemistry114, 181–188.

[13] Coolen, M.J.L., Abbas, B., van Bleijswijk, J., Hopmans, E.C., Kuypers, M.M.M., Wakeham, S.G., Damste, J.S.S., 2007. Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: a basin-wide ecological study using 16S ribosomal and functional genes and membrane lipids. Environmental Microbiology9, 1001–1016.

[14] Delgado-Baquerizo, M., Eldridge, D.J., Ochoa, V., Gozalo, B., Singh, B.K., Maestre, F.T., 2017. Soil microbial communities drive the resistance of ecosystem multifunctionality to global change in drylands across the globe. Ecology Letters20, 1295–1305.

[15] 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 Communications7, 10541.

[16] Delgado-Baquerizo, M., Reich, P.B., Trivedi, C., Eldridge, D.J., Abades, S., Alfaro, F.D., Bastida, F., Berhe, A.A., Cutler, N.A., Gallardo, A., García-Velázquez, L., Hart, S.C., Hayes, P.E., He, J.Z., Hseu, Z.Y., Hu, H.W., Kirchmair, M., Neuhauser, S., Pérez, C.A., Reed, S.C., Santos, F., Sullivan, B.W., Trivedi, P., Wang, J.T., Weber-Grullon, L., Williams, M.A., Singh, B.K., 2020. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nature Ecology & Evolution4, 210–220.

[17] Du, S.C., Dini-Andreote, F., Zhang, N., Liang, C.L., Yao, Z.Y., Zhang, H.J., Zhang, D.M., 2020. Divergent co-occurrence patterns and assembly processes structure the abundant and rare bacterial communities in a salt Marsh ecosystem. Applied and Environmental Microbiology86, e00322–20.

[18] 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 and Biochemistry50, 58–65.

[19] Feng, J.Y., Xu, Y., Ma, B., Tang, C.X., Brookes, P.C., He, Y., Xu, J.M., 2019. Assembly of root-associated microbiomes of typical rice cultivars in response to lindane pollution. Environment International131, 104975.

[20] Fortmann-Roe, S., 2015. Consistent and clear reporting of results from diverse modeling techniques: the A3 method. Journal of Statistical Software66, 1–23.

[21] Gao, G.F., Peng, D., Tripathi, B.M., Zhang, Y.H., Chu, H.Y., 2020. Distinct community assembly processes of abundant and rare soil bacteria in coastal wetlands along an inundation gradient. mSystems5, e01150–20.

[22] Garcia-Pichel, F., Loza, V., Marusenko, Y., Mateo, P., Potrafka, R.M., 2013. Temperature drives the Continental-Scale distribution of key microbes in topsoil communities. Science340, 1574–1577.

[23] Gong, Z.T., Zhang, G.L., Chen, Z.C., 2007. Pedogenesis and Soil Taxonomy. Beijing: Science Press.

[24] 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.

[25] 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.

[26] Hu, X.J., Liang, A.Z., Yao, Q., Liu, Z.X., Yu, Z.H., Wang, G.H., Liu, J.J., 2020. Ridge tillage improves soil properties, sustains diazotrophic communities, and enhances extensively cooperative interactions among diazotrophs in a clay loam soil. Frontiers in Microbiology11, 1333.

[27] Huang, L.T., Ni, H.W., Li, X.Y., Sun, B., Liang, Y.T., 2021. Molecular ecological network of bacteria and fungi in paddy soil profile of typical red soil. Acta Pedologica Sinica58, 1018–1027.

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

[29] 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.

[30] Jiao, S., Lu, Y.H., 2020. Abundant fungi adapt to broader environmental gradients than rare fungi in agricultural fields. Global Change Biology26, 4506–4520.

[31] 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.

[32] Jiao, S., Yang, Y.F., Xu, Y.Q., Zhang, J., Lu, Y.H., 2020. Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China. The ISME Journal14, 202–216.

[33] Jing, X., Sanders, N.J., Shi, Y., Chu, H.Y., Classen, A.T., Zhao, K., Chen, L.T., Shi, Y., Jiang, Y.X., He, J.S., 2015. The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nature Communications6, 8159.

[34] 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.W., Wei, Z., Hol, W.H.G., 2017. Where less may be more: how the rare biosphere pulls ecosystems strings. The ISME Journal11, 853–862.

[35] 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. Bioinformatics26, 1463–1464.

[36] Langfelder, P., Horvath, S., 2012. Fast R functions for robust correlations and hierarchical clustering. Journal of Statistical Software46, i11.

[37] Li, L.J., Lin, Q., Li, X.Z., Li, T.Z., He, X.H., Li, D.P., Tao, Y., 2019. Dynamics and potential roles of abundant and rare subcommunities in the bioremediation of cadmium-contaminated paddy soil by Pseudomonas chenduensis. Applied Microbiology and Biotechnology103, 8203–8214.

[38] Liu, B.Y., Zhang, G.L., Xie, Y., Shen, B., Gu, Z.J., Ding, Y.Y., 2021. Delineating the black soil region and typical black soil region of northeastern China. Chinese Science Bulletin66, 96–106.

[39] Liu, X.P., Wang, H.T., Wu, Y.J., Bi, Q.F., Ding, K., Lin, X.Y., 2022. Manure application effects on subsoils: abundant taxa initiate the diversity reduction of rare bacteria and community functional alterations. Soil Biology and Biochemistry174, 108816.

[40] Liu, Z.X., Gu, H.D., Hu, X.J., Yu, Z.H., Li, Y.S., Liu, J.J., Jin, J., Liu, X.B., Wang, G.H., 2024a. Coupling changes of soil functional gene abundances and extracellular enzyme activities across the diagnostic horizons of agricultural Isohumosols. Pedosphere34, 540–552.

[41] Liu, Z.X., Gu, H.D., Yao, Q., Jiao, F., Hu, X.J., Liu, J.J., Jin, J., Liu, X.B., Wang, G.H., 2024b. Soil pH and carbon quality index regulate the biogeochemical cycle couplings of carbon, nitrogen and phosphorus in the profiles of Isohumosols. Science of the Total Environment922, 171269.

[42] Liu, Z.X., Gu, H.D., Yao, Q., Jiao, F., Liu, J.J., Jin, J., Liu, X.B., Wang, G.H., 2022. Microbial communities in the diagnostic horizons of agricultural Isohumosols in northeast China reflect their soil classification. CATENA216, 106430.

[43] Locey, K.J., Lennon, J.T., 2016. Scaling laws predict global microbial diversity. Proceedings of the National Academy of Sciences of the United States of America113, 5970–5975.

[44] Luan, L., Liang, C., Chen, L.J., Wang, H.T., Xu, Q.S., Jiang, Y.J., Sun, B., 2020. Coupling bacterial community assembly to microbial metabolism across soil profiles. mSystems5, e00298–20.

[45] Luo, G.W., Rensing, C., Chen, H., Liu, M.Q., Wang, M., Guo, S.W., Ling, N., Shen, Q.R., 2018. Deciphering the associations between soil microbial diversity and ecosystem multifunctionality driven by long-term fertilization management. Functional Ecology32, 1103–1116.

[46] Ma, B., Wang, H.Z., Dsouza, M., Lou, J., He, Y., Dai, Z.M., Brookes, P.C., Xu, J.M., Gilbert, J.A., 2016. Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. The ISME Journal10, 1891–1901.

[47] Maestre, F.T., Quero, J.L., Gotelli, N.J., Escudero, A., Ochoa, V., Delgado-Baquerizo, M., García-Gómez, M., Bowker, M.A., Soliveres, S., Escolar, C., García-Palacios, P., Berdugo, M., Valencia, E., Gozalo, B., Gallardo, A., Aguilera, L., Arredondo, T., Blones, J., Boeken, B., Bran, D., Conceição, A.A., Cabrera, O., Chaieb, M., Derak, M., Eldridge, D.J., Espinosa, C.I., Florentino, A., Gaitán, J., Gatica, M.G., Ghiloufi, W., Gómez-González, S., Gutiérrez, J.R., Hernández, R.M., Huang, X.W., Huber-Sannwald, E., Jankju, M., Miriti, M., Monerris, J., Mau, R.L., Morici, E., Naseri, K., Ospina, A., Polo, V., Prina, A., Pucheta, E., Ramírez-Collantes, D.A., Romão, R., Tighe, M., Torres-Díaz, C., Val, J., Veiga, J.P., Wang, D.L., Zaady, E., 2012. Plant species richness and ecosystem multifunctionality in global drylands. Science335, 214–218.

[48] Martiny, J.B.H., Jones, S.E., Lennon, J.T., Martiny, A.C., 2015. Microbiomes in light of traits: a phylogenetic perspective. Science350, aac9323.

[49] Montesinos-Navarro, A., Hiraldo, F., Tella, J.L., Blanco, G., 2017. Network structure embracing mutualism–antagonism continuums increases community robustness. Nature Ecology & Evolution1, 1661–1669.

[50] Montoya, J.M., Pimm, S.L., Solé, R.V., 2006. Ecological networks and their fragility. Nature442, 259–264.

[51] 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 Communications8, 14349.

[52] Nilsson, R.H., Larsson, K.H., Taylor, A.F.S., Bengtsson-Palme, J., Jeppesen, T.S., Schigel, D., Kennedy, P., Picard, K., Glöckner, F.O., Tedersoo, L., Saar, I., Kõljalg, U., Abarenkov, K., 2018. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research47, D259–D264.

[53] 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.

[54] Oliverio, A.M., Bradford, M.A., Fierer, N., 2017. Identifying the microbial taxa that consistently respond to soil warming across time and space. Global Change Biology23, 2117–2129.

[55] Pandit, S.N., Kolasa, J., Cottenie, K., 2009. Contrasts between habitat generalists and specialists: an empirical extension to the basic metacommunity framework. Ecology90, 2253–2262.

[56] 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 Research41, D590–D596.

[57] Ramirez, K.S., Knight, C.G., De Hollander, M., Brearley, F.Q., Constantinides, B., Cotton, A., Creer, S., Crowther, T.W., Davison, J., Delgado-Baquerizo, M., Dorrepaal, E., Elliott, D.R., Fox, G., Griffiths, R.I., Hale, C., Hartman, K., Houlden, A., Jones, D.L., Krab, E.J., Maestre, F.T., McGuire, K.L., Monteux, S., Orr, C.H., Van Der Putten, W.H., Roberts, I.S., Robinson, D.A., Rocca, J.D., Rowntree, J., Schlaeppi, K., Shepherd, M., Singh, B.K., Straathof, A.L., Bhatnagar, J.M., Thion, C., Van Der Heijden, M.G.A., De Vries, F.T., 2018. Detecting macroecological patterns in bacterial communities across independent studies of global soils. Nature Microbiology3, 189–196.

[58] Rivett, D.W., Bell, T., 2018. Abundance determines the functional role of bacterial phylotypes in complex communities. Nature Microbiology3, 767–772.

[59] Saunders, A.M., Albertsen, M., Vollertsen, J., Nielsen, P.H., 2016. The activated sludge ecosystem contains a core community of abundant organisms. The ISME Journal10, 11–20.

[60] Schütz, K., Kandeler, E., Nagel, P., Scheu, S., Ruess, L., 2010. Functional microbial community response to nutrient pulses by artificial groundwater recharge practice in surface soils and subsoils. FEMS Microbiology Ecology72, 445–455.

[61] Shade, A., Jones, S.E., Caporaso, J.G., Handelsman, J., Knight, R., Fierer, N., Gilbert, J.A., 2014. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. mBio5, e01371–14.

[62] Singh, B.K., Quince, C., Macdonald, C.A., Khachane, A., Thomas, N., Al-Soud, W.A., Sørensen, S.J., He, Z.L., White, D., Sinclair, A., Crooks, B., Zhou, J.Z., Campbell, C.D., 2014. Loss of microbial diversity in soils is coincident with reductions in some specialized functions. Environmental Microbiology16, 2408–2420.

[63] 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 Journal7, 2069–2079.

[64] Stegen, J.C., Lin, X.J., Konopka, A.E., Fredrickson, J.K., 2012. Stochastic and deterministic assembly processes in subsurface microbial communities. The ISME Journal6, 1653–1664.

[65] Tenenhaus, M., Vinzi, V.E., Chatelin, Y.M., Lauro, C., 2005. PLS path modeling. Computational Statistics & Data Analysis48, 159–205.

[66] Toju, H., Tanabe, A.S., Sato, H., 2018. Network hubs in root-associated fungal metacommunities. Microbiome6, 116.

[67] Van Elsas, J.D., Chiurazzi, M., Mallon, C.A., Elhottovā, D., Krištůfek, V., Salles, J.F., 2012. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proceedings of the National Academy of Sciences of the United States of America109, 1159–1164.

[68] Vinzi, V.E., Trinchera, L., Squillacciotti, S., Tenenhaus, M., 2008. REBUS-PLS: a response-based procedure for detecting unit segments in PLS path modelling. Applied Stochastic Models in Business and Industry24, 439–458.

[69] 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.

[70] Xu, M., Huang, Q., Xiong, Z.Q., Liao, H., Lv, Z.G., Chen, W.L., Luo, X.S., Hao, X.L., 2021. Distinct responses of rare and abundant microbial taxa to in situ chemical stabilization of Cadmium-Contaminated soil. mSystems6, e0104021.

[71] Xu, Y., Ge, Y., Song, J.X., Rensing, C., 2020. Assembly of root-associated microbial community of typical rice cultivars in different soil types. Biology and Fertility of Soils56, 249–260.

[72] Xue, M.D., Guo, Z.Y., Gu, X.Y., Gao, H.L., Weng, S.M., Zhou, J., Gu, D.G., Lu, H.X., Zhou, X.Q., 2020. Rare rather than abundant microbial communities drive the effects of long-term greenhouse cultivation on ecosystem functions in subtropical agricultural soils. Science of the Total Environment706, 136004.

[73] 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.

[74] Zhang, J., Zhang, B.G., Liu, Y., Guo, Y.Q., Shi, P., Wei, G.H., 2018. Distinct large-scale biogeographic patterns of fungal communities in bulk soil and soybean rhizosphere in China. Science of the Total Environment644, 791–800.

[75] Zhang, Z.Q., Lu, Y.H., Wei, G.H., Jiao, S., 2022. Rare species-driven diversity–ecosystem multifunctionality relationships are promoted by stochastic community assembly. mBio13, e0044922.

[76] Zhou, J.Z., Deng, Y., Luo, F., He, Z.L., Tu, Q.C., Zhi, X.Y., 2010. Functional molecular ecological networks. mBio1, e00169–10.

[77] Zhou, J.Z., Deng, Y., Zhang, P., Xue, K., Liang, Y.T., Van Nostrand, J.D., Yang, Y.F., He, Z.L., Wu, L.Y., 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 America111, E836–E845.

[78] Zhou, L., Zhou, Y.Q., Yao, X.L., Cai, J., Liu, X., Tang, X.M., Zhang, Y.L., Jang, K.S., Jeppesen, E., 2020. Decreasing diversity of rare bacterial subcommunities relates to dissolved organic matter along permafrost thawing gradients. Environment International134, 105330.

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