Bacterial biogeography in China and its association to land use and soil organic carbon

Tao Lu, Nuohan Xu, Chaotang Lei, Qi Zhang, Zhenyan Zhang, Liwei Sun, Feng He, Ning-Yi Zhou, Josep Peñuelas, Yong-Guan Zhu, Haifeng Qian

PDF(7100 KB)
PDF(7100 KB)
Soil Ecology Letters ›› 2023, Vol. 5 ›› Issue (4) : 230172. DOI: 10.1007/s42832-023-0172-8
RESEARCH ARTICLE

Bacterial biogeography in China and its association to land use and soil organic carbon

Author information +
History +

Highlights

● 6102 high-quality sequencing results of soil bacterial samples were re-analyzed.

● The type of land use was the principal driver of bacterial richness and diversity.

● SOC content is positively correlated with key bacteria and total nitrogen content.

Abstract

Soil organic carbon (SOC) is the largest pool of carbon in terrestrial ecosystems and plays a crucial role in regulating atmospheric CO2 concentrations. Identifying the essential relationship between soil bacterial communities and SOC concentration is complicated because of many factors, one of which is geography. We systematically re-analyzed 6102 high-quality bacterial samples in China to delineate the bacterial biogeographic distribution of bacterial communities and identify key species associated with SOC concentration at the continental scale. The type of land use was the principal driver of bacterial richness and diversity, and we used machine learning to calculate its influence on microbial composition and their co-occurrence relationship with SOC concentration. Cultivated land was much more complex than forest, grassland, wetland and wasteland, with high SOC concentrations tending to enrich bacteria such as Rubrobacter, Terrimonas and Sphingomona. SOC concentration was positively correlated with the amounts of soil total nitrogen and key bacteria Xanthobacteraceae, Streptomyces and Acidobacteria but was negatively correlated with soil pH, total phosphorus and Micrococcaceae. Our study combined the SOC pool with bacteria and indicated that specific bacteria may be key factors affecting SOC concentration, forcing us to think about microbial communities associated with climate change in a new way.

Graphical abstract

Keywords

biogeography / soil organic carbon / land-use type / machine learning

Cite this article

Download citation ▾
Tao Lu, Nuohan Xu, Chaotang Lei, Qi Zhang, Zhenyan Zhang, Liwei Sun, Feng He, Ning-Yi Zhou, Josep Peñuelas, Yong-Guan Zhu, Haifeng Qian. Bacterial biogeography in China and its association to land use and soil organic carbon. Soil Ecology Letters, 2023, 5(4): 230172 https://doi.org/10.1007/s42832-023-0172-8

References

[1]
Bardgett, R.D., Freeman, C., Ostle, N.J., 2008. Microbial contributions to climate change through carbon cycle feedbacks. ISME Journal2, 805–814.
CrossRef Google scholar
[2]
Benner, R., 2011. Biosequestration of carbon by heterotrophic microorganisms. Nature Reviews Microbiology9, 75.
CrossRef Google scholar
[3]
Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N., 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-Rodriguez, 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.J., Kaehler, B.D., Kang, 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, M.S. II, 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., Wang, M., Warren, J., Weber, K.C., Williamson, C.H.D., Willis, A.D., Xu, Z.Z., Zaneveld, J.R., Zhang, Y., Zhu, Q., Knight, R., Caporaso, J.G., 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology37, 852–857.
CrossRef Google scholar
[4]
Bond-Lamberty, B., Bailey, V.L., Chen, M., Gough, C.M., Vargas, R., 2018. Globally rising soil heterotrophic respiration over recent decades. Nature560, 80–83.
CrossRef Google scholar
[5]
Bossio, D.A., Cook-Patton, S.C., Ellis, P.W., Fargione, J., Sanderman, J., Smith, P., Wood, S., Zomer, R.J., von Unger, M., Emmer, I.M., Griscom, B.W., 2020. The role of soil carbon in natural climate solutions. Nature Sustainability3, 391–398.
CrossRef Google scholar
[6]
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.
CrossRef Google scholar
[7]
Chen, J.M., Ju, W.M., Ciais, P., Viovy, N., Liu, R.G., Liu, Y., Lu, X.H., 2019. Vegetation structural change since 1981 significantly enhanced the terrestrial carbon sink. Nature Communications10, 4259.
CrossRef Google scholar
[8]
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 & Biochemistry141, 107686.
CrossRef Google scholar
[9]
Davidson, E.A., Janssens, I.A., 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature440, 165–173.
CrossRef Google scholar
[10]
Delgado-Baquerizo, M., Oliverio, A.M., Brewer, T.E., Benavent-Gonzalez, 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.
CrossRef Google scholar
[11]
Domeignoz-Horta, L.A., Pold, G., Liu, X.J.A., Frey, S.D., Melillo, J.M., DeAngelis, K.M., 2020. Microbial diversity drives carbon use efficiency in a model soil. Nature Communications11, 3684.
CrossRef Google scholar
[12]
Duan, Y., Chen, L., Li, Y.M., Wang, Q.Y., Zhang, C.Z., Ma, D.H., Li, J.Y., Zhang, J.B., 2021. N, P and straw return influence the accrual of organic carbon fractions and microbial traits in a Mollisol. Geoderma403, 115373.
CrossRef Google scholar
[13]
Fu, Y.Y., Luo, Y., Auwal, M., Singh, B.P., Van Zwieten, L., Xu, J.M., 2022. Biochar accelerates soil organic carbon mineralization via rhizodeposit-activated Actinobacteria. Biology and Fertility of Soils58, 565–577.
CrossRef Google scholar
[14]
Hashimoto, S., Carvalhais, N., Ito, A., Migliavacca, M., Nishina, K., Reichstein, M., 2015. Global spatiotemporal distribution of soil respiration modeled using a global database. Biogeosciences12, 4121–4132.
CrossRef Google scholar
[15]
Heimann, M., Reichstein, M., 2008. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature451, 289–292.
CrossRef Google scholar
[16]
Hong, S.H., Ham, S.Y., Kim, J.S., Kim, I.S., Lee, E.Y., 2016. Application of sodium polyacrylate and plant growth-promoting bacterium, Micrococcaceae HW-2, on the growth of plants cultivated in the rooftop. International Biodeterioration & Biodegradation113, 297–303.
CrossRef Google scholar
[17]
Huang, N., Wang, L., Song, X.P., Black, T.A., Jassal, R.S., Myneni, R.B., Wu, C.Y., Wang, L., Song, W.J., Ji, D.B., Yu, S.S., Niu, Z., 2020. Spatial and temporal variations in global soil respiration and their relationships with climate and land cover. Science Advances6, eabb8508.
CrossRef Google scholar
[18]
Jian, J.S., Steele, M.K., Thomas, R.Q., Day, S.D., Hodges, S.C., 2018. Constraining estimates of global soil respiration by quantifying sources of variability. Global Change Biology24, 4143–4159.
CrossRef Google scholar
[19]
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. ISME Journal14, 202–216.
CrossRef Google scholar
[20]
Kallenbach, C.M., Frey, S.D., Grandy, A.S., 2016. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nature Communications7, 13630.
CrossRef Google scholar
[21]
King, G.M., 2011. Enhancing soil carbon storage for carbon remediation: potential contributions and constraints by microbes. Trends in Microbiology19, 75–84.
CrossRef Google scholar
[22]
Kraychenko, A.N., Guber, A.K., Razavi, B.S., Koestel, J., Quigley, M.Y., Robertson, G.P., Kuzyakov, Y., 2019. Microbial spatial footprint as a driver of soil carbon stabilization. Nature Communications10, 3121.
CrossRef Google scholar
[23]
Lei, J.S., Guo, X., Zeng, Y.F., Zhou, J.Z., Gao, Q., Yang, Y.F., 2021. Temporal changes in global soil respiration since 1987. Nature Communications12, 403.
CrossRef Google scholar
[24]
Liang, C., 2020. Soil microbial carbon pump: Mechanism and appraisal. Soil Ecology Letters2, 241–254.
CrossRef Google scholar
[25]
Liang, C., Schimel, J.P., Jastrow, J.D., 2017. The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology2, 17105.
CrossRef Google scholar
[26]
Liu, C.X., Dong, Y.H., Hou, L.Y., Deng, N., Jiao, R.Z., 2017. Acidobacteria community responses to nitrogen dose and form in chinese fir plantations in Southern China. Current Microbiology74, 396–403.
CrossRef Google scholar
[27]
Liu, F., Rossiter, D.G., Zhang, G.L., Li, D.C., 2020a. A soil colour map of China. Geoderma379, 114556.
CrossRef Google scholar
[28]
Liu, F., Wu, H.Y., Zhao, Y.G., Li, D.C., Yang, J.L., Song, X.D., Shi, Z., Zhu, A.X., Zhang, G.L., 2022. Mapping high resolution National Soil Information Grids of China. Science Bulletin67, 328–340.
CrossRef Google scholar
[29]
Liu, F., Zhang, G.L., Song, X.D., Li, D.C., Zhao, Y.G., Yang, J.L., Wu, H.Y., Yang, F., 2020b. High-resolution and three-dimensional mapping of soil texture of China. Geoderma361, 114061.
CrossRef Google scholar
[30]
Llado, S., Zifcakova, L., Vetrovsky, T., Eichlerova, I., Baldrian, P., 2016. Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision 1 for polysaccharide decomposition. Biology and Fertility of Soils52, 251–260.
CrossRef Google scholar
[31]
Lu, T., Ke, M.J., Lavoie, M., Jin, Y.J., Fan, X.J., Zhang, Z.Y., Fu, Z.W., Sun, L.W., Gillings, M., Penuelas, J., Qian, H.F., Zhu, Y.G., 2018. Rhizosphere microorganisms can influence the timing of plant flowering. Microbiome6, 231.
CrossRef Google scholar
[32]
Ludwig, M., Achtenhagen, J., Miltner, A., Eckhardt, K.U., Leinweber, P., Emmerling, C., Thiele-Bruhn, S., 2015. Microbial contribution to SOM quantity and quality in density fractions of temperate arable soils. Soil Biology & Biochemistry81, 311–322.
CrossRef Google scholar
[33]
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. ISME Journal10, 1891–1901.
CrossRef Google scholar
[34]
Ni, H.W., Jing, X.Y., Xiao, X., Zhang, N., Wang, X.Y., Sui, Y.Y., Sun, B., Liang, Y.T., 2021. Microbial metabolism and necromass mediated fertilization effect on soil organic carbon after long-term community incubation in different climates. ISME Journal15, 2561–2573.
CrossRef Google scholar
[35]
Piao, S.L., Wang, X.H., Park, T., Chen, C., Lian, X., He, Y., Bjerke, J.W., Chen, A.P., Ciais, P., Tommervik, H., Nemani, R.R., Myneni, R.B., 2020. Characteristics, drivers and feedbacks of global greening. Nature Reviews Earth & Environment1, 14–27.
CrossRef Google scholar
[36]
Schimel, J.P., Schaeffer, S.M., 2012. Microbial control over carbon cycling in soil. Frontiers in Microbiology3, 348.
CrossRef Google scholar
[37]
Schmidt, M.W.I., Torn, M.S., Abiven, S., Dittmar, T., Guggenberger, G., Janssens, I.A., Kleber, M., Kogel-Knabner, I., Lehmann, J., Manning, D.A.C., Nannipieri, P., Rasse, D.P., Weiner, S., Trumbore, S.E., 2011. Persistence of soil organic matter as an ecosystem property. Nature478, 49–56.
CrossRef Google scholar
[38]
Shao, P., Li, T., Dong, K., Yang, H., Sun, J., 2021. Microbial residues as the nexus transforming inorganic carbon to organic carbon in coastal saline soils. Soil Ecology Letters4, 328–336.
[39]
Sokol, N.W., Slessarev, E., Marschmann, G.L., Nicolas, A., Blazewicz, S.J., Brodie, E.L., Firestone, M.K., Foley, M.M., Hestrin, R., Hungate, B.A., Koch, B.J., Stone, B.W., Sullivan, M.B., Zablocki, O., Pett-Ridge, J., Consortium, L.S.M., 2022. Life and death in the soil microbiome: how ecological processes influence biogeochemistry. Nature Reviews Microbiology20, 415–430.
CrossRef Google scholar
[40]
Stone, B.W., Li, J.H., Koch, B.J., Blazewicz, S.J., Dijkstra, P., Hayer, M., Hofmockel, K.S., Liu, X.J.A., Mau, R.L., Morrissey, E.M., Pett-Ridge, J., Schwartz, E., Hungate, B.A., 2021. Nutrients cause consolidation of soil carbon flux to small proportion of bacterial community. Nature Communications12, 3381.
CrossRef Google scholar
[41]
Wang, B.R., An, S.S., Liang, C., Liu, Y., Kuzyakov, Y., 2021a. Microbial necromass as the source of soil organic carbon in global ecosystems. Soil Biology & Biochemistry162, 108422.
CrossRef Google scholar
[42]
Wang, S., Chen, X., Li, D., Wu, J., 2021b. Effects of soil organism interactions and temperature on carbon use efficiency in three different forest soils. Soil Ecology Letters3, 156–166.
CrossRef Google scholar
[43]
Wei, Z., Gu, Y., Friman, V.P., Kowalchuk, G.A., Xu, Y.C., Shen, Q.R., Jousset, A., 2019. Initial soil microbiome composition and functioning predetermine future plant health. Science Advances5, eaaw0759.
CrossRef Google scholar
[44]
Wemheuer, F., Taylor, J.A., Daniel, R., Johnston, E., Meinicke, P., Thomas, T., Wemheuer, B., 2020. Tax4Fun2: prediction of habitat-specific functional profiles and functional redundancy based on 16S rRNA gene sequences. Environmental Microbiology15, 11.
CrossRef Google scholar
[45]
Wiesmeier, M., Urbanski, L., Hobley, E., Lang, B., von Lutzow, M., Marin-Spiotta, E., van Wesemael, B., Rabot, E., Liess, M., Garcia-Franco, N., Wollschlager, U., Vogel, H.J., Kogel-Knabner, I., 2019. Soil organic carbon storage as a key function of soils - A review of drivers and indicators at various scales. Geoderma333, 149–162.
CrossRef Google scholar
[46]
Xia, L.L., Lam, S.K., Wolf, B., Kiese, R., Chen, D.L., Butterbach-Bahl, K., 2018. Trade-offs between soil carbon sequestration and reactive nitrogen losses under straw return in global agroecosystems. Global Change Biology24, 5919–5932.
CrossRef Google scholar
[47]
Xu, L., Zhang, B., Wang, E., Zhu, B., Yao, M., Li, C., Li, X., 2021. Soil total organic carbon/total nitrogen ratio as a key driver deterministically shapes diazotrophic community assemblages during the succession of biological soil crusts. Soil Ecology Letters3, 328–341.
CrossRef Google scholar
[48]
Zhang, Q., Qin, W., Feng, J., Zhu, B., 2022a. Responses of soil microbial carbon use efficiency to warming: Review and prospects. Soil Ecology Letters4, 307–318.
CrossRef Google scholar
[49]
Zhang, Q., Zhang, Z.Y., Lu, T., Yu, Y.T., Penuelas, J., Zhu, Y.G., Qian, H.F., 2021. Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutants. Microbiome9, 196.
CrossRef Google scholar
[50]
Zhang, Z.Y., Zhang, Q., Cui, H.Z., Li, Y., Xu, N.H., Lu, T., Chen, J., Penuelas, J., Hu, B.L., Qian, H.F., 2022b. Composition identification and functional verification of bacterial community in disease-suppressive soils by machine learning. Environmental Microbiology24, 3405–3419.
CrossRef Google scholar
[51]
Zhang, Z.Y., Zhang, Q., Wang, T.Z., Xu, N.H., Lu, T., Hong, W.J., Penuelas, J., Gillings, M., Wang, M.X., Gao, W.W., Qian, H.F., 2022c. Assessment of global health risk of antibiotic resistance genes. Nature Communications13, 1553.
CrossRef Google scholar
[52]
Zhao, Y.C., Wang, M.Y., Hu, S.J., Zhang, X.D., Ouyang, Z., Zhang, G.L., Huang, B.A., Zhao, S.W., Wu, J.S., Xie, D.T., Zhu, B., Yu, D.S., Pan, X.Z., Xu, S.X., Shi, X.Z., 2018. Economics- and policy-driven organic carbon input enhancement dominates soil organic carbon accumulation in Chinese croplands. Proceedings of the National Academy of Sciences of the United States of America115, 4045–4050.
CrossRef Google scholar
[53]
Zhu, X.F., Jackson, R.D., DeLucia, E.H., Tiedje, J.M., Liang, C., 2020. The soil microbial carbon pump: From conceptual insights to empirical assessments. Global Change Biology26, 6032–6039.
CrossRef Google scholar

Data availability

All raw data used in this study are available in NCBI RefSeq database. Bioproject numbers of all samples are provided in Table S1.

Acknowledgments

We appreciate Liu et al. for their latest data (Liu et al., 2020a, 2020b, 2022) on national SOC, pH, as well as the contents of total nitrogen, phosphorus and potassium. Funding was provided by the Key R&D Program of Zhejiang Province (2022C02046 and 2022C02029), and the National Natural Science Foundation of China (21976161 and 21777145). J.P. acknowledges funding from the Spanish Government grant PID2019-110521GB-I00, the Fundación Ramón Areces grant CIVP20A6621, and the Catalan Government grant SGR2017-1005.

Author contributions

The contribution of our research article is: Haifeng Qian, Yong-Guan Zhu, and Ning-Yi Zhou conceived the study; Chaotang Lei, Qi Zhang, Zhenyan Zhang and Liwei Sun collected the data; Nuohan Xu and Tao Lu analyzed the data; Tao Lu, Nuohan Xu, Feng He, Josep Peñuelas and Haifeng Qian wrote the manuscript.

Ethics declarations

The authors declare that they have no competing interests.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-023-0172-8 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2023 Higher Education Press
审图号:GS京(2023)0915号
AI Summary AI Mindmap
PDF(7100 KB)

Accesses

Citations

Detail

Sections
Recommended

/