Articles | Volume 10, issue 1
https://doi.org/10.5194/soil-10-425-2024
© Author(s) 2024. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/soil-10-425-2024
© Author(s) 2024. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Original research article
| 
21 Jun 2024
Original research article |
| 21 Jun 2024
| 21 Jun 2024
Ectomycorrhizal fungal network complexity determines soil multi-enzymatic activity
Jorge Prieto-Rubio
CORRESPONDING AUTHOR
Departamento de Ecología y Cambio Global, Centro de Investigaciones sobre Desertificación (CSIC-UV-GV), Moncada, 46113, Spain
Departamento de Microbiología del Suelo y Planta, Estación Experimental del Zaidín (CSIC), Granada, 18008, Spain
Departamento de Suelo, Planta y Calidad Ambiental, Instituto de Ciencias Agrarias (CSIC), Madrid, 28006, Spain
José L. Garrido
Departamento de Microbiología del Suelo y Planta, Estación Experimental del Zaidín (CSIC), Granada, 18008, Spain
Departamento de Ecología Evolutiva, Estación Biológica de Doñana (CSIC), Seville, 41092, Spain
Julio M. Alcántara
Departamento de Biología Animal, Biología Vegetal y Ecología, Universidad de Jaén, Jaén, 23071, Spain
Instituto Interuniversitario de Investigación del Sistema Tierra en Andalucía, Granada, 18006, Spain
Concepción Azcón-Aguilar
Departamento de Microbiología del Suelo y Planta, Estación Experimental del Zaidín (CSIC), Granada, 18008, Spain
Ana Rincón
Departamento de Suelo, Planta y Calidad Ambiental, Instituto de Ciencias Agrarias (CSIC), Madrid, 28006, Spain
Álvaro López-García
Departamento de Biología Animal, Biología Vegetal y Ecología, Universidad de Jaén, Jaén, 23071, Spain
Instituto Interuniversitario de Investigación del Sistema Tierra en Andalucía, Granada, 18006, Spain
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Cited articles
Abarenkov, K., Nilsson, R. H., Larsson, K. H., Alexander, I. J., Eberhardt, U., Erland, S., Høiland, K., Kjøller, R., Larsson, E., Pennanen, T., Sen, R., Taylor, A. F. S., Tedersoo, L., Ursing, B. M., Vrålstad, T., Liimatainen, K., Peintner, U., and Kõljalg, U.: The UNITE database for molecular identification of fungi-recent updates and future perspectives, New Phytol., 186, 281–285, https://doi.org/10.1111/j.1469-8137.2009.03160.x, 2010.
Alcántara, J. M., Pulgar, M., Trøjelsgaard, K., Garrido, J. L., and Rey, P. J.: Stochastic and deterministic effects on interactions between canopy and recruiting species in forest communities, Funct. Ecol., 32, 2264–2274, https://doi.org/10.1111/1365-2435.13140, 2018.
Azcón-Aguilar, C. and Barea, J. M.: Nutrient cycling in the mycorrhizosphere, J. Soil Sci. Plant Nut., 15, 372–396. https://doi.org/10.4067/s0718-95162015005000035, 2015.
Bahram, M., Netherway, T., Hildebrand, F., Pritsch, K., Drenkhan, R., Loit, K., Anslan, S., Bork, P., and Tedersoo, L.: Plant nutrient-acquisition strategies drive topsoil microbiome structure and function, New Phytol., 227, 1189–1199, https://doi.org/10.1111/nph.16598, 2020.
Banerjee, S., Thrall, P. H., Bissett, A., van der Heijden, M. G. A., and Richardson, A. E.: Linking microbial co-occurrences to soil ecological processes across a woodland-grassland ecotone, Ecol. Evol., 17, 8217–8230, https://doi.org/10.1002/ece3.4346, 2018a.
Banerjee, S., Schlaeppi, K., and van der Heijden, M. G. A.: Keystone taxa as drivers of microbiome structure and functioning, Nat. Rev. Microbiol., 16, 567–576, https://doi.org/10.1038/s41579-018-0024-1, 2018b.
Bates, D., Maechler, M., Bolker, B., and Walker, S.: Fitting Linear Mixed-Effects Models Using lme4, J. Stat. Soft., 67, 1–48, https://doi.org/10.18637/jss.v067.i01, 2015.
Barberán, A., Bates, S. T., Casamayor, E. O., and Fierer, N.: Using network analysis to explore co-occurrence patterns in soil microbial communities, ISME J., 6, 343–351, https://doi.org/10.1038/ismej.2011.119, 2012.
Barner, A. K., Coblentz, K. E., Hacker, S. D., and Menge, B. A.: Fundamental contradictions among observational and experimental estimates of non-trophic species interactions, Ecology, 99, 557–566. https://doi.org/10.1002/ecy.2133, 2018.
Barroso-Bergadà, D., Pauvert, C., Vallance, J., Delière, L., Bohan, D. A., Buée, M., and Vacher, C.: Microbial networks inferred from environmental DNA data for biomonitoring ecosystem change: Strengths and pitfalls, Mol. Ecol. Resour., 21, 1–19, https://doi.org/10.1111/1755-0998.13302, 2020.
Baldrian, P. and Kohout, P.: Interactions of saprotrophic fungi with tree roots: can we observe the emergence of novel ectomycorrhizal fungi?, New Phytol., 215, 511–513, https://doi.org/10.1111/nph.14665, 2017.
Bastian, M., Heymann, S., and Jacomy, M.: Gephi: an open source software for exploring and manipulating networks, in: Proceedings of the international AAAI conference on web and social media, 3, 361–362, https://doi.org/10.1609/icwsm.v3i1.13937, 2009.
Bastida, F., García, C., Fierer, N., Eldridge, D. J., Bowker, M. A., Abades, S., Alfaro, F. D., Behre, A. A., Cutler, N. A., Gallardo, A., García-Velázquez, L., Hart, S. C., Hayes, P. E., Hernández, T., Hseu, Z., Jehmlich, M., Kirchmair, M., Lambers, H., Neuhauser, S., Peña-Ramírez, V. M., Pérez, C. A., Reed, S. C., Santos, F., Siebe, C., Sullivan, B. W., Trivedi, P., Vera, A., Williams, M. A., Moreno, J. L., and Delgado-Baquerizo, M.: Global ecological predictors of the soil priming effect, Nat. Commun., 10, 1–9, https://doi.org/10.1038/s41467-019-11472-7, 2019.
Berry, D. and Widder, S.: Deciphering microbial interactions and detecting keystone species with co-occurrence networks, Front. Microbiol., 5, 90985, https://doi.org/10.3389/fmicb.2014.00219, 2014.
Blondel, V. D., Guillaume, J. L., Lambiotte, R., and Lefebvre, E.: Fast unfolding of communities in large networks, J. Stat. Mech.-Theory E., 2008, P10008, https://doi.org/10.1088/1742-5468/2008/10/P10008, 2008.
Carvalhais, L. C. and Dennis, P. G. (Eds): The Plant Microbiome: Methods and Protocols, Springer US, 155–171, https://doi.org/10.1007/978-1-0716-1040-4, 2021.
Centenaro, G., de Miguel, S., Amouzgar, L., Piñuela, Y., Son, D., Bonet, J. A., Aragon, J. M., Dashevskaya, S., Cataño, C., and Alday, J. G.: Silvicultural management and altitude prevail on soil properties and fungal community in shaping understorey plant communities in a Mediterranean pine forest, Sci. Total Environ., 858, 159860, https://doi.org/10.1016/j.scitotenv.2022.159860, 2023.
Cheeke, T. E., Phillips, R. P., Brzostek, E. R., Rosling, A., Bever, J. D., and Fransson, P.: Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function, New Phytol., 214, 432–442, https://doi.org/10.1111/nph.14343, 2017.
Chomicki, G., Weber, M., Antonelli, A., Bascompte, J., and Kiers, E. T.: The impact of mutualisms on species richness, Trends Ecol. Evol., 34, 698–711, https://doi.org/10.1016/j.tree.2019.03.003, 2019.
Cole, J. R., Wang, Q., Fish, J. A., Chai, B., McGarrell, D. M., Sun, Y., Brown, C. T., Porras-Alfaro, A., Kuske, C. R., and Tiedje, J.M.: Ribosomal Database Project: Data and tools for high throughput rRNA analysis, Nucl. Acid. Res., 42, 633–642, https://doi.org/10.1093/nar/gkt1244, 2014.
Courty, P. E., Buée, M., Diedhiou, A. G., Frey-Klett, P., Le Tacon, F., Rineau, F., Turpault, M. P., Uroz, S., and Garbaye, J.: The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts, Soil Biol. Biochem., 42, 679–698, https://doi.org/10.1016/j.soilbio.2009.12.006, 2010.
Csardi, G. and Nepusz, T.: The igraph software package for complex network research, InterJournal, complex systems, 1695, 1–9, https://igraph.org (last access: 31 July 2023), 2006.
Davison, J., Moora, M., Semchenko, M., Adenan, S. B., Ahmed, T., Akhmetzhanova, A. A., Alatalo, J. M., Al-Quraishy, S., Andriyanova, E., Anslan, S., Bahram, M., Batbaatar, A., Brown, C., Bueno, C. G., Cahill, J., Cantero, J. J., Casper, B. B., Cherosov, M., Chideh, S., Coelho, A. P., Coghill, M., Decocq, G., Dudov, S., Chimbioputo Fabiano, E., Fedosov, V. E., Fraser, L., Glassman, S. I., Helm, A., Henry, H. A. L., Hérault, B., Hiiesalu, I., Hiiesalu, I., Hozzein, W. N., Kohout, P., Kõljalg, U., Koorem, K., Laanisto, L., Mander, Ü., Mucina, L., Munyampundu, J., Neuenkamp, L., Niinemets, Ü., Nyamukondiwa, C., Oja, J., Onipchenko, V., Pärtel, M., Phosri, C., Põlme, S., Püssa, K., Ronk, A., Saitta, A., Semboli, O., Sepp, S., Seregin, A., Sudheer, S., Peña-Venegas, C. P., Paz, C., Vahter, T., Vasar, M., Veraart, A. J., Tedersoo, L., Zobel, M., and Öpik, M.: Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi, New Phytol., 231, 763–776, https://doi.org/10.1111/nph.17240, 2021.
Davison, J., Vasar, M., Sepp, S. K., Oja, J., Al-Quraishy, S., Bueno, C. G., Cantero, J. J., Fabiano, E. C., Decocq, G., Fraser, L., Hiiesalu, I., Hozzein, W. N., Koorem, K., Moora, M., Mucina, L., Onipchenko, V., Öpik, M., Pärtel, M., Phosri, C., Semchenko, M., Vahter, T., Tedersoo, L., and Zobel, M.: Dominance, diversity, and niche breadth in arbuscular mycorrhizal fungal communities, Ecology, 103, e3761, https://doi.org/10.1002/ecy.3761, 2022.
Debray, R., Herbert, R. A., Jaffe, A. L., Crits-Christoph, A., Power, M. E., and Koskella, B.: Priority effects in microbiome assembly, Nat. Rev. Microbiol., 20, 109–121, https://doi.org/10.1038/s41579-021-00604-w, 2022.
Deguchi, T., Takahashi, K., Takayasu, H., and Takayasu, M.: Hubs and authorities in the world trade network using a weighted HITS algorithm, PLoS ONE, 9, 1–16, https://doi.org/10.1371/journal.pone.0100338, 2014.
Delgado-Baquerizo, M., Maestre, F. T., Reich, P. B., Jeffries, T. C., Gaitan, J. J., Encinar, D., Berdugo, M., Campbell, C. D., and Singh, B. K.: Microbial diversity drives multifunctionality in terrestrial ecosystems, Nat. Commun., 7, 1–8, https://doi.org/10.1038/ncomms10541, 2016.
Delmas, E., Besson, M., Brice, M. H., Burkle, L. A., dalla Riva, G. V., Fortin, M. J., Gravel, D., Guimarães Jr, P. R., Hembry, D. H., Newman, E. A., Olesen, J. M., Pires, M. M., Yeakel, J. D., and Poisot, T.: Analysing ecological networks of species interactions, Biol. Rev., 94, 16–36, https://doi.org/10.1111/brv.12433, 2019.
Fruchterman, T. M. and Reingold, E. M.: Graph drawing by force-directed placement, Softw. Pract. Exper., 21, 1129–1164, https://doi.org/10.1002/spe.4380211102, 1991.
Garrido, J. L., Alcántara, J. M., López-García, Á., Ozuna, C. V., Perea, A. J., Prieto, J., Rincón, A., and Azcón-Aguilar, C.: The structure and ecological function of the interactions between plants and arbuscular mycorrhizal fungi through multilayer networks, Funct. Ecol., 37, 2217–2230, https://doi.org/10.1111/1365-2435.14378, 2023.
Glassman, S. I., Wang, I. J., and Bruns, T. D.: Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales, Mol. Ecol., 26, 6960–6973, https://doi.org/10.1111/mec.14414, 2017.
Gloor, G. B., Macklaim, J. M., Pawlowsky-Glahn, V., and Egozcue, J. J.: Microbiome datasets are compositional: And this is not optional, Front. Microbiol., 8, 2224, https://doi.org/10.3389/fmicb.2017.02224, 2017.
Goberna, M. and Verdú, M.: Cautionary notes on the use of co-occurrence networks in soil ecology, Soil Biol. Biochem., 166, 108534, https://doi.org/10.1016/j.soilbio.2021.108534, 2022.
Götzenberger, L., de Bello, F., Bråthen, K. A., Davison, J., Dubuis, A., Guisan, A., Lepš, J., Lindborg, R., Moora, M., Pärtel, M., Pellissier, L., Pottier, J., Vittoz, P., Zobel, K., and Zobel, M.: Ecological assembly rules in plant communities-approaches, patterns and prospects, Biol. Rev., 87, 111–127, https://doi.org/10.1111/j.1469-185X.2011.00187.x, 2012.
Gouveia, C., Móréh, Á., and Jordán, F.: Combining centrality indices: Maximizing the predictability of keystone species in food webs, Ecol. Indic., 126, 107617, https://doi.org/10.1016/j.ecolind.2021.107617, 2021.
Gutiérrez-Girón, A., Díaz-Pinés, E., Rubio, A., and Gavilán, R. G.: Both altitude and vegetation affect temperature sensitivity of soil organic matter decomposition in Mediterranean high mountain soils, Geoderma, 237, 1–8, https://doi.org/10.1016/j.geoderma.2014.08.005, 2015.
Hernandez, D. J., David, A. S., Menges, E. S., Searcy, C. A., and Afkhami, M. E.: Environmental stress destabilizes microbial networks, ISME J., 15, 1722–1734, https://doi.org/10.1038/s41396-020-00882-x, 2021.
Jacomy, M., Venturini, T., Heymann, S., and Bastian, M.: ForceAtlas2, a continuous graph layout algorithm for handy network visualization designed for the Gephi software, PLoS ONE, 9, 1–12, https://doi.org/10.1371/journal.pone.0098679, 2014.
Ji, L., Yang, Y., and Yang, L.: Seasonal variations in soil fungal communities and co-occurrence networks along an altitudinal gradient in the cold temperate zone of China: A case study on Oakley Mountain, Catena, 204, 105448, https://doi.org/10.1016/j.catena.2021.105448, 2021.
Kadowaki, K., Yamamoto, S., Sato, H., Tanabe, A. S., Hidaka, A., and Toju, H.: Mycorrhizal fungi mediate the direction and strength of plant–soil feedbacks differently between arbuscular mycorrhizal and ectomycorrhizal communities, Commun. Biol., 1, 196, https://doi.org/10.1038/s42003-018-0201-9, 2018.
Kennedy, P. G., Peay, K. G., and Bruns, T. D.: Root tip competition among ectomycorrhizal fungi: Are priority effects a rule or an exception?, Ecology, 90, 2098–2107, https://doi.org/10.1890/08-1291.1, 2009.
Krapu, C. and Borsuk, M.: A spatial community regression approach to exploratory analysis of ecological data, Methods Ecol. Evol., 11, 608–620, https://doi.org/10.1111/2041-210X.13371, 2020.
Kurtz, Z. D., Müller, C. L., Miraldi, E. R., and Littman, D. R.: Sparse and Compositionally Robust Inference of Microbial Ecological Networks, Plos Comput. Biol., 11, 1–25, https://doi.org/10.1371/journal.pcbi.1004226, 2015.
Lamanna, J. A., Walton, M. L., Turner, B. L., and Myers, J. A.: Negative density dependence is stronger in resource-rich environments and diversifies communities when stronger for common but not rare species, Ecol. Lett., 19, 657–667, https://doi.org/10.1111/ele.12603, 2016.
Lassalle, G., Credoz, A., Hédacq, R., Bertoni, G., Dubucq, D., Fabre, S., and Elger, A.: Estimating persistent oil contamination in tropical region using vegetation indices and random forest regression, Ecotox. Environ. Safe., 184, 109654, https://doi.org/10.1016/j.ecoenv.2019.109654, 2019.
Lebreton, A., Zeng, Q., Miyauchi, S., Kohler, A., Dai, Y. C., and Martin, F. M.: Evolution of the mode of nutrition in symbiotic and saprotrophic fungi in forest ecosystems, Annu. Rev. Ecol. Evol. S., 52, 385–404, https://doi.org/10.1146/annurev-ecolsys-012021-114902, 2021.
Le Bagousse-Pinguet, Y., Soliveres, S., Gross, N., Torices, R., Berdugo, M., and Maestre, F. T.: Phylogenetic, functional, and taxonomic richness have both positive and negative effects on ecosystem multifunctionality, P. Natl. Acad. Sci. USA, 116, 8419–8424, https://doi.org/10.1073/pnas.1815727116, 2019.
Liang, M., Johnson, D., Burslem, D. F. R. P., Yu, S., Fang, M., Taylor, J. D., Taylor, A. F. S., Helgason, T., and Liu, X.: Soil fungal networks maintain local dominance of ectomycorrhizal trees, Nat. Commun., 11, 1–7, https://doi.org/10.1038/s41467-020-16507-y, 2020.
Liu, H., Roeder, K., and Wasserman, L.: Stability Approach to Regularization Selection (StARS) for High Dimensional Graphical Models, Advances in Neural Information Processing Systems, 23, https://proceedings.neurips.cc/paper_files/paper/2010/file/301ad0e3bd5cb1627a2044908a42fdc2-Paper.pdf (last access: 18 June 2024), 2010.
Liu, S., García-Palacios, P., Tedersoo, L., Guirado, E., van der Heijden, M. G., Wagg, C., Chen, D., Wang, Q., Wang, J., Singh, B. K., and Delgado-Baquerizo, M.: Phylotype diversity within soil fungal functional groups drives ecosystem stability, Nat. Ecol. Evol., 6, 900–909, https://doi.org/10.1038/s41559-022-01756-5, 2022.
Luo, S., Png, K., Ostle, N. J., Zhou, H., Hou, X., Luo, C., Quinton, J. N., Schaffner, U., Sweeney, C., Wang, D., Wu, J., Wu, Y., and Bardgett, R. D.: Grassland degradation-induced declines in soil fungal complexity reduce fungal community stability and ecosystem multifunctionality, Soil Biol. Biochem., 176, 108865, https://doi.org/10.1016/j.soilbio.2022.108865, 2022.
Mamet, S. D., Redlick, E., Brabant, M., Lamb, E. G., Helgason, B. L., Stanley, K., and Siciliano, S. D.: Structural equation modeling of a winnowed soil microbiome identifies how invasive plants re-structure microbial networks, ISME J., 13, 1988–1996, https://doi.org/10.1038/s41396-019-0407-y, 2019.
Mandakovic, D., Rojas, C., Maldonado, J., Latorre, M., Travisany, D., Delage, E., Bihouée, A., Jean, G., Díaz, F. P., Fernández-Gómez, B., Cabrera, P., Gaete, A., Latorre, C., Gutiérrez, R. A., Maass, A., Cambiazo, V., Navarrete, S. A., Eveillard, D., and González, M.: Structure and co-occurrence patterns in microbial communities under acute environmental stress reveal ecological factors fostering resilience, Sci. Rep., 8, 1–12, https://doi.org/10.1038/s41598-018-23931-0, 2018.
Martin, F. M. and van der Heijden, M. G. A.: The mycorrhizal symbiosis: research frontiers in genomics, ecology, and agricultural application, New Phytol., 242, 1486–1506, https://doi.org/10.1111/nph.19541, 2024.
Mazel, F., Pennell, M. W., Cadotte, M. W., Diaz, S., Dalla Riva, G. V., Grenyer, R., Leprieur, F., Mooers, A. O., Mouillot, D., Tucker, C. M., and Pearse, W.: Prioritizing phylogenetic diversity captures functional diversity unreliably, Nat Commun., 9, 2888, https://doi.org/10.1038/s41467-018-05126-3, 2018.
Meinshausen, N. and Bühlmann, P.: High-dimensional graphs and variable selection with the Lasso, Ann. Stat., 34, 1436–1462, https://doi.org/10.1214/009053606000000281, 2006.
Meyer, S. T., Ptacnik, R., Hillebrand, H., Bessler, H., Buchmann, N., Ebeling, A., Eisenhauer, N., Engels, C., Fischer, M., Halle, S., Klein, A., Oelmann, Y., Roscher, C., Rottstock, T., Scherber, C., Scheu, S., Schmid, B., Schulze, E., Temperton, V. M., Tscharntke, T., Voigt, W., Weigelt, A., Wilcke, W., and Weisser, W. W.: Biodiversity-multifunctionality relationships depend on identity and number of measured functions, Nat. Ecol. Evol., 2, 44–49, https://doi.org/10.1038/s41559-017-0391-4, 2018.
Miyauchi, S., Kiss, E., Kuo, A., Drula, E., Kohler, A., Sánchez-García, M., Morin, E., Andreopoulos, B., Barry, K. W., Bonito, G., Buée, M., Carver, A., Chen, C., Cichocki, N., Clum, A., Culley, D., Crous, P. W., Fauchery, L., Girlanda, M., Hayes, R. D., Kéri, Z., LaButti, K., Lipzen, A., Lombard, V., Magnuson, J., Maillard, F., Murat, C., Nolan, M., Ohm, R. A., Pangilinan, J., Pereira, M., Perotto, S., Peter, M., Pfister, S., Riley, R., Sitrit, Y., Stielow, J. B., Szöllõsi, G., Žifèáková, L., Štursová, M., Spatafora, J. W., Tedersoo, L., Vaario, L., Yamada, A., Yan, M., Wang, P., Xu, J., Bruns, T., Baldrian, P., Vilgalys, R., Dunand, C., Henrissat, B., Grigoriev, I. V., Hibbett, D., Nagy, L. G., and Martin, F. M.: Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits, Nat. Commun., 11, 1–17, https://doi.org/10.1038/s41467-020-18795-w, 2020.
Morueta-Holme, N., Blonder, B., Sandel, B., McGill, B. J., Peet, R. K., Ott, J. E., Violle, C., Enquist, B. J., Jørgensen, P. M., and Svenning, J. C.: A network approach for inferring species associations from co-occurrence data, Ecography, 39, 1139–1150. https://doi.org/10.1111/ecog.01892, 2016.
Nguyen, D. Q., Schneider, D., Brinkmann, N., Song, B., Janz, D., Schöning, I., Daniel, R., and Polle, A.: Soil and root nutrient chemistry structure root-associated fungal assemblages in temperate forests, Environ. Microbiol., 22, 3081–3095, https://doi.org/10.1111/1462-2920.15037, 2020.
Nguyen, N. H.: Fungal Hyphosphere Microbiomes Are Distinct from Surrounding Substrates and Show Consistent Association Patterns, Microb. Spec., 11, e04708-22, https://doi.org/10.1128/spectrum.04708-22, 2023.
Nguyen, N. H., Song, Z., Bates, S. T., Branco, S., Tedersoo, L., Menke, J., Schilling, J. S., and Kennedy, P. G.: FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild, Fungal Ecol., 20, 241–248, https://doi.org/10.1016/j.funeco.2015.06.006, 2016.
Oksanen, J., Simpson, G. L., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., Solymos, P., Stevens, M. H. H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., De Caceres, M., Durand, S., Evangelista, H. B. A., FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M. O., Lahti, L., McGlinn, D., Ouellette, M., Cunha, E. D., Smith, T., Stier, A., Ter Braak, C. J. F., and Weedon, J.: vegan: Community Ecology Package, R package version 2.6-4, https://CRAN.R-project.org/package=vegan (last access: 30 September 2023), 2022.
Pajares-Murgó, M., Garrido, J. L., Perea, A. J., López-García, Á., and Alcántara, J. M.: Biotic filters driving the differentiation of decomposer, epiphytic and pathogenic phyllosphere fungi across plant species, Oikos, 2023, e09624, https://doi.org/10.1111/oik.09624, 2023.
Pauvert. C., Buée, M., Laval, V., Edel-Hermann, V., Fauchery, L., Gautier, A., Lesur, I., Vallance, J., and Vacher, C.: Bioinformatics matters: The accuracy of plant and soil fungal community data is highly dependent on the metabarcoding pipeline, Fungal Ecol., 41, 23–33, https://doi.org/10.1016/j.funeco.2019.03.005, 2019.
Pérez-Izquierdo, L., Zabal-Aguirre, M., Flores-Rentería, D., González-Martínez, S. C., Buée, M., and Rincón, A.: Functional outcomes of fungal community shifts driven by tree genotype and spatial-temporal factors in Mediterranean pine forests, Environ. Microbiol., 19, 1639–1652, https://doi.org/10.1111/1462-2920.13690, 2017.
Pérez-Izquierdo, L., Saint-André, L., Santenoise, P., Buée, M., and Rincón, A.: Tree genotype and seasonal effects on soil properties and biogeochemical functioning in Mediterranean pine forests, Eur. J. Soil Sci., 69, 1087–1097, https://doi.org/10.1111/ejss.12712, 2018.
Pérez-Izquierdo, L., Zabal-Aguirre, M., Verdú, M., Buée, M., and Rincón, A.: Ectomycorrhizal fungal diversity decreases in Mediterranean pine forests adapted to recurrent fires, Mol. Ecol., 1–14, 2463–2476, https://doi.org/10.1111/mec.15493, 2020.
Pérez-Valera, E., Goberna, M., Faust, K., Raes, J., García, C., and Verdú, M.: Fire modifies the phylogenetic structure of soil bacterial co-occurrence networks, Environ. Microbiol., 19, 317–327, https://doi.org/10.1111/1462-2920.13609, 2017.
Poudel, R., Jumpponen, A., Schlatter, D. C., Paulitz, T. C., Gardener, B. B. M., Kinkel, L. L., and Garrett, K. A.: Microbiome Networks: A Systems Framework for Identifying Candidate Microbial Assemblages for Disease Management, Phytopathology, 106, 1083–1096, https://doi.org/10.1094/PHYTO-02-16-0058-FI, 2016.
Pritsch, K. and Garbaye, J.: Enzyme secretion by ECM fungi and exploitation of mineral nutrients from soil organic matter, Ann. Forest Sci., 68, 25–32, https://doi.org/10.1007/s13595-010-0004-8, 2011.
Prieto-Rubio, J., Garrido, J. L., Pérez-Izquierdo, L., Alcántara, J. M., Azcón-Aguilar, C., López-García, A., and Rincón, A.: Scale dependency of ectomycorrhizal fungal community assembly processes in Mediterranean mixed forests, Mycorrhiza, 32, 315–325, https://doi.org/10.1007/s00572-022-01083-4, 2022.
Prieto-Rubio, J., Perea, A., Garrido, J. L., Alcántara, J. M., Azcón-Aguilar, C., López-García, A., and Rincón, A.: Plant Traits and Phylogeny Predict Soil Carbon and Nutrient Cycling in Mediterranean Mixed Forests, Ecosystems, 26, 1047–1060, https://doi.org/10.1007/s10021-022-00815-z, 2023.
Pulgar, M., Alcántara, J. M., and Rey, P. J.: Effects of sampling effort on estimates of the structure of replacement networks, J. Veg. Sci., 28, 445–457, https://doi.org/10.1111/jvs.12492, 2017.
Rincón, A., Santamaría, B. P., Ocaña, L., and Verdú, M.: Structure and phylogenetic diversity of post-fire ectomycorrhizal communities of maritime pine, Mycorrhiza, 24, 131–141, https://doi.org/10.1007/s00572-013-0520-0, 2014.
Rincón, A., Santamaría-Pérez, B., Rabasa, S. G., Coince, A., Marçais, B., and Buée, M.: Compartmentalized and contrasted response of ectomycorrhizal and soil fungal communities of s cots pine forests along elevation gradients in f rance and s pain, Environ. Microbiol., 17, 3009–3024, https://doi.org/10.1111/1462-2920.12894, 2015.
Rivas-Martínez, S.: Memoria del mapa de series de vegetación de España 1:400.000, 268 pp., ICONA, Ministerio de Agricultura, Pesca y Alimentación, Madrid, 1987.
Segnitz, R. M., Russo, S. E., Davies, S. J., and Peay, K. G.: Ectomycorrhizal fungi drive positive phylogenetic plant–soil feedbacks in a regionally dominant tropical plant family, Ecology, 101, 1–15, https://doi.org/10.1002/ecy.3083, 2020.
Siles, G., Rey, P. J., Alcántara, J. M., and Ramírez, J. M.: Assessing the long-term contribution of nurse plants to restoration of Mediterranean forests through Markovian models, J. App. Ecol., 45, 1790–1798, https://doi.org/10.1111/j.1365-2664.2008.01574.x, 2008.
Siles, J. A. and Margesin, R.: Seasonal soil microbial responses are limited to changes in functionality at two Alpine forest sites differing in altitude and vegetation, Sci. Rep., 7, 1–16, https://doi.org/10.1038/s41598-017-02363-2, 2017.
Smith, S. and Read, D.: Mycorrhizal Symbiosis, Elsevier Ltd., https://doi.org/10.1016/B978-0-12-370526-6.X5001-6, 2008.
Trivedi, P., Delgado-Baquerizo, M., Trivedi, C., Hu, H., Anderson, I. C., Jeffries, T. C., Zhou, J., and Singh, B. K.: Microbial regulation of the soil carbon cycle: Evidence from gene-enzyme relationships, ISME J., 10, 2593–2604, https://doi.org/10.1038/ismej.2016.65, 2008.
Trivedi, P., Delgado-Baquerizo, M., Trivedi, C., Hu, H., Anderson, I. C., Jeffries, T. C., Zou, J., and Singh, B. K.: Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships, ISME J., 10, 2593–2604, https://doi.org/10.1038/ismej.2016.65, 2016.
Tripathi, B. M., Stegen, J. C., Kim, M., Dong, K., Adams, J. M., and Lee, Y. K.: Soil pH mediates the balance between stochastic and deterministic assembly of bacteria, ISME J., 12, 1072–1083, https://doi.org/10.1038/s41396-018-0082-4, 2018.
Van der Heijden, M. G., Martin, F. M., Selosse, M. A., and Sanders, I. R.: Mycorrhizal ecology and evolution: the past, the present, and the future, New Phytol., 205, 1406–1423, https://doi.org/10.1111/nph.13288, 2015.
Vandenkoornhuyse, P., Quaiser, A., Duhamel, M., Le Van, A., and Dufresne, A.: The importance of the microbiome of the plant holobiont, New Phytol., 206, 1196–1206, https://doi.org/10.1111/nph.13312, 2015.
Wagg, C., Schlaeppi, K., Banerjee, S., Kuramae, E. E., and van der Heijden, M. G.: Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning, Nat. Commun., 10, 4841, https://doi.org/10.1038/s41467-019-12798-y, 2019.
Wagg, C., Hautier, Y., Pellkofer, S., Banerjee, S., Schmid, B., and van der Heijden, M. G. A.: Diversity and asynchrony in soil microbial communities stabilizes ecosystem functioning, ELife, 10, 1–19, https://doi.org/10.7554/eLife.62813, 2021.
Walkley, A. and Black, I. A.: An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method, Soil Sci., 37, 29–38, 1934.
Wang, J., Liao, L., Wang, G., Liu, H., Wu, Y., Liu, G., and Zhang, C.: N-induced root exudates mediate the rhizosphere fungal assembly and affect species coexistence, Sci. Total Environ., 804, 150148, https://doi.org/10.1016/j.scitotenv.2021.150148, 2022.
Wang, S., Isbell, F., Deng, W., Hong, P., Dee, L. E., Thompson, P., and Loreau, M.: How complementarity and selection affect the relationship between ecosystem functioning and stability, Ecology, 102, 1–12, https://doi.org/10.1002/ecy.3347, 2021.
Ward, E. B., Duguid, M. C., Kuebbing, S. E., Lendemer, J. C., Warren, R. J., and Bradford, M. A.: Ericoid mycorrhizal shrubs alter the relationship between tree mycorrhizal dominance and soil carbon and nitrogen, J. Ecol., 109, 3524–3540, https://doi.org/10.1111/1365-2745.13734, 2021.
Watts, S. C., Ritchie, S. C., Inouye, M., and Holt, K. E.: FastSpar: Rapid and scalable correlation estimation for compositional data, Bioinformatics, 35, 1064–1066, https://doi.org/10.1093/bioinformatics/bty734, 2019.
Wu, B.-W., Gao, C., Chen, L., Buscot, F., Goldmann, K., Purahong, W., Ji, N. N., Wang, Y. L., Lü, P. P., Li, X. C., and Guo, L. D.: Host Phylogeny Is a Major Determinant of Fagaceae-Associated Ectomycorrhizal Fungal Community Assembly at a Regional Scale, Front. Microbiol., 9, 1–12, https://doi.org/10.3389/fmicb.2018.02409, 2018.
Xun, W., Liu, Y., Li, W., Ren, Y., Xiong, W., Xu, Z., Zhang, N., Miao, Y., Shen, Q., and Zhang, R.: Specialized metabolic functions of keystone taxa sustain soil microbiome stability, Microbiome, 9, 1–15, https://doi.org/10.1186/s40168-020-00985-9, 2021.
Zhan, P., Liu, Y., Wang, H., Wang, C., Xia, M., Wang, N., Cui, W., Xiao, D., and Wang, H.: Plant litter decomposition in wetlands is closely associated with phyllospheric fungi as revealed by microbial community dynamics and co-occurrence network, Sci. Total Environ., 753, 142194, https://doi.org/10.1016/j.scitotenv.2020.142194, 2021.
Zobel, M., Koorem, K., Moora, M., Semchenko, M., and Davison, J.: Symbiont plasticity as a driver of plant success, New Phytol., 241, 2340–2352, https://doi.org/10.1111/nph.19566, 2024.
Zou, H. and Hastie, T.: Regularization and variable selection via the elastic net, J. Roy. Stat. Soc. B., 67, 301–320, https://doi.org/10.1111/j.1467-9868.2005.00503.x, 2005.
Short summary
Changes in soil biological activity when microbial taxa interact remain little understood. To address this, we approach network analyses of ectomycorrhizal fungal communities. The study highlights how distinct fungi contribute to explaining community structure, whilst others mainly do for soil enzymatic activity. This differentiation between structural and functional roles of ectomycorrhizal fungi adds new insights to understand soil fungal community complexity and its functionality in soils.
Changes in soil biological activity when microbial taxa interact remain little understood. To...
