Litter and soil biodiversity jointly drive ecosystem functions.

ecosystem multifunctionality fungal saprobes litter decomposition plant diversity plant production soil biodiversity

Journal

Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746

Informations de publication

Date de publication:
Nov 2023
Historique:
revised: 31 07 2023
received: 26 03 2023
accepted: 01 08 2023
pubmed: 14 8 2023
medline: 14 8 2023
entrez: 14 8 2023
Statut: ppublish

Résumé

The decomposition of litter and the supply of nutrients into and from the soil are two fundamental processes through which the above- and belowground world interact. Microbial biodiversity, and especially that of decomposers, plays a key role in these processes by helping litter decomposition. Yet the relative contribution of litter diversity and soil biodiversity in supporting multiple ecosystem services remains virtually unknown. Here we conducted a mesocosm experiment where leaf litter and soil biodiversity were manipulated to investigate their influence on plant productivity, litter decomposition, soil respiration, and enzymatic activity in the littersphere. We showed that both leaf litter diversity and soil microbial diversity (richness and community composition) independently contributed to explain multiple ecosystem functions. Fungal saprobes community composition was especially important for supporting ecosystem multifunctionality (EMF), plant production, litter decomposition, and activity of soil phosphatase when compared with bacteria or other fungal functional groups and litter species richness. Moreover, leaf litter diversity and soil microbial diversity exerted previously undescribed and significantly interactive effects on EMF and multiple individual ecosystem functions, such as litter decomposition and plant production. Together, our work provides experimental evidence supporting the independent and interactive roles of litter and belowground soil biodiversity to maintain ecosystem functions and multiple services.

Identifiants

pubmed: 37578170
doi: 10.1111/gcb.16913
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

6276-6285

Subventions

Organisme : National Natural Science Foundation of China
ID : 32101491
Organisme : Spanish Ministry of Science and Innovation
ID : PID2020-115813RA-I00
Organisme : Spanish Ministry of Science and Innovation
ID : TED2021-130908B-C41
Organisme : China Postdoctoral Science Foundation
ID : 2021M701968
Organisme : China Postdoctoral Science Foundation
ID : 2022T150375
Organisme : Yunnan Science and Technology Talent and Platform Program
ID : 202105AG070002
Organisme : Humbodlt Research Foundation
Organisme : MICINN
ID : RYC-2017 22032
Organisme : MICINN
ID : RYC-2021-033454
Organisme : R&D Project of the Ministry of Science and Innovation
ID : PID2019-106004RA-I00
Organisme : European Agricultural Fund for Rural Development (EAFRD)
Organisme : Australian Research Council
ID : DP210102081

Informations de copyright

© 2023 The Authors. Global Change Biology published by John Wiley & Sons Ltd.

Références

Allison, S. D., & Martiny, J. B. (2008). Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences of the United States of America, 105, 11512-11519.
Averill, C., Turner, B. L., & Finzi, A. C. (2014). Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature, 505, 543-545.
Baldrian, P., López-Mondéjar, R., & Kohout, P. (2023). Forest microbiome and global change. Nature Reviews. Microbiology, 21, 487-501.
Barantal, S., Schimann, H., Fromin, N., & Hättenschwiler, S. (2014). C, N and P fertilization in an Amazonian rainforest supports stoichiometric dissimilarity as a driver of litter diversity effects on decomposition. Proceedings of the Royal Society B: Biological Sciences, 281, 20141682.
Bardgett, R. D., & van der Putten, W. H. (2014). Belowground biodiversity and ecosystem functioning. Nature, 515, 505-511.
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2014). lme4: Linear mixed-effects models using Eigen and S4. Journal of Statistical Software, 67, 1-48.
Bell, C. W., Fricks, B. E., Rocca, J. D., Steinweg, J. M., McMahon, S. K., & Wallenstein, M. D. (2013). High-throughput fluorometric measurement of potential soil extracellular enzyme activities. Journal of Visualized Experiments, 81, e50961.
Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C. C., Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., Asnicar, F., & Bai, Y. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37, 1091.
Bradford, M. A. (2014). Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition. Proceedings of the National Academy of Sciences of the United States of America, 111, 14478-14483.
Bradford, M. A., Berg, B., Maynard, D. S., Wieder, W. R., & Wood, S. A. (2016). Understanding the dominant controls on litter decomposition. Journal of Ecology, 104, 229-238.
Breiman, L. (2001). Random forests. Machine Learning, 45, 5-32.
Byrnes, J. E., Gamfeldt, L., Isbell, F., Lefcheck, J. S., Griffin, J. N., Hector, A., Cardinale, B. J., Hooper, D. U., Dee, L. E., & Emmett Duffy, J. (2014). Investigating the relationship between biodiversity and ecosystem multifunctionality: Challenges and solutions. Methods in Ecology and Evolution, 5, 111-124.
Campbell, C., Chapman, S., Cameron, C., Davidson, M., & Potts, J. A. (2003). Rapid microtiter plate method to measure carbon dioxideevolved from carbon substrate amendments so as to determinethe physiological profiles of soil microbial communities by usingwhole soil. Applied and Environmental Microbiology, 69, 3593-3599.
Cornwell, W. K., Cornelissen, J., Amatangelo, K., Dorrepaal, E., Eviner, V. T., Godoy, O., Hobbie, S. E., Hoorens, B., Kurokawa, H., Pérez-Harguindeguy, N., & Quested, H. M. (2010). Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology Letters, 11, 1065-1071.
Cotrufo, M., Soong, J., Horton, A., Campbell, E. E., Haddix, M. L., Wall, D. H., & Parton, W. J. (2015). Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nature Geoscience, 8, 776-779.
Craven, D., Isbell, F., Manning, P., Connolly, J., Bruelheide, H., Ebeling, A., Roscher, C., van Ruijven, J., Weigelt, A., Wilsey, B., Beierkuhnlein, C., de Luca, E., Griffin, J. N., Hautier, Y., Hector, A., Jentsch, A., Kreyling, J., Lanta, V., Loreau, M., … Eisenhauer, N. (2016). Plant diversity effects on grassland productivity are robust to both nutrient enrichment and drought. Philosophical Transactions of the Royal Society B: Biological Sciences, 371, 20150277.
de Vries, F. T., Thebault, E., Liiri, M., Birkhofer, K., Tsiafouli, M. A., Bjornlund, L., Jørgensen, H. B., Brady, M. V., Christensen, S., De Ruiter, P. C., & d'Hertefeldt, T. (2013). Soil food web properties explain ecosystem services across European land use systems. Proceedings of the National Academy of Sciences of the United States of America, 110, 14296-14301.
Delgado-Baquerizo, M., Giaramida, L., Reich, P. B., Khachane, A. N., Hamonts, K., Edwards, C., Lawton, L. A., & Singh, B. K. (2016). Lack of functional redundancy in the relationship between microbial diversity and ecosystem functioning. Journal of Ecology, 104, 936-946.
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. Science, 359(6373), 320-325. https://doi.org/10.1126/science.aap9516
Delgado-Baquerizo, M., Reich, P. B., Khachane, A. N., Campbell, C. D., Thomas, N., Freitag, T. E., Abu al-Soud, W., Sørensen, S., Bardgett, R. D., & Singh, B. K. (2017). It is elemental: Soil nutrient stoichiometry drives bacterial diversity. Environmental Microbiology, 19, 1176-1188.
Delgado-Baquerizo, M., Reich, P. B., Trivedi, C., Eldridge, D. J., Abades, S., Alfaro, F. D., Bastida, F., Berhe, A. A., Cutler, N. A., Gallardo, A., García-Velázquez, L., Hart, S. C., Hayes, P. E., He, J. Z., Hseu, Z. Y., Hu, H. W., Kirchmair, M., Neuhauser, S., Pérez, C. A., … Singh, B. K. (2020). Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nature Ecology and Evolution, 4, 210-220.
Delgado-Baquerizo, M., Trivedi, P., Trivedi, C., Eldridge, D. J., Reich, P. B., Jeffries, T. C., & Singh, B. K. (2017). Microbial richness and composition independently drive soil multifunctionality. Functional Ecology, 31, 2330-2343.
Edgar, R. C. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996-998.
Edgar, R. C. (2016). UNOISE2: Improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv, 081257.
Eisenhauer, N. (2022). The shape that matters: How important is biodiversity for ecosystem functioning? Science China Life Sciences, 65, 651-653.
Eldridge, D. J., Guirado, E., Reich, P. B., Ochoa-Hueso, R., Berdugo, M., Sáez-Sandino, T., Blanco-Pastor, J. L., Tedersoo, L., Plaza, C., Ding, J., Sun, W., Mamet, S., Cui, H., He, J. Z., Hu, H. W., Sokoya, B., Abades, S., Alfaro, F., Bamigboye, A. R., … Delgado-Baquerizo, M. (2023). The global contribution of soil mosses to ecosystem services. Nature Geoscience, 16, 430-438.
García-Palacios, P., Crowther, T. W., Dacal, M., Hartley, I. P., Reinsch, S., Rinnan, R., Rousk, J., van den Hoogen, J., Ye, J. S., & Bradford, M. A. (2021). Evidence for large microbial-mediated losses of soil carbon under anthropogenic warming. Nature Reviews Earth & Environment, 2, 507-517.
García-Palacios, P., Maestre, F. T., Kattge, J., & Wall, D. H. (2013). Climate and litter quality differently modulate the effects of soil fauna on litter decomposition across biomes. Ecology Letters, 16, 1045-1053.
Gessner, M. O., Swan, C. M., Dang, C. K., McKie, B. G., Bardgett, R. D., Wall, D. H., & Hattenschwiler, S. (2010). Diversity meets decomposition. Trends in Ecology & Evolution, 25, 372-380.
Grömping, U. (2006). Relative importance for linear regression in R: The package relaimpo. Journal of Statistical Software, 17, 1-27.
Guerra, C. A., Berdugo, M., Eldridge, D. J., Eisenhauer, N., Singh, B. K., Cui, H., Abades, S., Alfaro, F. D., Bamigboye, A. R., Bastida, F., Blanco-Pastor, J. L., de los Ríos, A., Durán, J., Grebenc, T., Illán, J. G., Liu, Y. R., Makhalanyane, T. P., Mamet, S., Molina-Montenegro, M. A., … Delgado-Baquerizo, M. (2022). Global hotspots for soil nature conservation. Nature, 610, 693-698.
Handa, I. T., Aerts, R., Berendse, F., Berg, M. P., Bruder, A., Butenschoen, O., Chauvet, E., Gessner, M. O., Jabiol, J., Makkonen, M., McKie, B. G., Malmqvist, B., Peeters, E. T. H. M., Scheu, S., Schmid, B., van Ruijven, J., Vos, V. C. A., & Hättenschwiler, S. (2014). Consequences of biodiversity loss for litter decomposition across biomes. Nature, 509, 218-221.
Hautier, Y., Isbell, F., Borer, E. T., Seabloom, E. W., Harpole, W. S., Lind, E. M., MacDougall, A., Stevens, C. J., Adler, P. B., Alberti, J., Bakker, J. D., Brudvig, L. A., Buckley, Y. M., Cadotte, M., Caldeira, M. C., Chaneton, E. J., Chu, C., Daleo, P., Dickman, C. R., … Hector, A. (2018). Local loss and spatial homogenization of plant diversity reduce ecosystem multifunctionality. Nature Ecology & Evolution, 2, 50-56.
Huys, R., Poirier, V., Bourget, M. Y., Roumet, C., Hättenschwiler, S., Fromin, N., Munson, A. D., & Freschet, G. T. (2022). Plant litter chemistry controls coarse-textured soil carbon dynamics. Journal of Ecology, 110, 2911-2928.
Jiao, S., Lu, Y. H., & Wei, G. H. (2022). Soil multitrophic network complexity enhances the link between biodiversity and multifunctionality in agricultural systems. Global Change Biology, 28, 140-153.
Jing, X., Sanders, N., Shi, Y., Chu, H., Classen, A. T., Zhao, K., Chen, L., Shi, Y., Jiang, Y., & He, J. S. (2015). The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nature Communications, 6, 8159.
Kou, L., Jiang, L., Hättenschwiler, S., Zhang, M. M., Niu, S. L., Fu, X. L., Dai, X. Q., Yan, H., Li, S. G., & Wang, H. M. (2020). Diversity-decomposition relationships in forests worldwide. eLife, 9, e55813.
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82, 1-26.
Lange, M., Eisenhauer, N., Sierra, C., Bessler, H., Engels, C., Griffiths, R. I., Mellado-Vázquez, P. G., Malik, A. A., Roy, J., Scheu, S., & Steinbeiss, S. (2015). Plant diversity increases soil microbial activity and soil carbon storage. Nature Communications, 6, 6707.
Li, Y., Ge, Y., Wang, J. C., Shen, C. C., & Liu, Y. J. (2021). Functional redundancy and specific taxa modulate the contribution of prokaryotic diversity and composition to multifunctionality. Molecular Ecology, 30, 2915-2930.
Liu, S., Pablo, G.-P., Leho, T., Guirado, E., van der Heijden, M. G. A., Wagg, C., Chen, D. M., Wang, Q. K., Wang, J. T., Singh, B. K., & Delgado-Baquerizo, M. (2022). Phylotype diversity within soil fungal functional groups drives ecosystem stability. Nature Ecology & Evolution, 6, 900-909.
Liu, S., Wang, H., Tian, P., Yao, X., Sun, H., Wang, Q., & Delgado-Baquerizo, M. (2020). Decoupled diversity patterns in bacteria and fungi across continental forest ecosystems. Soil Biology and Biochemistry, 144, 107763.
Maestre, F. T., Castillo-Monroy, A. P., Bowker, M. A., & Ochoa-Hueso, R. (2012). Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. Journal of Ecology, 100, 317-330.
Maestre, F. T., Quero, J. L., Gotelli, N. J., Escudero, A., Ochoa, V., Delgado-Baquerizo, M., & Zaady, E. (2012). Plant species richness and ecosystem multifunctionality in global drylands. Science, 335, 214-218.
Meier, C. L., & Bowman, W. D. (2008). Links between plant litter chemistry, species diversity, and below-ground ecosystem function. Proceedings of the National Academy of Sciences of the United States of America, 105, 19780-19785.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H., & Wagner, H. (2013). Vegan: Community ecology package. R Foundation for Statistical Computing.
Otsing, E., Barantal, S., Anslan, S., Koricheva, J., & Tedersoo, L. (2018). Litter species richness and composition effects on fungal richness and community composition in decomposing foliar and root litter. Soil Biology and Biochemistry, 125, 328-339.
Philippot, L., Spor, A., Hénault, C., Bru, D., Bizouard, F., Jones, C. M., Sarr, A., & Maron, P. A. (2013). Loss in microbial diversity affects nitrogen cycling in soil. The ISME Journal, 7, 1609-1619.
Phillips, R. P., Brzostek, E., & Midgley, M. G. (2013). The mycorrhizal-associated nutrient economy: A new framework for predicting carbon-nutrient couplings in temperate forests. The New Phytologist, 199, 41-51.
Põlme, S., Abarenkov, K., Henrik Nilsson, R., Lindahl, B. D., Clemmensen, K. E., Kauserud, H., Nguyen, N., Kjøller, R., Bates, S. T., Baldrian, P., Frøslev, T. G., Adojaan, K., Vizzini, A., Suija, A., Pfister, D., Baral, H. O., Järv, H., Madrid, H., Nordén, J., … Tedersoo, L. (2020). FungalTraits: A user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Diversity, 105, 1-16.
Rivett, D. W., & Bell, T. (2018). Abundance determines the functional role of bacterial phylotypes in complex communities. Nature Microbiology, 3, 767-772.
Semchenko, M., Leff, J. W., Lozano, Y. M., Saar, S., Davison, J., Wilkinson, A., Jackson, B. G., Pritchard, W. J., de Long, J. R., Oakley, S., Mason, K. E., Ostle, N. J., Baggs, E. M., Johnson, D., Fierer, N., & Bardgett, R. D. (2018). Fungal diversity regulates plant-soil feedbacks in temperate grassland. Science Advances, 4, eaau4578.
Swift, M. J., Heal, O. W., & Anderson, J. M. (1979). Decomposition in terrestrial ecosystems. University of California Press.
Tedersoo, L., Bahram, M., & Zobel, M. (2020). How do mycorrhizal associations drive plant population and community biology? Science, 367, eaba1223.
Tilman, D., Wedin, D., & Knops, J. (1996). Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature, 379, 718-720.
Trivedi, P., Delgado-Baquerizo, M., Trivedi, C., Hu, H., Anderson, I. C., Jeffries, T. C., Zhou, J., & Singh, B. K. (2016). Microbial regulation of the soil carbon cycle: Evidence from gene-enzyme relationships. The ISME Journal, 10, 2593-2604.
Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T., & Singh, B. K. (2020). Plant-microbiome interactions: From community assembly to plant health. Nature Reviews. Microbiology, 18, 607-621.
Vos, V. C., van Ruijven, J., Berg, M. P., Peeters, E. T., & Berendse, F. (2013). Leaf litter quality drives litter mixing effects through complementary resource use among detritivores. Oecologia, 173, 269-280.
Wagg, C., Bender, S. F., Widmer, F., & van der Heijden, M. G. A. (2014). Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America, 111, 5266-5270.
Wardle, D. A., Yeates, G. W., Barker, G. M., & Bonner, K. I. (2006). The influence of plant litter diversity on decomposer abundance and diversity. Soil Biology and Biochemistry, 38, 1052-1062.
Xiao, W., Chen, C., Chen, X., Huang, Z., & Chen, H. (2020). Functional and phylogenetic diversity promote litter decomposition across terrestrial ecosystems. Global Ecology and Biogeography, 29, 2261-2272.
Yang, G. W., Wagg, C., Veresoglou, S. D., Hempel, S., & Rillig, M. C. (2018). How soil biota drive ecosystem stability. Trends in Plant Science, 23, 1057-1067.
Yang, G. W., Wagg, C., Veresoglou, S. D., Hempel, S., & Rillig, M. C. (2021). Plant and soil biodiversity have non-substitutable stabilizing effects on biomass production. Ecology Letters, 24, 1582-1593.
Zhou, G. Y., Lucas-Borja, M. E., Eisenhauer, N., Eldridge, D. J., Liu, S. E., & Delgado-Baquerizo, M. (2022). Understorey biodiversity supports the multifunctionality of mature Mediterranean forests. Soil Biology and Biochemistry, 172, 108774.

Auteurs

Shengen Liu (S)

College of Forestry, Fujian Agriculture and Forestry University, Fuzhou, China.
Yunnan Key Laboratory of Plateau Wetland Conservation, Restoration and Ecological Services, Kunming, China.
Laboratorio de Biodiversidad y Funcionamiento Ecosistémico, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain.

César Plaza (C)

Instituto de Ciencias Agrarias (ICA), CSIC, Madrid, Spain.

Raúl Ochoa-Hueso (R)

Department of Biology, IVAGRO, University of Cádiz, Campus de Excelencia Internacional Agroalimentario (CeiA3), Cádiz, Spain.
Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.
Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.

Chanda Trivedi (C)

Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.

Juntao Wang (J)

Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.

Pankaj Trivedi (P)

Microbiome Network and Department of Agricultural Biology, Colorado State University, Fort Collins, Colorado, USA.

Guiyao Zhou (G)

Laboratorio de Biodiversidad y Funcionamiento Ecosistémico, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain.
German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany.

Juan Piñeiro (J)

Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.
ETSI Montes, Forestal y del Medio Natural, Universidad Politécnica de Madrid, Madrid, Spain.

Catarina S C Martins (CSC)

Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.

Brajesh K Singh (BK)

Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.
Global Centre for Land-Based Innovation, Western Sydney University, Penrith, New South Wales, Australia.

Manuel Delgado-Baquerizo (M)

Laboratorio de Biodiversidad y Funcionamiento Ecosistémico, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain.

Classifications MeSH