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Conversion of steppe to cropland increases spatial heterogeneity of soil functional genes

The ISME Journal volume 17, pages 1872–1883 (2023)Cite this article

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Abstract

The microbiome function responses to land use change are important for the long-term prediction and management of soil ecological functions under human influence. However, it has remains uncertain how the biogeographic patterns of soil functional composition change when transitioning from natural steppe soils (NS) to agricultural soils (AS). We collected soil samples from adjacent pairs of AS and NS across 900 km of Mollisol areas in northeast China, and the soil functional composition was characterized using shotgun sequencing. AS had higher functional alpha-diversity indices with respect to KO trait richness and a higher Shannon index than NS. The distance-decay slopes of functional gene composition were steeper in AS than in NS along both spatial and environmental gradients. Land-use conversion from steppe to farmland diversified functional gene profiles both locally and spatially; it increased the abundances of functional genes related to labile carbon, but decreased those related to recalcitrant substrate mobilization (e.g., lignin), P cycling, and S cycling. The composition of gene functional traits was strongly driven by stochastic processes, while the degree of stochasticity was higher in NS than in AS, as revealed by the neutral community model and normalized stochasticity ratio analysis. Alpha-diversity of core functional genes was strongly related to multi-nutrient cycling in AS, suggesting a key relationship to soil fertility. The results of this study challenge the paradigm that the conversion of natural to agricultural habitat will homogenize soil properties and biology while reducing local and regional gene functional diversity.

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Fig. 1: General spatial distributions of functional alpha- and beta-diversity in agricultural (AS) and natural soils (NS).
Fig. 2: Assembly mechanisms of functional genes in agricultural (AS) and natural soils (NS).
Fig. 3: Distance-decay relationships between the similarity of the functional genes and geographic distance and environmental dissimilarity distance.
Fig. 4: The key environmental drivers and ecological clusters of the functional genes identified in agricultural (AS) and natural soils (NS).
Fig. 5: Ecological roles of the functional genes in agricultural (AS) and natural soils (NS) as shown in the co-occurrence networks based on Spearman’s correlation analysis.
Fig. 6: Analysis of functional gene differences between agricultural (AS) and natural soils (NS).

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Data availability

The raw sequence data of this study have been deposited into the Genome Sequence Archive (GSA) database under accession number of CRA004163, which were publicly accessible at. All code used for processing and analyzing the data is available in this GitHub repository [https://github.com/Microbion/2022-Conversion-of-steppe-to-agriculture].

References

  1. Forrest JR, Thorp RW, Kremen C, Williams NM. Contrasting patterns in species and functional-trait diversity of bees in an agricultural landscape. J Appl Ecol. 2015;52:706–15.

    Google Scholar 

  2. Mbuthia LW, Acosta-Martínez V, DeBruyn J, Schaeffer S, Tyler D, Odoi E, et al. Long term tillage, cover crop, and fertilization effects on microbial community structure, activity: implications for soil quality. Soil Biol Biochem. 2015;89:24–34.

    CAS  Google Scholar 

  3. Xun W, Xu Z, Li W, Ren Y, Huang T, Ran W, et al. Long-term organic-inorganic fertilization ensures great soil productivity and bacterial diversity after natural to agricultural ecosystem conversion. J Microbiol. 2016;54:611–7.

    CAS  PubMed  Google Scholar 

  4. Cornell CR, Zhang Y, Ning D, Wu L, Wagle P, Steiner JL, et al. Temporal dynamics of bacterial communities along a gradient of disturbance in a US Southern Plains agroecosystem. mBio 2022;13:e03829–21.

    PubMed  PubMed Central  Google Scholar 

  5. Borrelli P, Robinson DA, Panagos P, Lugato E, Yang JE, Alewell C, et al. Land use and climate change impacts on global soil erosion by water (2015-2070). Proc Natl Acad Sci USA. 2020;117:21994–2001.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Gupta A, Singh UB, Sahu PK, Paul S, Kumar A, Malviya D, et al. Linking soil microbial diversity to modern agriculture practices: a review. Int J Environ Res Public Health. 2022;19:3141.

    PubMed  PubMed Central  Google Scholar 

  7. Göpel J, Schüngel J, Stuch B, Schaldach R. Assessing the effects of agricultural intensification on natural habitats and biodiversity in Southern Amazonia. PloS One. 2020;15:e0225914.

    PubMed  PubMed Central  Google Scholar 

  8. Šálek M, Kalinová K, Daňková R, Grill S, Żmihorski M. Reduced diversity of farmland birds in homogenized agricultural landscape: a cross-border comparison over the former Iron Curtain. Agric Ecosyst Environ. 2021;321:107628.

    Google Scholar 

  9. Tripathi BM, Edwards DP, Mendes LW, Kim M, Dong K, Kim H, et al. The impact of tropical forest logging and oil palm agriculture on the soil microbiome. Mol Ecol. 2016;25:2244–57.

    CAS  PubMed  Google Scholar 

  10. Philippot L, Spor A, Hénault C, Bru D, Bizouard F, Jones CM, et al. Loss in microbial diversity affects nitrogen cycling in soil. ISME J. 2013;7:1609–19.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Wang GH, Jin J, Liu JJ, Chen XL, Liu JD, Liu XB. Bacterial community structure in a mollisol under long-term natural restoration, cropping, and bare fallow history estimated by PCR-DGGE. Pedosphere. 2009;19:156–65.

    CAS  Google Scholar 

  12. Delgado-Baquerizo M, Eldridge DJ, Liu YR, Sokoya B, Wang JT, Hu HW, et al. Global homogenization of the structure and function in the soil microbiome of urban greenspaces. Sci Adv. 2021;7:eabg5809.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Hartmann FE, McDonald BA, Croll D. Genome-wide evidence for divergent selection between populations of a major agricultural pathogen. Mol Ecol. 2018;27:2725–41.

    PubMed  PubMed Central  Google Scholar 

  14. Hufnagel J, Reckling M, Ewert F. Diverse approaches to crop diversification in agricultural research. A review. Agron Sustain Dev. 2020;40:1–17.

    Google Scholar 

  15. Duan Y, Wang X, Wang L, Lian J, Wang W, Wu F, et al. Biogeographic patterns of soil microbe communities in the deserts of the Hexi Corridor, northern China. Catena. 2022;211:106026.

    Google Scholar 

  16. Zhu W, Zhu M, Liu X, Xia J, Yin H, Li X. Different responses of bacteria and microeukaryote to assembly processes and co-occurrence pattern in the coastal upwelling. Microb Ecol. 2022;86:174–86.

    PubMed  Google Scholar 

  17. Gong X, Liu X, Li Y, Ma K, Song W, Zhou J, et al. Distinct ecological processes mediate domain-level differentiation in microbial spatial scaling. Appl Environ Microbiol. 2023;89:e02096–22.

    PubMed  PubMed Central  Google Scholar 

  18. Feng M, Tripathi BM, Shi Y, Adams JM, Zhu YG, Chu H. Interpreting distance‐decay pattern of soil bacteria via quantifying the assembly processes at multiple spatial scales. MicrobiologyOpen 2019;8:e00851.

    PubMed  PubMed Central  Google Scholar 

  19. Clark DR, Underwood GJ, McGenity TJ, Dumbrell AJ. What drives study‐dependent differences in distance-decay relationships of microbial communities? Glob Ecol Biogeogr. 2021;30:811–25.

    Google Scholar 

  20. Schadt CW, Chen H, Ma K, Lu C, Fu Q, Qiu Y, et al. Functional redundancy in soil microbial community based on metagenomics across the globe. Front Microbiol. 2022;13:87897.

    Google Scholar 

  21. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T. Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA. 2011;108:14288–93.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, et al. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci USA. 2012;109:21390–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Guan X, Wang J, Zhao H, Wang J, Luo X, Liu F, et al. Soil bacterial communities shaped by geochemical factors and land use in a less-explored area, Tibetan Plateau. BMC Genom. 2013;14:1–13.

    Google Scholar 

  24. Manoharan L, Kushwaha SK, Ahrén D, Hedlund K. Agricultural land use determines functional genetic diversity of soil microbial communities. Soil Biol Biochem. 2017;115:423–32.

    CAS  Google Scholar 

  25. Monteux S, Keuper F, Fontaine S, Gavazov K, Hallin S, Juhanson J, et al. Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations. Nat Geosci. 2020;13:794–8.

    CAS  Google Scholar 

  26. Aryal B, Gurung R, Camargo AF, Fongaro G, Treichel H, Mainali B, et al. Nitrous oxide emission in altered nitrogen cycle and implications for climate change. Environ Pollut. 2022;314:120272.

    CAS  PubMed  Google Scholar 

  27. Mohapatra M, Yadav R, Rajput V, Dharne MS, Rastogi G. Metagenomic analysis reveals genetic insights on biogeochemical cycling, xenobiotic degradation, and stress resistance in mudflat microbiome. J Environ Manag. 2021;292:112738.

    CAS  Google Scholar 

  28. Merloti LF, Mendes LW, Pedrinho A, de Souza LF, Ferrari BM, Tsai SM. Forest to agriculture conversion in Amazon drives soil microbial communities and N-cycle. Soil Biol Biochem. 2019;137:107567.

    CAS  Google Scholar 

  29. Chen Y, Yang X, Fu W, Chen B, Hu H, Feng K, et al. Conversion of natural grassland to cropland alters microbial community assembly across northern China. Environ Microbiol. 2022;24:5630–42.

    CAS  PubMed  Google Scholar 

  30. Jiao S, Xu Y, Zhang J, Hao X, Lu Y. Core microbiota in agricultural soils and their potential associations with nutrient cycling. Msystems 2019;4:e00313–18.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Jiao S, Chen W, Wei G. Core microbiota drive functional stability of soil microbiome in reforestation ecosystems. Glob Change Biol. 2022;28:1038–47.

    CAS  Google Scholar 

  32. Shi Q, Wang T, Lee C. MEMS based broadband piezoelectric ultrasonic energy harvester (PUEH) for enabling self-powered implantable biomedical devices. Sci Rep. 2016;6:1–10.

    CAS  Google Scholar 

  33. Liu X, Lee Burras C, Kravchenko YS, Duran A, Huffman T, Morras H, et al. Overview of mollisols in the world: distribution, land use and management. Can J Soil Sci. 2012;92:383–402.

    CAS  Google Scholar 

  34. Walsh MG, de Smalen AW, Mor SM. Climatic influence on anthrax suitability in warming northern latitudes. Sci Rep. 2018;8:9269.

    PubMed  PubMed Central  Google Scholar 

  35. Chendev YG, Sauer TJ, Hernandez Ramirez G, Burras CL. History of east European chernozem soil degradation; protection and restoration by tree windbreaks in the Russian steppe. Sustainability .2015;7:705–24.

    Google Scholar 

  36. Stakhurlova L, Svistova I, Shcheglov D. Biological activity as an indicator of chernozem fertility in different biocenoses. Eurasia Soil Sci. 2007;40:694–9.

    Google Scholar 

  37. Eremin D. Changes in the content and quality of humus in leached chernozems of the Trans-Ural forest-steppe zone under the impact of their agricultural use. Eurasia Soil Sci. 2016;49:538–45.

    CAS  Google Scholar 

  38. Lal R. Managing soils and ecosystems for mitigating anthropogenic carbon emissions and advancing global food security. BioScience 2010;60:708–21.

    Google Scholar 

  39. Zhang Y, Liang A, Wang Y, Chen X, Zhang S, Jia S, et al. Climate change impacts on soil fertility in Chinese Mollisols. In Sustainable Crop Productivity and Quality under Climate Change. Academic Press: Cambridge, MA, USA, 2022. pp 275–93.

  40. Shi Y, Li Y, Xiang X, Sun R, Yang T, He D, et al. Spatial scale affects the relative role of stochasticity versus determinism in soil bacterial communities in wheat fields across the North China Plain. Microbiome. 2018;6:1–12.

    CAS  Google Scholar 

  41. Paul BG, Burstein D, Castelle CJ, Handa S, Arambula D, Czornyj E, et al. Retroelement-guided protein diversification abounds in vast lineages of Bacteria and Archaea. Nat Microbiol. 2017;2:1–7.

    Google Scholar 

  42. Zhang T, Qiao Q, Novikova PY, Wang Q, Yue J, Guan Y, et al. Genome of Crucihimalaya himalaica, a close relative of Arabidopsis, shows ecological adaptation to high altitude. Proc Natl Acad Sci USA. 2019;116:7137–46.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11:1–9.

    Google Scholar 

  44. Anderson M PCO: a FORTRAN computer program for principal coordinate analysis. Department of Statistics, University of Auckland, New Zealand. 2003.

  45. Anderson MJ Permutational multivariate analysis of variance. In Wiley StatsRef: Statistics Reference Online. Wiley: Hoboken, NJ, USA, 2017. pp 1–5.

  46. Liaw A, Wiener M. Classification and regression by randomForest. R News. 2002;2:18–22.

    Google Scholar 

  47. Chen QL, Xiang Q, Sun AQ, Hu HW. Aridity differentially alters the stability of soil bacterial and fungal networks. Environ Microbiol. 2022;24:5574–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Ma B, Stirling E, Liu Y, Zhao K, Zhou J, Singh BK, et al. Soil biogeochemical cycle couplings inferred from a function-taxon network. Research 2021;2021:7102769.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Ma B, Zhao K, Lv X, Su W, Dai Z, Gilbert JA, et al. Genetic correlation network prediction of forest soil microbial functional organization. ISME J. 2018;12:2492–505.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun. 2016;7:10541.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Flynn DF, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, et al. Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett. 2009;12:22–33.

    PubMed  Google Scholar 

  52. Milder JC, Clark S. Conservation development practices, extent, and land-use effects in the United States. Conserv Biol. 2011;25:697–707.

    PubMed  Google Scholar 

  53. Mayfield MM, Bonser S, Morgan J, Aubin I, McNamara S, Vesk P. What does species richness tell us about functional trait diversity? Predictions and evidence for responses of species and functional trait diversity to land-use change. Glob Ecol Biogeogr. 2010;19:423–31.

    Google Scholar 

  54. Farneda FZ, Grelle CE, Rocha R, Ferreira DF, López-Baucells A, Meyer CF. Predicting biodiversity loss in island and countryside ecosystems through the lens of taxonomic and functional biogeography. Ecography. 2020;43:97–106.

    Google Scholar 

  55. Trivedi C, Delgado-Baquerizo M, Hamonts K, Lai K, Reich PB, Singh BK. Losses in microbial functional diversity reduce the rate of key soil processes. Soil Biol Biochem. 2019;135:267–74.

    CAS  Google Scholar 

  56. Verbruggen E, Toby, Kiers E. Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl. 2010;3:547–60.

    PubMed  PubMed Central  Google Scholar 

  57. Estel S, Kuemmerle T, Levers C, Baumann M, Hostert P. Mapping cropland-use intensity across Europe using MODIS NDVI time series. Environ Res Lett. 2016;11:024015.

    Google Scholar 

  58. Menta C Soil fauna diversity-function, soil degradation, biological indices, soil restoration. In: Lameed, GA (eds). Biodiversity Conservation and Utilization in a Diverse World. IntechOpen, London, UK, 2012. pp 59–94.

  59. Prinzing A, Reiffers R, Braakhekke WG, Hennekens SM, Tackenberg O, Ozinga WA, et al. Less lineages–more trait variation: phylogenetically clustered plant communities are functionally more diverse. Ecol Lett. 2008;11:809–19.

    PubMed  Google Scholar 

  60. Homburg JA, Sandor JA. Anthropogenic effects on soil quality of ancient agricultural systems of the American Southwest. Catena. 2011;85:144–54.

    Google Scholar 

  61. Crow WT, Berg AA, Cosh MH, Loew A, Mohanty BP, Panciera R, et al. Upscaling sparse ground-based soil moisture observations for the validation of coarse-resolution satellite soil moisture products. Rev Geophys. 2012;50:GT2002.

    Google Scholar 

  62. Frainer A, Primicerio R, Kortsch S, Aune M, Dolgov AV, et al. Climate-driven changes in functional biogeography of Arctic marine fish communities. Proc Natl Acad Sci USA. 2017;114:12202–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Rey A, Pegoraro E, Oyonarte C, Were A, Escribano P, Raimundo J. Impact of land degradation on soil respiration in a steppe (Stipa tenacissima L.) semi-arid ecosystem in the SE of Spain. Soil Biol Biochem. 2011;43:393–403.

    CAS  Google Scholar 

  64. He Z, Xu M, Deng Y, Kang S, Kellogg L, Wu L, et al. Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. Ecol Lett. 2010;13:564–75.

    PubMed  Google Scholar 

  65. Su JQ, Ding LJ, Xue K, Yao HY, Quensen J, Bai SJ, et al. Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. Mol Ecol. 2015;24:136–50.

    CAS  PubMed  Google Scholar 

  66. Poeplau C, Don A, Vesterdal L, Leifeld J, Van Wesemael B, Schumacher J, et al. Temporal dynamics of soil organic carbon after land-use change in the temperate zone-carbon response functions as a model approach. Glob Change Biol. 2011;17:2415–27.

    Google Scholar 

  67. Bischoff N, Mikutta R, Shibistova O, Puzanov A, Reichert E, Silanteva M, et al. Land-use change under different climatic conditions: Consequences for organic matter and microbial communities in Siberian steppe soils. Agric, Ecosyst Environ. 2016;235:253–64.

    Google Scholar 

  68. Jacinthe P-A, Lal R. Labile carbon and methane uptake as affected by tillage intensity in a Mollisol. Soil Tillage Res. 2005;80:35–45.

    Google Scholar 

  69. Yuan H, Ge T, Chen X, Liu S, Zhu Z, Wu X, et al. Abundance and diversity of CO2-assimilating bacteria and algae within red agricultural soils are modulated by changing management practice. Micro Ecol. 2015;70:971–80.

    CAS  Google Scholar 

  70. Xiao KQ, Ge TD, Wu XH, Peacock CL, Zhu ZK, Peng J, et al. Metagenomic and 14C tracing evidence for autotrophic microbial CO2 fixation in paddy soils. Environ Microbiol. 2021;23:924–33.

    CAS  PubMed  Google Scholar 

  71. Anderson-Teixeira KJ, Masters MD, Black CK, Zeri M, Hussain MZ, Bernacchi CJ, et al. Altered belowground carbon cycling following land-use change to perennial bioenergy crops. Ecosystems. 2013;16:508–20.

    CAS  Google Scholar 

  72. Yu L, Luo S, Xu X, Gou Y, Wang J. The soil carbon cycle determined by GeoChip 5.0 in sugarcane and soybean intercropping systems with reduced nitrogen input in South China. Appl Soil Ecol. 2020;155:103653.

    Google Scholar 

  73. Dobbelaere S, Vanderleyden J, Okon Y. Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci. 2003;22:107–49.

    CAS  Google Scholar 

  74. Blaud A, van der Zaan B, Menon M, Lair GJ, Zhang D, Huber P, et al. The abundance of nitrogen cycle genes and potential greenhouse gas fluxes depends on land use type and little on soil aggregate size. Appl Soil Ecol. 2018;125:1–11.

    Google Scholar 

  75. Schmidt CS, Richardson DJ, Baggs EM. Constraining the conditions conducive to dissimilatory nitrate reduction to ammonium in temperate arable soils. Soil Biol Biochem. 2011;43:1607–11.

    CAS  Google Scholar 

  76. Gao W, Kou L, Yang H, Zhang J, Müller C, Li S. Are nitrate production and retention processes in subtropical acidic forest soils responsive to ammonium deposition? Soil Biol Biochem. 2016;100:102–9.

    CAS  Google Scholar 

  77. Stevens R, Laughlin R, Malone J. Soil pH affects the processes reducing nitrate to nitrous oxide and dinitrogen. Soil Biol Biochem. 1998;30:1119–26.

    CAS  Google Scholar 

  78. Zhang Y, Zheng X, Ren X, Zhang J, Misselbrook T, Cardenas L, et al. Land-use type affects nitrate production and consumption pathways in subtropical acidic soils. Geoderma .2019;337:22–31.

    CAS  Google Scholar 

  79. Zhu X, Burger M, Doane TA, Horwath WR. Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc Natl Acad Sci USA. 2013;110:6328–33.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Liang M, Frank S, Lünsdorf H, Warren MJ, Prentice MB. Bacterial microcompartment‐directed polyphosphate kinase promotes stable polyphosphate accumulation in E. coli. Biotechnol J. 2017;12:1600415.

    Google Scholar 

  81. Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, et al. Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil. 2011;349:121–56.

    CAS  Google Scholar 

  82. Bergkemper F, Schöler A, Engel M, Lang F, Krüger J, Schloter M, et al. Phosphorus depletion in forest soils shapes bacterial communities towards phosphorus recycling systems. Environ Microbiol. 2016;18:1988–2000.

    CAS  PubMed  Google Scholar 

  83. Yao Q, Li Z, Song Y, Wright SJ, Guo X, Tringe SG, et al. Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil. Nat Ecol Evol. 2018;2:499–509.

    PubMed  Google Scholar 

  84. Zhao FJ, Tausz M, De Kok LJ Role of sulfur for plant production in agricultural and natural ecosystems. In: R Hell, C Dahl, D Knaff, T Leustek (eds). Sulfur metabolism in phototrophic organisms. Advances in photosynthesis and respiration, vol. 27. Dordrecht, the Netherlands, Springer, 2008. pp 417–35.

  85. Edmeades D, Thorrold B, Roberts A. The diagnosis and correction of sulfur deficiency and the management of sulfur requirements in New Zealand pastures: a review. Aust J Exp Agric. 2005;45:1205–23.

    CAS  Google Scholar 

  86. Wang F, Liang Y, Jiang Y, Yang Y, Xue K, Xiong J, et al. Planting increases the abundance and structure complexity of soil core functional genes relevant to carbon and nitrogen cycling. Sci Rep. 2015;5:14345.

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Xie H, Huang Y, Chen Q, Zhang Y, Wu Q. Prospects for agricultural sustainable intensification: a review of research. Land. 2019;8:157.

    Google Scholar 

  88. Trivedi P, Mattupalli C, Eversole K, Leach JE. Enabling sustainable agriculture through understanding and enhancement of microbiomes. N. Phytol. 2021;230:2129–47.

    Google Scholar 

  89. Liu M, Zhang G, Yin F, Wang S, Li L. Relationship between biodiversity and ecosystem multifunctionality along the elevation gradient in alpine meadows on the eastern Qinghai-Tibetan plateau. Ecol Indic. 2022;141:109097.

    Google Scholar 

  90. Morris BE, Henneberger R, Huber H, Moissl-Eichinger C. Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev. 2013;37:384–406.

    CAS  PubMed  Google Scholar 

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Funding

This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA28020201, XDA28070302), Key Research Program of Frontier Sciences, Chinese Academy of Sciences (ZDBS-LY-DQC017), National Key Research and Development Program of China (2022YFD1500200), National Science and Technology Basic Resources Investigation Special Project (2021FY100400), National Natural Science Foundation of China (42177105), CAS International partnership project (131323KYSB20210004), Natural Science Foundation of Heilongjiang Province (ZD2022D001), and Youth Innovation Promotion Association of Chinese Academy of Sciences (2023237).

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  1. These authors contributed equally: Junjie Liu, Yaping Guo.

Authors and Affiliations

  1. State Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin, 150081, P R China

    Junjie Liu, Haidong Gu, Zhuxiu Liu, Xiaojing Hu, Zhenhua Yu, Yansheng Li, Lujun Li, Yueyu Sui, Jian Jin, Xiaobing Liu & Guanghua Wang

  2. School of Geography and Ocean Science, Nanjing University, Nanjing, 210023, P R China

    Yaping Guo & Jonathan M. Adams

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Contributions

JJL, JMA and GHW conceptualized and managed the study. JJL, LJL, ZHY, YSL and ZXL generated the data. HDG, ZXL, YPG and XJH analyzed and interpreted the data. JJL, JMA, YPG, and GHW drafted the manuscript. ZXL, JMA, JJ, YYS and XBL reviewed and edited the corrected manuscript.

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Correspondence to Jonathan M. Adams or Guanghua Wang.

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Liu, J., Guo, Y., Gu, H. et al. Conversion of steppe to cropland increases spatial heterogeneity of soil functional genes. ISME J 17, 1872–1883 (2023). https://doi.org/10.1038/s41396-023-01496-9

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