Anecic earthworm enhanced the soil multifunctionality by affecting soil bacterial abundant taxa

Abstract

Earthworm gut microbiome can significantly influence soil microbial community and functions. However, how earthworms affect the abundant, intermediate, and rare soil bacterial taxa and subsequently regulate soil multifunctionality remains poorly understood. In this study, we investigated bacteria composition and functional gene traits with and without earthworm addition in low-nutrient soil. Our results show that earthworm addition enhanced soil multifunctionality, including organic carbon, nitrogen, and phosphorus mineralization. Compared to other groups, abundant taxa in earthworm-treated soil exhibited higher 16S rRNA operon copy numbers, copiotroph/oligotroph ratios, niche width, and network efficiency, suggesting a greater competitive capacity for resource acquisition. We identified a core set of persistent abundant taxa genera (11 genera) in earthworm-treated soil, which persisted throughout the incubation period, and were notably dominant among abundant taxa in the earthworm gut (67.1%−79.2%). Furthermore, structural equation modeling revealed that gut-associated abundant taxa strongly influenced the composition of soil abundant taxa and persistent core abundant taxa genera, which in turn increased soil r-strategists and enhanced multifunctionality. Overall, our findings provide new insights into the ecological strategies of different soil taxa in response to earthworm addition and highlight the role of earthworm gut microbiome in adapting to nutrient-poor environments.

Graphical abstract

Keywords

earthworm gut / abundant taxa / microbial r-K selection / soil multifunctionality

Highlight

	● Earthworm gut persistently changed soil bacteria structure.
	● Soil abundant taxa primarily drive soil multifunctionality.
	● Earthworm increased the r-strategy prevalence of soil bacterial community.
	● Earthworms altered soil r/K strategy, not diversity, to drive soil multifunctionality.

References

[1] Adhikari, K., Hartemink, A.E., 2016. Linking soils to ecosystem services — A global review. Geoderma262, 101–111.

[2] Bastian, M., Heymann, S., Jacomy, M., 2009. Gephi: an open source software for exploring and manipulating networks. In: Proceedings of the International AAAI Conference on Web and Social Media. San Jose: AAAI, 361–362.

[3] Bernard, L., Chapuis-Lardy, L., Razafimbelo, T., Razafindrakoto, M., Pablo, A.L., Legname, E., Poulain, J., Brüls, T., O’Donohue, M., Brauman, A., Chotte, J.L., Blanchart, E., 2012. Endogeic earthworms shape bacterial functional communities and affect organic matter mineralization in a tropical soil. The ISME Journal6, 213–222.

[4] Biswas, J.K., Banerjee, A., Rai, M., Naidu, R., Biswas, B., Vithanage, M., Dash, M.C., Sarkar, S.K., Meers, E., 2018. Potential application of selected metal resistant phosphate solubilizing bacteria isolated from the gut of earthworm (Metaphire posthuma) in plant growth promotion. Geoderma330, 117–124.

[5] Bi, Q.F., Jin, B.J., Zhu, D., Jiang, Y.G., Zheng, B.X., O’Connor, P., Yang, X.R., Richter, A., Lin, X.Y., Zhu, Y.G., 2021. How can fertilization regimes and durations shape earthworm gut microbiota in a long-term field experiment? Ecotoxicology and Environmental Safety 224, 112643.

[6] Blouin, M., Robin, A., Amans, L., Reverchon, F., Barois, I., Lavelle, P., 2025. A meta-analysis reveals earthworms as mutualists rather than predators of soil microorganisms. Geoderma455, 117238.

[7] 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.

[8] Chen, B.B., Peng, Z.H., Chen, S., Liu, Y., Qi, J.J., Pan, H.B., Gao, H., Gao, J.M., Liang, C.L., Liu, J.A., Qian, X., Zhang, X., Chen, S.F., Zhou, J.Z., Wei, G.H., Jiao, S., 2024. Bridging ecological processes to diversity formation and functional profiles in belowground bacterial communities. Soil Biology and Biochemistry198, 109573.

[9] 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.

[10] Chen, Y.J., Neilson, J.W., Kushwaha, P., Maier, R.M., Barberán, A., 2021. Life-history strategies of soil microbial communities in an arid ecosystem. The ISME Journal15, 649–657.

[11] Coleman, D. C., Callaham, M. A., Crossley Jr, D. A., 2004. Fundamentals of Soil Ecology, 2nd. Elsevier, New York.

[12] Dai, T.J., Wen, D.H., Bates, C.T., Wu, L.W., Guo, X., Liu, S., Su, Y.F., Lei, J.S., Zhou, J.Z., Yang, Y.F., 2022. Nutrient supply controls the linkage between species abundance and ecological interactions in marine bacterial communities. Nature Communications13, 175.

[13] Dal Bello, M., Lee, H., Goyal, A., Gore, J., 2021. Resource-diversity relationships in bacterial communities reflect the network structure of microbial metabolism. Nature Ecology & Evolution5, 1424–1434.

[14] 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.

[15] Delgado-Baquerizo, M., Oliverio, A.M., Brewer, T.E., Benavent-González, A., Eldridge, D.J., Bardgett, R.D., Maestre, F.T., Singh, B.K., Fierer, N., 2018. A global atlas of the dominant bacteria found in soil. Science359, 320–325.

[16] Deng, Y., Jiang, Y.H., Yang, Y.F., He, Z.L., Luo, F., Zhou, J.Z., 2012. Molecular ecological network analyses. BMC Bioinformatics13, 113.

[17] Drake, H.L., Horn, M.A., 2007. As the worm turns: the earthworm gut as a transient habitat for soil microbial biomes. Annual Review of Microbiology61, 169–189.

[18] Eldridge, D.J., Delgado-Baquerizo, M., Travers, S.K., Val, J., Oliver, I., Hamonts, K., Singh, B.K., 2017. Competition drives the response of soil microbial diversity to increased grazing by vertebrate herbivores. Ecology98, 1922–1931.

[19] Erlandson, S., Wei, X.J., Savage, J., Cavender-Bares, J., Peay, K., 2018. Soil abiotic variables are more important than Salicaceae phylogeny or habitat specialization in determining soil microbial community structure. Molecular Ecology27, 2007–2024.

[20] Escalas, A., Paula, F.S., Guilhaumon, F., Yuan, M.T., Yang, Y.F., Wu, L.W., Liu, F.F., Feng, J., Zhang, Y.G., Zhou, J.Z., 2022. Macroecological distributions of gene variants highlight the functional organization of soil microbial systems. The ISME Journal16, 726–737.

[21] Feng, K., Peng, X., Zhang, Z., Gu, S.S., He, Q., Shen, W.L., Wang, Z.J., Wang, D.R., Hu, Q.L., Li, Y., Wang, S., Deng, Y., 2022. iNAP: An integrated network analysis pipeline for microbiome studies. iMeta1, e13.

[22] Fierer, N., Bradford, M.A., Jackson, R.B., 2007. Toward an ecological classification of soil bacteria. Ecology88, 1354–1364.

[23] Galand, P.E., Casamayor, E.O., Kirchman, D.L., Lovejoy, C., 2009. Ecology of the rare microbial biosphere of the Arctic Ocean. Proceedings of the National Academy of Sciences of the United States of America106, 22427–22432.

[24] Hanks, R.J., Holmes, W.E., Tanner, C.B., 1954. Field Capacity Approximation Based on the Moisture-Transmitting Properties of the Soil. Soil Science Society of America Journal18, 252–254.

[25] Han, L.X., Fang, K., You, X.W., Li, Y.Q., Wang, X.G., Wang, J., 2023. Earthworms synergize with indigenous soil functional microorganisms to accelerate the preferential degradation of the highly toxic S-enantiomer of the fungicide imazalil in soil. Journal of Hazardous Materials457, 131778.

[26] Hu, P.L., Zhang, W., Kuzyakov, Y., Xiao, L.M., Xiao, D., Xu, L., Chen, H.S., Zhao, J., Wang, K.L., 2023. Linking bacterial life strategies with soil organic matter accrual by karst vegetation restoration. Soil Biology and Biochemistry177, 108925.

[27] Huber, P., Metz, S., Unrein, F., Mayora, G., Sarmento, H., Devercelli, M., 2020. Environmental heterogeneity determines the ecological processes that govern bacterial metacommunity assembly in a floodplain river system. The ISME Journal14, 2951–2966.

[28] Irshad, S., Frouz, J., 2024. How the effect of earthworms on soil organic matter mineralization and stabilization is affected by litter quality and stage of soil development. Biogeochemistry167, 1425–1436.

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

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

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

[32] Jin, B.J., Bi, Q.F., Li, K.J., Yu, Q.G., Ni, L., Lin, X.Y., Zhu, Y.G., 2022a. Long-term combined application of chemical fertilizers and organic manure shapes the gut microbial diversity and functional community structures of earthworms. Applied Soil Ecology170, 104250.

[33] Jin, B.J., Liu, X.P., Roux, X.L., Bi, Q.F., Li, K.J., Wu, C.Y., Sun, C.L., Zhu, Y.G., Lin, X.Y., 2022b. Biochar addition regulates soil and earthworm gut microbiome and multifunctionality. Soil Biology and Biochemistry173, 108810.

[34] Jin, B.J., Liu, X.P., Zhang, M., Hu, Y., Sun, C.L., Li, G., Zhu, Y.G., Lin, X.Y., 2023. Earthworms enhance the inhibition efficiency of 3,4-dimethylpyrazole phosphate on soil nitrification by altering soil AOB communities and gut denitrifier communities. Biology and Fertility of Soils59, 747–761.

[35] Klappenbach, J.A., Dunbar, J.M., Schmidt, T.M., 2000. rRNA operon copy number reflects Ecological strategies of bacteria. Applied and Environmental Microbiology66, 1328–1333.

[36] Lavelle, P., Lattaud, C., Trigo, D., Barois, I., 1995. Mutualism and biodiversity in soils. Plant and Soil170, 23–33.

[37] Lavelle, P., Spain, A.V., 2001. Soil Ecology, Springer Science & Business Media, Amsterdam.

[38] Li, H., Zhang, Y.Y., Yang, S., Wang, Z.R., Feng, X., Liu, H.Y., Jiang, Y., 2019. Variations in soil bacterial taxonomic profiles and putative functions in response to straw incorporation combined with N fertilization during the maize growing season. Agriculture, Ecosystems & Environment283, 106578.

[39] Lin, J.N., Lin, D.M., Zhu, G.Y., Wang, H.J., Qian, S.H., Zhao, L., Yang, Y.C., Fanin, N., 2022. Earthworms exert long lasting afterlife effects on soil microbial communities. Geoderma420, 115906.

[40] Liu, J.A., Peng, Z.H., Tu, H.R., Qiu, Y., Liu, Y., Li, X.M., Gao, H., Pan, H.B., Chen, B.B., Liang, C.L., Chen, S., Qi, J.J., Wang, Y.H., Wei, G.H., Jiao, S., 2024. Oligotrophic microbes are recruited to resist multiple global change factors in agricultural subsoils. Environment International183, 108429.

[41] Liu, T., Chen, X.Y., Gong, X., Lubbers, I.M., Jiang, Y.Y., Feng, W., Li, X.P., Whalen, J.K., Bonkowski, M., Griffiths, B.S., Hu, F., Liu, M.Q., 2019. Earthworms coordinate soil biota to improve multiple ecosystem functions. Current Biology29, 3420–3429.e5.

[42] 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.

[43] Mallon, C.A., Poly, F., Le Roux, X., Marring, I., van Elsas, J.D., Salles, J.F., 2015. Resource pulses can alleviate the biodiversity-invasion relationship in soil microbial communities. Ecology96, 915–926.

[44] Medina-Sauza, R.M., Álvarez-Jiménez, M., Delhal, A., Reverchon, F., Blouin, M., Guerrero-Analco, J.A., Cerdán, C.R., Guevara, R., Villain, L., Barois, I., 2019. Earthworms building up soil microbiota, a review. Frontiers in Environmental Science7, 81.

[45] Mo, Y.Y., Zhang, W.J., Yang, J., Lin, Y.S., Yu, Z., Lin, S.J., 2018. Biogeographic patterns of abundant and rare bacterioplankton in three subtropical bays resulting from selective and neutral processes. The ISME Journal12, 2198–2210.

[46] 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.

[47] Nemergut, D.R., Costello, E.K., Hamady, M., Lozupone, C., Jiang, L., Schmidt, S.K., Fierer, N., Townsend, A.R., Cleveland, C.C., Stanish, L., Knight, R., 2011. Global patterns in the biogeography of bacterial taxa. Environmental Microbiology13, 135–144.

[48] Nemergut, D.R., Knelman, J.E., Ferrenberg, S., Bilinski, T., Melbourne, B., Jiang, L., Violle, C., Darcy, J.L., Prest, T., Schmidt, S.K., Townsend, A.R., 2016. Decreases in average bacterial community rRNA operon copy number during succession. The ISME Journal10, 1147–1156.

[49] Newton, R.J., Shade, A., 2016. Lifestyles of rarity: understanding heterotrophic strategies to inform the ecology of the microbial rare biosphere. Aquatic Microbial Ecology78, 51–63.

[50] Ning, D.L., Yuan, M.T., Wu, L.W., Zhang, Y., Guo, X., Zhou, X.S., Yang, Y.F., Arkin, A.P., Firestone, M.K., Zhou, J.Z., 2020. A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nature Communications11, 4717.

[51] OECD Publishing, Paris. https://doi.org/10.1787/9789264264496-en.

[52] Oksanen, J., Simpson, G.L., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., Caceres, M.D., Durand, S., Evangelista, H.B.A., FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M.O., Lahti, L., McGlinn, D., Ouellette, M.H., Cunha, E.R., Smith, T., Stier, A., Braak, C.J.F. T., Weedon, J., 2024. vegan: Community Ecology Package.

[53] Pass, D.A., Morgan, A.J., Read, D.S., Field, D., Weightman, A.J., Kille, P 2015. The effect of anthropogenic arsenic contamination on the earthworm microbiome. Environmental Microbiology17, 1884–1896.

[54] Pedrós-Alió, C., 2012. The rare bacterial biosphere. Annual Review of Marine Science4, 449–466.

[55] Peng, J.W., Liu, H., Hu, Y., Sun, Y., Liu, Q., Li, J.G., Dong, Y.H., 2022. Shift in soil bacterial communities from K- to r-strategists facilitates adaptation to grassland degradation. Land Degradation & Development33, 2076–2091.

[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] Ratsiatosika, O., Razafindrakoto, M., Razafimbelo, T., Rabenarivo, M., Becquer, T., Bernard, L., Trap, J., Blanchart, E., 2021. Earthworm inoculation improves upland rice crop yield and other agrosystem services in Madagascar. Agriculture11, 60.

[58] Razanamalala, K., Razafimbelo, T., Maron, P.A., Ranjard, L., Chemidlin, N., Lelièvre, M., Dequiedt, S., Ramaroson, V.H., Marsden, C., Becquer, T., Trap, J., Blanchart, E., Bernard, L., 2018. Soil microbial diversity drives the priming effect along climate gradients: a case study in Madagascar. The ISME Journal12, 451–462.

[59] Rosseel, Y., Jorgensen, T.D., Wilde, L.D., Oberski, D., Byrnes, J., Vanbrabant, L., Savalei, V., Merkle, E., Hallquist, M., Rhemtulla, M., Katsikatsou, M., Barendse, M., Rockwood, N., Scharf, F., Du, H., Jamil, H., Classe, F., 2024. lavaan: Latent Variable Analysis.

[60] Sapkota, R., Santos, S., Farias, P., Krogh, P.H., Winding, A., 2020. Insights into the earthworm gut multi-kingdom microbial communities. Science of the Total Environment727, 138301.

[61] 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.

[62] Swart, E., Goodall, T., Kille, P., Spurgeon, D.J., Svendsen, C., 2020. The earthworm microbiome is resilient to exposure to biocidal metal nanoparticles. Environmental Pollution267, 115633.

[63] Thomas Kelly, S., 2018. {info. centrality}: an R implementation of information centrality using igraph

[64] Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry19, 703–707.

[65] Villeneuve, C., Beauregard, P., Bradley, R.L., 2024. Non-native earthworms preferentially promote bacterial rather than fungal denitrification in northern temperate deciduous forests. Soil Biology and Biochemistry196, 109496.

[66] von Meijenfeldt, F.A.B., Hogeweg, P., Dutilh, B.E., 2023. A social niche breadth score reveals niche range strategies of generalists and specialists. Nature Ecology & Evolution7, 768–781.

[67] Vos, H.M.J., Ros, M.B.H., Koopmans, G.F., van Groenigen, J.W., 2014. Do earthworms affect phosphorus availability to grass? A pot experiment. Soil Biology and Biochemistry79, 34–42.

[68] Wang, C., Wan, S., Xing, X., Zhang, L., Han, X., 2006. Temperature and soil moisture interactively affected soil net N mineralization in temperate grassland in Northern China. Soil Biology and Biochemistry38, 1101–1110.

[69] Wang, N., Wang, W., Jiang, Y., Dai, W., Li, P., Yao, D., Wang, J., Shi, Y., Cui, Z., Cao, H., Dong, Y., Wang, H., 2021. Variations in bacterial taxonomic profiles and potential functions in response to the gut transit of earthworms (Eisenia fetida) feeding on cow manure. Science of Total Environment787, 147392.

[70] Wüst, P.K., Horn, M.A., Drake, H.L., 2011. Clostridiaceae and Enterobacteriaceae as active fermenters in earthworm gut content. The ISME Journal5, 92–106.

[71] Xia, R., Shi, Y., Wang, X.W., Wu, Y.L., Sun, M.M., Hu, F., 2022. Metagenomic sequencing reveals that the assembly of functional genes and taxa varied highly and lacked redundancy in the earthworm gut compared with soil under vanadium stress. mSystems7, e0125321.

[72] Xie, Z., Li, Y.T., Xiong, K., Tu, Z.H., Waiho, K., Yang, C.Y., Deng, Y.W., Li, S.S., Fang, J.K.H., Hu, M.H., Dupont, S., Wang, Y.J., 2023. Combined effect of salinity and hypoxia on digestive enzymes and intestinal microbiota in the oyster Crassostrea hongkongensis. Environmental Pollution331, 121921.

[73] 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.

[74] Yang, J.J., Schrader, S., Tebbe, C.C., 2024. Legacy effects of earthworms on soil microbial abundance, diversity, and community dynamics. Soil Biology and Biochemistry190, 109294.

[75] Yang, Y., Dou, Y.X., Wang, B.R., Xue, Z.J., Wang, Y.Q., An, S.S., Chang, S.X., 2023a. Deciphering factors driving soil microbial life-history strategies in restored grasslands. iMeta2, e66.

[76] Yang, Y.R., Callaham, M.A., Wu, X.F., Zhang, Y.F., Wu, D.H., Wang, D.L., 2023b. Gut microbial communities and their potential roles in cellulose digestion and thermal adaptation of earthworms. Science of the Total Environment903, 166666.

[77] 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.

[78] Zelezniak, A., Andrejev, S., Ponomarova, O., Mende, D.R., Bork, P., Patil, K.R., 2015. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proceedings of the National Academy of Sciences of the United States of America112, 6449–6454.

[79] Zhang, J.H., Meng, H., Kong, X.C., Cheng, X.Y., Ma, T., He, H., Du, W.C., Yang, S.G., Li, S.Y., Zhang, L.M., 2021. Combined effects of polyethylene and organic contaminant on zebrafish (Danio rerio): Accumulation of 9-Nitroanthracene, biomarkers and intestinal microbiota. Environmental Pollution277, 116767.

[80] Zhang, M., Jin, B.J., Bi, Q.F., Li, K.J., Sun, C.L., Lin, X.Y., Zhu, Y.G., 2022. Variations of earthworm gut bacterial community composition and metabolic functions in coastal upland soil along a 700-year reclamation chronosequence. Science of the Total Environment804, 149994.

[81] Zheng, B.X., Zhu, Y.G., Sardans, J., Peñuelas, J., Su, J.Q., 2018. QMEC: a tool for high-throughput quantitative assessment of microbial functional potential in C, N, P, and S biogeochemical cycling. Science China Life Sciences61, 1451–1462.

[82] Zheng, Q., Hu, Y.T., Zhang, S.S., Noll, L., Böckle, T., Dietrich, M., Herbold, C.W., Eichorst, S.A., Woebken, D., Richter, A., Wanek, W., 2019. Soil multifunctionality is affected by the soil environment and by microbial community composition and diversity. Soil Biology and Biochemistry136, 107521.

[83] Zheng, W.N., Fan, X.P., Chen, H., Ye, M.J., Yin, C., Wu, C.Y., Liang, Y.C., 2024. The response patterns of r- and K-strategist bacteria to long-term organic and inorganic fertilization regimes within the microbial food web are closely linked to rice production. Science of the Total Environment942, 173681.

[84] Zhu, G.F., Schmidt, O., Luan, L., Xue, J.R., Fan, J.B., Geisen, S., Sun, B., Jiang, Y.J., 2022. Bacterial keystone taxa regulate carbon metabolism in the earthworm gut. Microbiology Spectrum10, e0108122.

RIGHTS & PERMISSIONS

Higher Education Press