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Structure and function of the global topsoil microbiome

Author

Listed:
  • Mohammad Bahram

    (University of Tartu
    Uppsala University
    Swedish University of Agricultural Sciences)

  • Falk Hildebrand

    (European Molecular Biology Laboratory)

  • Sofia K. Forslund

    (European Molecular Biology Laboratory
    a cooperation of Charité-Universitätsmedizin and the Max-Delbrück Center
    Max Delbrück Centre for Molecular Medicine)

  • Jennifer L. Anderson

    (Uppsala University)

  • Nadejda A. Soudzilovskaia

    (CML, Leiden University)

  • Peter M. Bodegom

    (CML, Leiden University)

  • Johan Bengtsson-Palme

    (The Sahlgrenska Academy, University of Göteborg
    Centre for Antibiotic Resistance research (CARe), University of Göteborg
    University of Wisconsin-Madison)

  • Sten Anslan

    (University of Tartu
    Braunschweig University of Technology, Zoological Institute)

  • Luis Pedro Coelho

    (European Molecular Biology Laboratory)

  • Helery Harend

    (University of Tartu)

  • Jaime Huerta-Cepas

    (European Molecular Biology Laboratory
    Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA))

  • Marnix H. Medema

    (Bioinformatics Group, Wageningen University)

  • Mia R. Maltz

    (University of California, Riverside)

  • Sunil Mundra

    (University of Oslo)

  • Pål Axel Olsson

    (Ecology building, Lund University)

  • Mari Pent

    (University of Tartu)

  • Sergei Põlme

    (University of Tartu)

  • Shinichi Sunagawa

    (European Molecular Biology Laboratory
    Institute of Microbiology, ETH Zurich)

  • Martin Ryberg

    (Uppsala University)

  • Leho Tedersoo

    (Natural History Museum, University of Tartu)

  • Peer Bork

    (European Molecular Biology Laboratory
    Max Delbrück Centre for Molecular Medicine
    University of Würzburg)

Abstract

Soils harbour some of the most diverse microbiomes on Earth and are essential for both nutrient cycling and carbon storage. To understand soil functioning, it is necessary to model the global distribution patterns and functional gene repertoires of soil microorganisms, as well as the biotic and environmental associations between the diversity and structure of both bacterial and fungal soil communities1–4. Here we show, by leveraging metagenomics and metabarcoding of global topsoil samples (189 sites, 7,560 subsamples), that bacterial, but not fungal, genetic diversity is highest in temperate habitats and that microbial gene composition varies more strongly with environmental variables than with geographic distance. We demonstrate that fungi and bacteria show global niche differentiation that is associated with contrasting diversity responses to precipitation and soil pH. Furthermore, we provide evidence for strong bacterial–fungal antagonism, inferred from antibiotic-resistance genes, in topsoil and ocean habitats, indicating the substantial role of biotic interactions in shaping microbial communities. Our results suggest that both competition and environmental filtering affect the abundance, composition and encoded gene functions of bacterial and fungal communities, indicating that the relative contributions of these microorganisms to global nutrient cycling varies spatially.

Suggested Citation

  • Mohammad Bahram & Falk Hildebrand & Sofia K. Forslund & Jennifer L. Anderson & Nadejda A. Soudzilovskaia & Peter M. Bodegom & Johan Bengtsson-Palme & Sten Anslan & Luis Pedro Coelho & Helery Harend & , 2018. "Structure and function of the global topsoil microbiome," Nature, Nature, vol. 560(7717), pages 233-237, August.
  • Handle: RePEc:nat:nature:v:560:y:2018:i:7717:d:10.1038_s41586-018-0386-6
    DOI: 10.1038/s41586-018-0386-6
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    Citations

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    Cited by:

    1. Jincai Ma & Sumiya Nergui & Ziming Han & Guannan Huang & Huiru Li & Rui Zhang & Liyue Zhu & Jiafen Liao, 2019. "The Variation of the Soil Bacterial and Fungal Community Is Linked to Land Use Types in Northeast China," Sustainability, MDPI, vol. 11(12), pages 1-15, June.
    2. Patrick Munk & Christian Brinch & Frederik Duus Møller & Thomas N. Petersen & Rene S. Hendriksen & Anne Mette Seyfarth & Jette S. Kjeldgaard & Christina Aaby Svendsen & Bram Bunnik & Fanny Berglund & , 2022. "Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Abdullah Kaviani Rad & Angelika Astaykina & Rostislav Streletskii & Yeganeh Afsharyzad & Hassan Etesami & Mehdi Zarei & Siva K. Balasundram, 2022. "An Overview of Antibiotic Resistance and Abiotic Stresses Affecting Antimicrobial Resistance in Agricultural Soils," IJERPH, MDPI, vol. 19(8), pages 1-27, April.
    4. Cong Wang & Qing-Yi Yu & Niu-Niu Ji & Yong Zheng & John W. Taylor & Liang-Dong Guo & Cheng Gao, 2023. "Bacterial genome size and gene functional diversity negatively correlate with taxonomic diversity along a pH gradient," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    5. Tarquin Netherway & Jan Bengtsson & Franz Buegger & Joachim Fritscher & Jane Oja & Karin Pritsch & Falk Hildebrand & Eveline J. Krab & Mohammad Bahram, 2024. "Pervasive associations between dark septate endophytic fungi with tree root and soil microbiomes across Europe," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Yukun Zheng & Hongyan Liu & Huan Yang & Hongya Wang & Wenjie Zhao & Zeyu Zhang & Miao Huang & Weihang Liu, 2022. "Decoupled Asian monsoon intensity and precipitation during glacial-interglacial transitions on the Chinese Loess Plateau," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    7. Mengxia Zhou & Hui Yang & Tongbin Zhu & Cheng Zhang & Degen Zhu, 2022. "Preliminary Research on Agricultural Cultivation Decreasing Amino Sugar Accumulation in Calcareous Soils in Subtropical Karst Region of China," Land, MDPI, vol. 11(10), pages 1-12, September.
    8. Zhenyan Zhang & Qi Zhang & Tingzhang Wang & Nuohan Xu & Tao Lu & Wenjie Hong & Josep Penuelas & Michael Gillings & Meixia Wang & Wenwen Gao & Haifeng Qian, 2022. "Assessment of global health risk of antibiotic resistance genes," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    9. Samiran Banerjee & Cheng Zhao & Gina Garland & Anna Edlinger & Pablo García-Palacios & Sana Romdhane & Florine Degrune & David S. Pescador & Chantal Herzog & Lennel A. Camuy-Velez & Jordi Bascompte & , 2024. "Biotic homogenization, lower soil fungal diversity and fewer rare taxa in arable soils across Europe," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    10. Jun Li & Yan Chen & Xiangyang Qin & Aocheng Cao & Anxiang Lu, 2022. "Impact of Biochar on Rhizosphere Bacterial Diversity Restoration Following Chloropicrin Fumigation of Planted Soil," IJERPH, MDPI, vol. 19(4), pages 1-14, February.
    11. Anton M. Potapov & Carlos A. Guerra & Johan Hoogen & Anatoly Babenko & Bruno C. Bellini & Matty P. Berg & Steven L. Chown & Louis Deharveng & Ľubomír Kováč & Natalia A. Kuznetsova & Jean-François Pong, 2023. "Globally invariant metabolism but density-diversity mismatch in springtails," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    12. Zhu, Jinjin & Niu, Wenquan & Zhang, Zhenhua & Siddique, Kadambot H.M. & Dan Sun, & Yang, Runya, 2022. "Distinct roles for soil bacterial and fungal communities associated with the availability of carbon and phosphorus under aerated drip irrigation," Agricultural Water Management, Elsevier, vol. 274(C).
    13. Howard W. Mielke & Christopher R. Gonzales & Eric T. Powell, 2019. "Curtailing Lead Aerosols: Effects of Primary Prevention on Declining Soil Lead and Children’s Blood Lead in Metropolitan New Orleans," IJERPH, MDPI, vol. 16(12), pages 1-10, June.
    14. Mohammad Bahram & Mikk Espenberg & Jaan Pärn & Laura Lehtovirta-Morley & Sten Anslan & Kuno Kasak & Urmas Kõljalg & Jaan Liira & Martin Maddison & Mari Moora & Ülo Niinemets & Maarja Öpik & Meelis Pär, 2022. "Structure and function of the soil microbiome underlying N2O emissions from global wetlands," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    15. Mahmoud F. Seleiman & Nasser Al-Suhaibani & Salah El-Hendawy & Kamel Abdella & Majed Alotaibi & Ali Alderfasi, 2021. "Impacts of Long- and Short-Term of Irrigation with Treated Wastewater and Synthetic Fertilizers on the Growth, Biomass, Heavy Metal Content, and Energy Traits of Three Potential Bioenergy Crops in Ari," Energies, MDPI, vol. 14(11), pages 1-22, May.
    16. Maëva Labouyrie & Cristiano Ballabio & Ferran Romero & Panos Panagos & Arwyn Jones & Marc W. Schmid & Vladimir Mikryukov & Olesya Dulya & Leho Tedersoo & Mohammad Bahram & Emanuele Lugato & Marcel G. , 2023. "Patterns in soil microbial diversity across Europe," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    17. Hu Liao & Hu Li & Chen-Song Duan & Xin-Yuan Zhou & Qiu-Ping Luo & Xin-Li An & Yong-Guan Zhu & Jian-Qiang Su, 2022. "Response of soil viral communities to land use changes," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    18. Jie-Liang Liang & Shi-wei Feng & Jing-li Lu & Xiao-nan Wang & Feng-lin Li & Yu-qian Guo & Shen-yan Liu & Yuan-yue Zhuang & Sheng-ji Zhong & Jin Zheng & Ping Wen & Xinzhu Yi & Pu Jia & Bin Liao & Wen-s, 2024. "Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Dong Zhao & Huping Hou & Haiya Liu & Chen Wang & Zhongyi Ding & Jinting Xiong, 2023. "Microbial Community Structure and Predictive Functional Analysis in Reclaimed Soil with Different Vegetation Types: The Example of the Xiaoyi Mine Waste Dump in Shanxi," Land, MDPI, vol. 12(2), pages 1-14, February.
    20. de la Riva, Enrique G. & Ulrich, Werner & Batáry, Péter & Baudry, Julia & Beaumelle, Léa & Bucher, Roman & Čerevková, Andrea & Felipe-Lucia, María R. & Gallé, Róbert & Kesse-Guyot, Emmanuelle & Rembia, 2023. "From functional diversity to human well-being: A conceptual framework for agroecosystem sustainability," Agricultural Systems, Elsevier, vol. 208(C).
    21. Asada, K. & Kanda, T. & Yamashita, N. & Asano, M. & Eguchi, S., 2022. "Interpreting stoichiometric homeostasis and flexibility of soil microbial biomass carbon, nitrogen, and phosphorus," Ecological Modelling, Elsevier, vol. 470(C).
    22. Wen Zhao & Yali Yin & Shixiong Li & Jingjing Liu & Yiling Dong & Shifeng Su, 2022. "Soil Microbial Community Varied with Vegetation Types on a Small Regional Scale of the Qilian Mountains," Sustainability, MDPI, vol. 14(13), pages 1-15, June.
    23. Pengfa Li & Leho Tedersoo & Thomas W. Crowther & Baozhan Wang & Yu Shi & Lu Kuang & Ting Li & Meng Wu & Ming Liu & Lu Luan & Jia Liu & Dongzhen Li & Yongxia Li & Songhan Wang & Muhammad Saleem & Alex , 2023. "Global diversity and biogeography of potential phytopathogenic fungi in a changing world," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    24. Taimoor Hassan Farooq & Uttam Kumar & Awais Shakoor & Gadah Albasher & Saad Alkahtani & Humaira Rizwana & Muhammad Tayyab & Jalpa Dobaria & Muhammad Iftikhar Hussain & Pengfei Wu, 2021. "Influence of Intraspecific Competition Stress on Soil Fungal Diversity and Composition in Relation to Tree Growth and Soil Fertility in Sub-Tropical Soils under Chinese Fir Monoculture," Sustainability, MDPI, vol. 13(19), pages 1-18, September.

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