Effects of core soil microbial taxa on soil carbon source utilization under different long-term fertilization treatments in Ultisol

Highlights

● Core taxa play an important role in regulating soil carbon metabolism.

● Ecological cluster with oligotrophic made key contributions to soil carbon metabolism.

● Microbial cluster characteristics link microorganisms to carbon metabolism.

Abstract

Characterizing the ecological roles of core soil microbial species in soil carbon metabolism is critically important for enhancing carbon sequestration in agricultural systems; however, no studies to date have determined the effects of core soil microbial taxa on carbon metabolism under various long-term fertilization practices. Here, we collected soil samples from field plots that had been subjected to different fertilization practices for nearly 30 years and examined the long-term effects of fertilization on the preferences of core soil bacterial taxa for different carbon sources. We also examined the relative contribution of core soil bacterial taxa in utilization of different carbon source types in Biolog Eco microplates. Long-term fertilization treatment had a significant effect on soil properties and bacterial community structure. The core taxa were closely related to soil carbon source utilization. The co-occurrence network showed that the major ecological clusters containing core taxa made key contributions to soil carbon source utilization. The organic fertilization increased the abundance of a core cluster with a low weighted average rrn copy number. This ecological cluster was the most important factor affecting soil carbon source utilization even among soil physicochemical factors considered. Our findings indicate that core taxa characterized by oligotrophic bacteria have a major effect on carbon source utilization in Ultisols.

Graphical abstract

Keywords

core taxa / long-term fertilization / life-history strategy / agricultural ecosystems / sequencing

References

[1] Abdalla, K., Sun, Y., Zarebanadkouki, M., Gaiser, T., Seidel, S., Pausch, J., 2022. Long-term continuous farmyard manure application increases soil carbon when combined with mineral fertilizers due to lower priming effects. Geoderma428, 116216.

[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] Bian, Q., Wang, X.Y., Bao, X.G., Zhu, L.Y., Xie, Z.B., Che, Z.X., Sun, B., 2022. Exogenous substrate quality determines the dominant keystone taxa linked to carbon mineralization: evidence from a 30-year experiment. Soil Biology and Biochemistry169, 108683.

[4] Cai, A.D., Xu, M.G., Wang, B.R., Zhang, W.J., Liang, G.P., Hou, E.Q., Luo, Y.Q., 2019. Manure acts as a better fertilizer for increasing crop yields than synthetic fertilizer does by improving soil fertility. Soil and Tillage Research189, 168–175.

[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 Methods7, 335–336.

[6] 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.

[7] 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.

[8] 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.

[9] Dai, Z.M., Zang, H.D., Chen, J., Fu, Y.Y., Wang, X.H., Liu, H.T., Shen, C.C., Wang, J.J., Kuzyakov, Y., Becker, J.N., Hemp, A., Barberán, A., Gunina, A., Chen, H.H., Luo, Y., Xu, J.M., 2021. Metagenomic insights into soil microbial communities involved in carbon cycling along an elevation climosequences. Environmental Microbiology23, 4631–4645.

[10] 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.

[11] Du, S., Li, X.Q., Feng, J., Huang, Q.Y., Liu, Y.R., 2023. Soil core microbiota drive community resistance to mercury stress and maintain functional stability. Science of the Total Environment894, 165056.

[12] Fan, K.K., Chu, H.Y., Eldridge, D.J., Gaitan, J.J., Liu, Y.R., Sokoya, B., Wang, J.T., Hu, H.W., He, J.Z., Sun, W., Cui, H.Y., Alfaro, F.D., Abades, S., Bastida, F., Díaz-López, M., Bamigboye, A.R., Berdugo, M., Blanco-Pastor, J.L., Grebenc, T., Duran, J., Illán, J.G., Makhalanyane, T.P., Mukherjee, A., Nahberger, T.U., Peñaloza-Bojacá, G.F., Plaza, C., Verma, J.P., Rey, A., Rodríguez, A., Siebe, C., Teixido, A.L., Trivedi, P., Wang, L., Wang, J.Y., Yang, T.X., Zhou, X.Q., Zhou, X.B., Zaady, E., Tedersoo, L., Delgado-Baquerizo, M., 2023. Soil biodiversity supports the delivery of multiple ecosystem functions in urban greenspaces. Nature Ecology & Evolution7, 113–126.

[13] Feng, Y.Z., Delgado-Baquerizo, M., Zhu, Y.G., Han, X.Z., Han, X.R., Xin, X.L., Li, W., Guo, Z.B., Dang, T.H., Li, C.H., Zhu, B., Cai, Z.J., Li, D.M., Zhang, J.B., 2022. Responses of soil bacterial diversity to fertilization are driven by local environmental context across China. Engineering12, 164–170.

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

[15] Francioli, D., Schulz, E., Lentendu, G., Wubet, T., Buscot, F., Reitz, T., 2016. Mineral vs. organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Frontiers in Microbiology7, 1446.

[16] Hartmann, M., Six, J., 2023. Soil structure and microbiome functions in agroecosystems. Nature Reviews Earth & Environment4, 4–18.

[17] He, W., Ye, W.H., Sun, M.J., Li, Y.P., Chen, M.M., Wei, M., Hu, G.Q., Yang, Q.G., Pan, H., Lou, Y.H., Wang, H., Zhuge, Y.P., 2022. Soil phosphorus availability and stoichiometry determine microbial activity and functional diversity of fluvo-aquic soils under long-term fertilization regimes. Journal of Soils and Sediments22, 1214–1227.

[18] Ho, A., Di Lonardo, D.P., Bodelier, P.L.E., 2017. Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiology Ecology93, fix006.

[19] Hu, X.J., Gu, H.D., Liu, J.J., Wei, D., Zhu, P., Cui, X.A., Zhou, B.K., Chen, X.L., Jin, J., Liu, X.B., Wang, G.H., 2022. Metagenomics reveals divergent functional profiles of soil carbon and nitrogen cycling under long-term addition of chemical and organic fertilizers in the black soil region. Geoderma418, 115846.

[20] Jiao, S., Chen, W.M., Wei, G.H., 2022a. Core microbiota drive functional stability of soil microbiome in reforestation ecosystems. Global Change Biology28, 1038–1047.

[21] Jiao, S., Qi, J.J., Jin, C.J., Liu, Y., Wang, Y., Pan, H.B., Chen, S., Liang, C.L., Peng, Z.H., Chen, B.B., Qian, X., Wei, G.H., 2022b. Core phylotypes enhance the resistance of soil microbiome to environmental changes to maintain multifunctionality in agricultural ecosystems. Global Change Biology28, 6653–6664.

[22] Jiao, S., Xu, Y.Q., Zhang, J., Hao, X., Lu, Y.H., 2019. Core microbiota in agricultural soils and their potential associations with nutrient cycling. mSystems4, e00313–18.

[23] Kumar, U., Shahid, M., Tripathi, R., Mohanty, S., Kumar, A., Bhattacharyya, P., Lal, B., Gautam, P., Raja, R., Panda, B.B., Jambhulkar, N.N., Shukla, A.K., Nayak, A.K., 2017. Variation of functional diversity of soil microbial community in sub-humid tropical rice-rice cropping system under long-term organic and inorganic fertilization. Ecological Indicators73, 536–543.

[24] Lal, R., 2004. Soil carbon sequestration impacts on global climate change and food security. Science304, 1623–1627.

[25] Leff, J.W., Jones, S.E., Prober, S.M., Barberán, A., Borer, E.T., Firn, J.L., Harpole, W.S., Hobbie, S.E., Hofmockel, K.S., Knops, J.M.H., McCulley, R.L., La Pierre, K., Risch, A.C., Seabloom, E.W., Schütz, M., Steenbock, C., Stevens, C.J., Fierer, N., 2015. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proceedings of the National Academy of Sciences of the United States of America112, 10967–10972.

[26] Li, Y.Z., Hou, Y.T., Hou, Q.M., Long, M., Yang, Y.L., Wang, Z.T., Liao, Y.C., 2023. Long-term plastic mulching decreases rhizoplane soil carbon sequestration by decreasing microbial anabolism. Science of the Total Environment868, 161713.

[27] Liang, C., Schimel, J.P., Jastrow, J.D., 2017. The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology2, 17105.

[28] Lin, Q., De Vrieze, J., Fang, X.Y., Li, L.J., Li, X.Z., 2022. Microbial life strategy with high rRNA operon copy number facilitates the energy and nutrient flux in anaerobic digestion. Water Research226, 119307.

[29] Liu, J., Liu, M., Wu, M., Jiang, C.Y., Chen, X.F., Cai, Z.J., Wang, B.R., Zhang, J., Zhang, T.L., Li, Z.P., 2018. Soil pH rather than nutrients drive changes in microbial community following long-term fertilization in acidic Ultisols of southern China. Journal of Soils and Sediments18, 1853–1864.

[30] 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.

[31] Louca, S., Polz, M.F., Mazel, F., Albright, M.B.N., Huber, J.A., O’Connor, M.I., Ackermann, M., Hahn, A.S., Srivastava, D.S., Crowe, S.A., Doebeli, M., Parfrey, L.W., 2018. Function and functional redundancy in microbial systems. Nature Ecology & Evolution2, 936–943.

[32] Ma, T., Gao, W.J., Shi, B.W., Yang, Z.Y., Li, Y.F., Zhu, J.X., He, J.S., 2023. Effects of short- and long-term nutrient addition on microbial carbon use efficiency and carbon accumulation efficiency in the Tibetan alpine grassland. Soil and Tillage Research229, 105657.

[33] Philippot, L., Andersson, S.G.E., Battin, T.J., Prosser, J.I., Schimel, J.P., Whitman, W.B., Hallin, S., 2010. The ecological coherence of high bacterial taxonomic ranks. Nature Reviews Microbiology8, 523–529.

[34] Raza, S., Miao, N., Wang, P.Z., Ju, X.T., Chen, Z.J., Zhou, J.B., Kuzyakov, Y., 2020. Dramatic loss of inorganic carbon by nitrogen-induced soil acidification in Chinese croplands. Global Change Biology26, 3738–3751.

[35] Roller, B.R.K., Stoddard, S.F., Schmidt, T.M., 2016. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nature Microbiology1, 16160.

[36] Rousk, J., Bååth, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G., Knight, R., Fierer, N., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. The ISME Journal4, 1340–1351.

[37] Schimel, J.P., Schaeffer, S.M., 2012. Microbial control over carbon cycling in soil. Frontiers in Microbiology3, 348.

[38] Shade, A., Handelsman, J., 2012. Beyond the Venn diagram: the hunt for a core microbiome. Environmental Microbiology14, 4–12.

[39] Sheng, Y.Q., Zhan, Y., Zhu, L.Z., 2016. Reduced carbon sequestration potential of biochar in acidic soil. Science of the Total Environment572, 129–137.

[40] Stockmann, U., Adams, M.A., Crawford, J.W., Field, D.J., Henakaarchchi, N., Jenkins, M., Minasny, B., McBratney, A.B., de Remy de Courcelles, V., Singh, K., Wheeler, I., Abbott, L., Angers, D.A., Baldock, J., Bird, M., Brookes, P.C., Chenu, C., Jastrow, J.D., Lal, R., Lehmann, J., O’Donnell, A.G., Parton, W.J., Whitehead, D., Zimmermann, M., 2013. The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agriculture, Ecosystems & Environment164, 80–99.

[41] Stoddard, S.F., Smith, B.J., Hein, R., Roller, B.R.K., Schmidt, T.M., 2015. rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Research43, D593–D598.

[42] Toju, H., Peay, K.G., Yamamichi, M., Narisawa, K., Hiruma, K., Naito, K., Fukuda, S., Ushio, M., Nakaoka, S., Onoda, Y., Yoshida, K., Schlaeppi, K., Bai, Y., Sugiura, R., Ichihashi, Y., Minamisawa, K., Kiers, E.T., 2018. Core microbiomes for sustainable agroecosystems. Nature Plants4, 247–257.

[43] Wang, J.L., Liu, K.L., Zhao, X.Q., Gao, G.F., Wu, Y.H., Shen, R.F., 2022a. Microbial keystone taxa drive crop productivity through shifting aboveground-belowground mineral element flows. Science of the Total Environment811, 152342.

[44] Wang, Y.F., Chen, P., Wang, F.H., Han, W.X., Qiao, M., Dong, W.X., Hu, C.S., Zhu, D., Chu, H.Y., Zhu, Y.G., 2022b. The ecological clusters of soil organisms drive the ecosystem multifunctionality under long-term fertilization. Environment International161, 107133.

[45] Wei, M., Hu, G.Q., Wang, H., Bai, E., Lou, Y.H., Zhang, A.J., Zhuge, Y.P., 2017. 35 years of manure and chemical fertilizer application alters soil microbial community composition in a Fluvo-aquic soil in Northern China. European Journal of Soil Biology82, 27–34.

[46] Wertz, S., Degrange, V., Prosser, J.I., Poly, F., Commeaux, C., Guillaumaud, N., Le Roux, X., 2007. Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. Environmental Microbiology9, 2211–2219.

[47] Wu, Z.X., Li, H.H., Liu, Q.L., Ye, C.Y., Yu, F.X., 2020. Application of bio-organic fertilizer, not biochar, in degraded red soil improves soil nutrients and plant growth. Rhizosphere16, 100264.

[48] Xiang, X.J., Adams, J.M., Qiu, C.F., Qin, W.J., Chen, J.R., Jin, L.L., Xu, C.X., Liu, J., 2021. Nutrient improvement and soil acidification inducing contrary effects on bacterial community structure following application of hairy vetch (Vicia villosa Roth L. ) in Ultisol. Agriculture, Ecosystems & Environment312, 107348.

[49] Xiang, X.J., Liu, J., Zhang, J., Li, D.M., Xu, C.X., Kuzyakov, Y., 2020. Divergence in fungal abundance and community structure between soils under long-term mineral and organic fertilization. Soil and Tillage Research196, 104491.

[50] Xiao, Q., Huang, Y.P., Wu, L., Tian, Y.F., Wang, Q.Q., Wang, B.R., Xu, M.G., Zhang, W.J., 2021. Long-term manuring increases microbial carbon use efficiency and mitigates priming effect via alleviated soil acidification and resource limitation. Biology and Fertility of Soils57, 925–934.

[51] Xun, W.B., Zhao, J., Xue, C., Zhang, G.S., Ran, W., Wang, B.R., Shen, Q.R., Zhang, R.F., 2016. Significant alteration of soil bacterial communities and organic carbon decomposition by different long-term fertilization management conditions of extremely low-productivity arable soil in South China. Environmental Microbiology18, 1907–1917.

[52] Yang, G.W., Ryo, M., Roy, J., Lammel, D.R., Ballhausen, M.B., Jing, X., Zhu, X.F., Rillig, M.C., 2022. Multiple anthropogenic pressures eliminate the effects of soil microbial diversity on ecosystem functions in experimental microcosms. Nature Communications13, 4260.

[53] Yeoh, Y.K., Dennis, P.G., Paungfoo-Lonhienne, C., Weber, L., Brackin, R., Ragan, M.A., Schmidt, S., Hugenholtz, P., 2017. Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence. Nature Communications8, 215.

[54] Zhang, X.B., Wu, L.H., Sun, N., Ding, X.S., Li, J.W., Wang, B.R., Li, D.C., 2014. Soil CO₂ and N₂O emissions in maize growing season under different fertilizer regimes in an upland red soil region of South China. Journal of Integrative Agriculture13, 604–614.

[55] Zhu, D., Delgado-Baquerizo, M., Su, J.Q., Ding, J., Li, H., Gillings, M.R., Penuelas, J., Zhu, Y.G., 2021. Deciphering potential roles of earthworms in mitigation of antibiotic resistance in the soils from diverse ecosystems. Environmental Science & Technology55, 7445–7455.

Acknowledgments

This work was supported by the National Key Research and Development Program of China (Grant No. 2021YFD1901201-05), the National Natural Science Foundation of China (Grant No. 41661052), Agricultural Projects Jiangxi Province (Grant No. JXNK202307-01), Special Program for Basic Research and Talent Training of Jiangxi Academy of Agricultural Sciences (Grant No. JXSNKYJCRC202301), the Outstanding Youth Research Project of Anhui Province (Grant No. 2022AH030015).

Data availability

The datasets for this study can be found in SRA of the NCBI under accession number PRJNA1009978.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-024-0241-7 and is accessible for authorized users.

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