Unearthing the soil-borne microbiome of land plants

Raúl Ochoa-Hueso^{1

2}, David J Eldridge³, Miguel Berdugo^{4

5}, Pankaj Trivedi⁶, Blessing Sokoya⁷, Concha Cano-Díaz⁸, Sebastian Abades⁹, Fernando Alfaro¹⁰, Adebola R Bamigboye¹¹, Felipe Bastida¹², José L Blanco-Pastor¹, Asunción de Los Rios¹³, Jorge Durán¹⁴, Stefan Geisen¹⁵, Tine Grebenc¹⁶, Javier G Illán¹⁷, Yu-Rong Liu¹⁸, Thulani P Makhalanyane¹⁹, Steven Mamet²⁰, Marco A Molina-Montenegro²¹, José L Moreno¹², Tina Unuk Nahberger¹⁶, Gabriel F Peñaloza-Bojacá²², César Plaza²³, Ana Rey¹³, Alexandra Rodríguez²⁴, Christina Siebe²⁵, Brajesh K Singh^{26

27}, Alberto L Teixido⁴, Cristian Torres-Díaz²⁸, Ling Wang²⁹, Jianyong Wang²⁹, Juntao Wang²⁶, Eli Zaady³⁰, Xiaobing Zhou³¹, Xin-Quan Zhou¹⁸, Leho Tedersoo³², Manuel Delgado-Baquerizo³³

Affiliations

¹ Department of Biology, Botany Area, University of Cádiz, Vitivinicultural and Agri-Food Research Institute (IVAGRO), Cádiz, Spain.
² Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.
³ Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of NSW, Sydney, New South Wales, Australia.
⁴ Departmento de Biodiversidad, Ecología y Evolución, Facultad de Ciencias Biológicas, Universidad Complutense de Madrid, Madrid, Spain.
⁵ Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland.
⁶ Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA.
⁷ Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado, USA.
⁸ CISAS - Center for Research and Development in Agrifood Systems and Sustainability, Instituto Politécnico de Viana do Castelo, Rua Escola Industrial e Comercial Nun'Álvares, Viana do Castelo, Portugal.
⁹ Instituto de Ecología y Biodiversidad (IEB), Santiago, Chile.
¹⁰ GEMA Center for Genomics, Ecology & Environment, Faculty of Interdisciplinary Studies, Universidad Mayor, Santiago, Chile.
¹¹ Natural History Museum (Botany Unit), Obafemi Awolowo University, Ile-Ife, Nigeria.
¹² CEBAS-CSIC, Campus Universitario de Espinardo, Murcia, Spain.
¹³ Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Madrid, Spain.
¹⁴ Misión Biológica de Galicia, Consejo Superior de Investigaciones Científicas, Pontevedra, Spain.
¹⁵ Laboratory of Nematology, Wageningen University, Wageningen, The Netherlands.
¹⁶ Slovenian Forestry Institute, Ljubljana, Slovenia.
¹⁷ Department of Entomology, Washington State University, Pullman, Washington, USA.
¹⁸ College of Resources and Environment, Huazhong Agricultural University, Wuhan, China.
¹⁹ Centre for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa.
²⁰ College of Agriculture and Bioresources, Department of Soil Science, University of Saskatchewan, Saskatoon, Canada.
²¹ CEAZA, Universidad Católica del Norte, Coquimbo, Chile.
²² Laboratório de Sistemática Vegetal, Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.
²³ Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, Madrid, Spain.
²⁴ Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Coimbra, Portugal.
²⁵ Instituto de Geología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Mexico City, Mexico.
²⁶ Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.
²⁷ Global Centre for Land-Based Innovation, Western Sydney University, Penrith South, New South Wales, Australia.
²⁸ Grupo de Biodiversidad y Cambio Global (BCG), Departamento de Ciencias Básicas, Universidad del Bío-Bío, Chillán, Chile.
²⁹ Institute of Grassland Science, Northeast Normal University, Key Laboratory of Vegetation Ecology, Ministry of Education, Jilin Songnen Grassland Ecosystem National Observation and Research Station, Changchun, China.
³⁰ Department of Natural Resources, Agricultural Research Organization, Institute of Plant Sciences, Gilat Research Center, Negev, Israel.
³¹ State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Xinjiang, China.
³² Mycology and Microbiology Center, University of Tartu, Tartu, Estonia.
³³ Laboratorio de Biodiversidad y Funcionamiento Ecosistémico, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain.

PMID: 38804108
DOI: 10.1111/gcb.17295

Unearthing the soil-borne microbiome of land plants

Raúl Ochoa-Hueso et al. Glob Chang Biol. 2024 May.

. 2024 May;30(5):e17295.

doi: 10.1111/gcb.17295.

Authors

Affiliations

¹ Department of Biology, Botany Area, University of Cádiz, Vitivinicultural and Agri-Food Research Institute (IVAGRO), Cádiz, Spain.
² Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.
³ Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of NSW, Sydney, New South Wales, Australia.
⁴ Departmento de Biodiversidad, Ecología y Evolución, Facultad de Ciencias Biológicas, Universidad Complutense de Madrid, Madrid, Spain.
⁵ Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland.
⁶ Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA.
⁷ Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado, USA.
⁸ CISAS - Center for Research and Development in Agrifood Systems and Sustainability, Instituto Politécnico de Viana do Castelo, Rua Escola Industrial e Comercial Nun'Álvares, Viana do Castelo, Portugal.
⁹ Instituto de Ecología y Biodiversidad (IEB), Santiago, Chile.
¹⁰ GEMA Center for Genomics, Ecology & Environment, Faculty of Interdisciplinary Studies, Universidad Mayor, Santiago, Chile.
¹¹ Natural History Museum (Botany Unit), Obafemi Awolowo University, Ile-Ife, Nigeria.
¹² CEBAS-CSIC, Campus Universitario de Espinardo, Murcia, Spain.
¹³ Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Madrid, Spain.
¹⁴ Misión Biológica de Galicia, Consejo Superior de Investigaciones Científicas, Pontevedra, Spain.
¹⁵ Laboratory of Nematology, Wageningen University, Wageningen, The Netherlands.
¹⁶ Slovenian Forestry Institute, Ljubljana, Slovenia.
¹⁷ Department of Entomology, Washington State University, Pullman, Washington, USA.
¹⁸ College of Resources and Environment, Huazhong Agricultural University, Wuhan, China.
¹⁹ Centre for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa.
²⁰ College of Agriculture and Bioresources, Department of Soil Science, University of Saskatchewan, Saskatoon, Canada.
²¹ CEAZA, Universidad Católica del Norte, Coquimbo, Chile.
²² Laboratório de Sistemática Vegetal, Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.
²³ Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, Madrid, Spain.
²⁴ Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Coimbra, Portugal.
²⁵ Instituto de Geología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Mexico City, Mexico.
²⁶ Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.
²⁷ Global Centre for Land-Based Innovation, Western Sydney University, Penrith South, New South Wales, Australia.
²⁸ Grupo de Biodiversidad y Cambio Global (BCG), Departamento de Ciencias Básicas, Universidad del Bío-Bío, Chillán, Chile.
²⁹ Institute of Grassland Science, Northeast Normal University, Key Laboratory of Vegetation Ecology, Ministry of Education, Jilin Songnen Grassland Ecosystem National Observation and Research Station, Changchun, China.
³⁰ Department of Natural Resources, Agricultural Research Organization, Institute of Plant Sciences, Gilat Research Center, Negev, Israel.
³¹ State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Xinjiang, China.
³² Mycology and Microbiology Center, University of Tartu, Tartu, Estonia.
³³ Laboratorio de Biodiversidad y Funcionamiento Ecosistémico, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain.

PMID: 38804108
DOI: 10.1111/gcb.17295

Abstract

Plant-soil biodiversity interactions are fundamental for the functioning of terrestrial ecosystems. Yet, the existence of a set of globally distributed topsoil microbial and small invertebrate organisms consistently associated with land plants (i.e., their consistent soil-borne microbiome), together with the environmental preferences and functional capabilities of these organisms, remains unknown. We conducted a standardized field survey under 150 species of land plants, including 58 species of bryophytes and 92 of vascular plants, across 124 locations from all continents. We found that, despite the immense biodiversity of soil organisms, the land plants evaluated only shared a small fraction (less than 1%) of all microbial and invertebrate taxa that were present across contrasting climatic and soil conditions and vegetation types. These consistent taxa were dominated by generalist decomposers and phagotrophs and their presence was positively correlated with the abundance of functional genes linked to mineralization. Finally, we showed that crossing environmental thresholds in aridity (aridity index of 0.65, i.e., the transition from mesic to dry ecosystems), soil pH (5.5; i.e., the transition from acidic to strongly acidic soils), and carbon (less than 2%, the lower limit of fertile soils) can result in drastic disruptions in the associations between land plants and soil organisms, with potential implications for the delivery of soil ecosystem processes under ongoing global environmental change.

Keywords: belowground networks; environmental thresholds; moss microbiome; plant microbiome; plant–soil interactions.

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Unearthing the soil-borne microbiome of land plants

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Unearthing the soil-borne microbiome of land plants

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