Biotic homogenization, lower soil fungal diversity and fewer rare taxa in arable soils across Europe.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
06 Jan 2024
06 Jan 2024
Historique:
received:
01
03
2023
accepted:
29
11
2023
medline:
7
1
2024
pubmed:
7
1
2024
entrez:
6
1
2024
Statut:
epublish
Résumé
Soil fungi are a key constituent of global biodiversity and play a pivotal role in agroecosystems. How arable farming affects soil fungal biogeography and whether it has a disproportional impact on rare taxa is poorly understood. Here, we used the high-resolution PacBio Sequel targeting the entire ITS region to investigate the distribution of soil fungi in 217 sites across a 3000 km gradient in Europe. We found a consistently lower diversity of fungi in arable lands than grasslands, with geographic locations significantly impacting fungal community structures. Prevalent fungal groups became even more abundant, whereas rare groups became fewer or absent in arable lands, suggesting a biotic homogenization due to arable farming. The rare fungal groups were narrowly distributed and more common in grasslands. Our findings suggest that rare soil fungi are disproportionally affected by arable farming, and sustainable farming practices should protect rare taxa and the ecosystem services they support.
Identifiants
pubmed: 38184663
doi: 10.1038/s41467-023-44073-6
pii: 10.1038/s41467-023-44073-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
327Informations de copyright
© 2024. The Author(s).
Références
Peay, K. G., Kennedy, P. G. & Talbot, J. M. Dimensions of biodiversity in the Earth mycobiome. Nat. Rev. Microbiol. 14, 434–447 (2016).
pubmed: 27296482
doi: 10.1038/nrmicro.2016.59
van der Heijden, M. G. A., Bardgett, R. D. & Van Straalen, N. M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310 (2008).
pubmed: 18047587
doi: 10.1111/j.1461-0248.2007.01139.x
Crowther, T. W. et al. The global soil community and its influence on biogeochemistry. Science 365, eaav0550 (2019).
pubmed: 31439761
doi: 10.1126/science.aav0550
Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 34, 1256688 (2014).
doi: 10.1126/science.1256688
Gossner, M. M. et al. Land-use intensification causes multitrophic homogenization of grassland communities. Nature 540, 266–269 (2016).
pubmed: 27919075
doi: 10.1038/nature20575
Tsiafouli, M. A. et al. Intensive agriculture reduces soil biodiversity across Europe. Glob. Chang. Biol. 21, 973–985 (2015).
pubmed: 25242445
doi: 10.1111/gcb.12752
Helgason, T., Daniell, T. J., Husband, R., Fitter, A. H. & Young, J. P. Ploughing up the wood-wide web? Nature 394, 431 (1998).
pubmed: 9697763
doi: 10.1038/28764
Tedersoo, L. et al. Global patterns in endemicity and vulnerability of soil fungi. Glob. Chang. Biol. 28, 6696–6710 (2022).
pubmed: 36056462
pmcid: 9826061
doi: 10.1111/gcb.16398
Tuomisto, H. L., Hodge, I. D., Riordan, P. & Macdonald, D. W. Does organic farming reduce environmental impacts? - A meta-analysis of European research. J. Environ. Manag. 112, 309–320 (2012).
doi: 10.1016/j.jenvman.2012.08.018
Gabriel, D., Sait, S. M., Kunin, W. E. & Benton, T. G. Food production vs. biodiversity: comparing organic and conventional agriculture. J. Appl. Ecol. 50, 355–364 (2013).
doi: 10.1111/1365-2664.12035
Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018).
pubmed: 30069051
doi: 10.1038/s41586-018-0386-6
Talbot, J. M. et al. Endemism and functional convergence across the North American soil mycobiome. Proc. Natl. Acad. Sci. 111, 6341–6346 (2014).
pubmed: 24733885
pmcid: 4035912
doi: 10.1073/pnas.1402584111
Averill, C., Cates, L. A. L., Dietze, M. C. & Bhatnagar, J. M. Spatial vs. temporal controls over soil fungal community similarity at continental and global scales. ISME J. 13, 2082–2093 (2019).
pubmed: 31019271
pmcid: 6776031
doi: 10.1038/s41396-019-0420-1
Labouyrie, M. et al. Patterns in soil microbial diversity across Europe. Nat. Commun. 14, 3311 (2023).
Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C. & Martiny, J. B. H. Beyond biogeographic patterns: Processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506 (2012).
pubmed: 22580365
doi: 10.1038/nrmicro2795
Fierer, N. & Jackson, R. B. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. USA 103, 626–631 (2006).
pubmed: 16407148
pmcid: 1334650
doi: 10.1073/pnas.0507535103
Yang, T., Lupwayi, N., Marc, S. A., Siddique, K. H. M. & Bainard, L. D. Anthropogenic drivers of soil microbial communities and impacts on soil biological functions in agroecosystems. Glob. Ecol. Conserv. 27, e01521 (2021).
Chen, Y., Kuang, J., Wang, P., Shu, W. & Barberán, A. Associations between human impacts and forest soil microbial communities. Elementa 8, 1 (2020).
Martiny, J. B. H. et al. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102–112 (2006).
pubmed: 16415926
doi: 10.1038/nrmicro1341
Jiao, S. & Lu, Y. Abundant fungi adapt to broader environmental gradients than rare fungi in agricultural fields. Glob. Chang. Biol. 26, 4506–4520 (2020).
pubmed: 32324306
doi: 10.1111/gcb.15130
Enquist, B. J. et al. The commonness of rarity: Global and future distribution of rarity across land plants. Sci. Adv. 5, 1–14 (2019).
doi: 10.1126/sciadv.aaz0414
Jousset, A. et al. Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J. 11, 853–862 (2017).
pubmed: 28072420
pmcid: 5364357
doi: 10.1038/ismej.2016.174
Chen, Q. L. et al. Rare microbial taxa as the major drivers of ecosystem multifunctionality in long-term fertilized soils. Soil Biol. Biochem. 141, 107686 (2020).
doi: 10.1016/j.soilbio.2019.107686
Xiong, C. et al. Rare taxa maintain the stability of crop mycobiomes and ecosystem functions. Environ. Microbiol. 23, 1907–1924 (2021).
pubmed: 32996254
doi: 10.1111/1462-2920.15262
Delgado-Baquerizo, M. et al. Global homogenization of the structure and function in the soil microbiome of urban greenspaces. Sci. Adv. 7, eabg5809 (2021).
Jia, X., Dini-Andreote, F. & Salles, J. F. Unravelling the interplay of ecological processes structuring the bacterial rare biosphere. ISME Commun. 2, 1–11 (2022).
doi: 10.1038/s43705-022-00177-6
Banerjee, S. et al. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J. 13, 1722–1736 (2019).
pubmed: 30850707
pmcid: 6591126
doi: 10.1038/s41396-019-0383-2
Garland, G. et al. Crop cover is more important than rotational diversity for soil multifunctionality and cereal yields in European cropping systems. Nat. Food 2, 28–37 (2021).
pubmed: 37117662
doi: 10.1038/s43016-020-00210-8
Gámez-Virués, S. et al. Landscape simplification filters species traits and drives biotic homogenization. Nat. Commun. 6, 8568 (2015).
Robinson, R. & Sutherland, W. J. Post-war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 39, 157–176 (2002).
doi: 10.1046/j.1365-2664.2002.00695.x
Riedo, J. et al. Widespread occurrence of pesticides in organically managed agricultural soils-The ghost of a conventional agricultural past? Environ. Sci. Technol. 55, 2919–2928 (2021).
pubmed: 33534554
doi: 10.1021/acs.est.0c06405
Edlinger, A. et al. Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts. Nat. Ecol. Evol. 6, 1145–1154 (2022).
pubmed: 35798840
pmcid: 7613230
doi: 10.1038/s41559-022-01799-8
Romdhane, S. et al. Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity. Environ. Microbiomes 17, 1–15 (2022).
doi: 10.1186/s40793-021-00396-9
de Vries, F. T., Hoffland, E., van Eekeren, N., Brussaard, L. & Bloem, J. Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol. Biochem. 38, 2092–2103 (2006).
doi: 10.1016/j.soilbio.2006.01.008
Henle, K. et al. Identifying and managing the conflicts between agriculture and biodiversity conservation in Europe–A review. Agric. Ecosyst. Environ. 124, 60–71 (2008).
doi: 10.1016/j.agee.2007.09.005
d’Andrimont, R. et al. Harmonised LUCAS in-situ land cover and use database for field surveys from 2006 to 2018 in the European Union. Sci. Data 7, 1–15 (2020).
doi: 10.1038/s41597-020-00675-z
Delgado-Baquerizo, M. et al. A global atlas of the dominant bacteria found in soil. Science 359, 320–325 (2018).
pubmed: 29348236
doi: 10.1126/science.aap9516
Egidi, E. et al. A few Ascomycota taxa dominate soil fungal communities worldwide. Nat. Commun. 101, 1–9 (2019).
Meyer, K. M. et al. Why do microbes exhibit weak biogeographic patterns? ISME J. 12, 1404–1413 (2018).
pubmed: 29662146
pmcid: 5956095
doi: 10.1038/s41396-018-0103-3
Davies, K. F., Margules, C. R. & Lawrence, J. F. A synergistic effect puts rare, specialized species at greater risk of extinction. Ecology 85, 265–271 (2004).
doi: 10.1890/03-0110
Hedlund, B. P. & Staley, J. T. Microbial Endemism and Biogeography. in Microbial Diversity and Bioprospecting 225–231 (ASM Press, 2004). https://doi.org/10.1128/9781555817770.ch22
Bünemann, E. K. et al. Soil quality – A critical review. Soil Biol. Biochem. 120, 105–125 (2018).
doi: 10.1016/j.soilbio.2018.01.030
Cox, F., Newsham, K. K. & Robinson, C. H. Endemic and cosmopolitan fungal taxa exhibit differential abundances in total and active communities of Antarctic soils. Environ. Microbiol. 21, 1586–1596 (2019).
pubmed: 30652397
pmcid: 6850668
doi: 10.1111/1462-2920.14533
Carini, P. et al. Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat. Microbiol. 2, 1–6 (2016).
doi: 10.1038/nmicrobiol.2016.242
Johnson, C. N. et al. Biodiversity losses and conservation responses in the Anthropocene. Science 356, 270–275 (2017).
pubmed: 28428393
doi: 10.1126/science.aam9317
Guerra, C. A. et al. Global hotspots for soil nature conservation. Nature 610, 693–698 (2022).
pubmed: 36224389
doi: 10.1038/s41586-022-05292-x
Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fonseca, G. A. B. & Kent, J. Biodiversity hotspots for conservation priorities. 403, 853–858 (2000).
Brook, B. W., Sodhi, N. S. & Bradshaw, C. J. A. Synergies among extinction drivers under global change. Trends Ecol. Evol. 23, 453–460 (2008).
pubmed: 18582986
doi: 10.1016/j.tree.2008.03.011
Banerjee, S. & Heijden, M. G. A. Soil microbiomes and one health. Nat. Rev. Microbiol. 19, (2022).
Anthony, M. A., Bender, S. F. & van der Heijden, M. G. Enumerating soil biodiversity Mark. Proc. Natl. Acad. Sci. 120, e2304663120 (2023).
pubmed: 37549278
doi: 10.1073/pnas.2304663120
Edlinger, A. et al. The impact of agricultural management on soil aggregation and carbon storage is regulated by climatic thresholds across a 3000 km European gradient. Glob. Chang. Biol. 29, 3177–3192 (2023).
pubmed: 36897740
doi: 10.1111/gcb.16677
Agroscope. Schweizerische Referenzmethoden der Forschungsanstalten Agroscope. Agroscope, Zürich. (1996).
Ashworth, J., Keyes, D., Kirk, R. & Lessard, R. Standard procedure in the hydrometer method for particle size analysis. Commun. Soil Sci. Plant Anal. 32, 633–642 (2001).
doi: 10.1081/CSS-100103897
Vance, E. D., Brookes, P. C. & Jenkinson, D. S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707 (1987).
doi: 10.1016/0038-0717(87)90052-6
Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and ruts. Mol. Ecol. 2, 113–118 (1993).
pubmed: 8180733
doi: 10.1111/j.1365-294X.1993.tb00005.x
Lindahl, B. D. et al. Fungal community analysis by high-throughput sequencing of amplified markers–a user’s guide. N. Phytol. 199, 288–299 (2013).
doi: 10.1111/nph.12243
Schlaeppi, K. et al. High-resolution community profiling of arbuscular mycorrhizal fungi. N. Phytol. 212, 780–791 (2016).
doi: 10.1111/nph.14070
Schmieder, R. & Edwards, R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27, 863–864 (2011).
pubmed: 21278185
pmcid: 3051327
doi: 10.1093/bioinformatics/btr026
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
pubmed: 20709691
doi: 10.1093/bioinformatics/btq461
Kõljalg, U. et al. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. N. Phytol. 166, 1063–1068 (2005).
doi: 10.1111/j.1469-8137.2005.01376.x
Bengtsson-Palme, J. et al. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. 4, 914–919 (2013).
doi: 10.1111/2041-210X.12073
Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
doi: 10.1002/joc.5086
McMurdie, P. J. & Holmes, S. Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS One 8, e61217 (2013).
Nguyen, N. H. et al. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. (2016). https://doi.org/10.1016/j.funeco.2015.06.006
Mazerolle, M. Model selection and multimodel inference using the AICcmodavg package. https://mirror.marwan.ma/cran/web/packages/AICcmodavg/vignettes/AICcmodavg.pdf (2020).
Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).
Rosseel, Y. lavaan: an R package for structural equation modeling and more. J. Stat. Comput. https://doi.org/10.18637/jss.v048.i02 (2012).
Tredennick, A. T., Hooker, G., Ellner, S. P. & Adler, P. B. A practical guide to selecting models for exploration, inference, and prediction in ecology. Ecology 102, e03336 (2021).
Finn, D. R. et al. MicroNiche: an R package for assessing microbial niche breadth and overlap from amplicon sequencing data. FEMS Microbiol. Ecol. 96, 131 (2020).
doi: 10.1093/femsec/fiaa131
Põlme, S. et al. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Divers. 105, 1–16 (2020).
Krivonos, D. V., Konanov, D. N. & Ilina, E. N. FunFun: ITS-based functional annotator of fungal communities. Ecol. Evol. 13, 1–7 (2023).
doi: 10.1002/ece3.9874