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.
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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Straw return with diverse nitrogen fertilizer application rates modulate ecosystem services and microbial traits in a meadow soil
Biochar promotes soil aggregate stability and associated organic carbon sequestration and regulates microbial community structures in Mollisols from northeast China
Only a minority of bacteria grow after wetting in both natural and post-mining biocrusts in a hyperarid phosphate mine
Lower functional redundancy in “narrow” than “broad” functions in global soil metagenomics
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Network complexity of rubber plantations is lower than tropical forests for soil bacteria but not for fungi
Changes in soil physicochemical properties and bacterial communities at different soil depths after long-term straw mulching under a no-till system
Microbial communities and their predictive functional profiles in the arid soil of Saudi Arabia
Development of a soil biological quality index for soils of semi-arid tropics
What do we know about how the terrestrial multicellular soil fauna reacts to microplastic?
Soil microbial biomass and function are altered by 12 years of crop rotation
Soil denitrifier community size changes with land use change to perennial bioenergy cropping systems
Knowledge needs, available practices, and future challenges in agricultural soils
Technological advancements and their importance for nematode identification
Fire affects root decomposition, soil food web structure, and carbon flow in tallgrass prairie
Case study of microarthropod communities to assess soil quality in different managed vineyards
A meta-analysis of soil biodiversity impacts on the carbon cycle
Christophe Djemiel, Samuel Dequiedt, Walid Horrigue, Arthur Bailly, Mélanie Lelièvre, Julie Tripied, Charles Guilland, Solène Perrin, Gwendoline Comment, Nicolas P. A. Saby, Claudy Jolivet, Antonio Bispo, Line Boulonne, Antoine Pierart, Patrick Wincker, Corinne Cruaud, Pierre-Alain Maron, Sébastien Terrat, and Lionel Ranjard
SOIL, 10, 251–273, https://doi.org/10.5194/soil-10-251-2024, https://doi.org/10.5194/soil-10-251-2024, 2024
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The fungal kingdom has been diversifying for more than 800 million years by colonizing a large number of habitats on Earth. Based on a unique dataset (18S rDNA meta-barcoding), we described the spatial distribution of fungal diversity at the scale of France and the environmental drivers by tackling biogeographical patterns. We also explored the fungal network interactions across land uses and climate types.
Yan Duan, Minghui Cao, Wenling Zhong, Yuming Wang, Zheng Ni, Mengxia Zhang, Jiangye Li, Yumei Li, Xianghai Meng, and Lifang Wu
EGUsphere, https://doi.org/10.5194/egusphere-2023-2498, https://doi.org/10.5194/egusphere-2023-2498, 2023
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Nitrogen (N) fertilization has received worldwide attention due to its effects on ecosystem services. However, soil multifunctionality and the underlying microbial mechanisms remain unclear. Therefore, we carried out in-situ field and incubation experiments. We propose that: straw return with 25 % N fertilizer reduction may achieve high soil multifunctionality by regulating soil C:N ratio and N input level and specific keystone taxa-driven community contributed to soil ecology services.
Jing Sun, Xinrui Lu, Guoshuang Chen, Nana Luo, Qilin Zhang, and Xiujun Li
SOIL, 9, 261–275, https://doi.org/10.5194/soil-9-261-2023, https://doi.org/10.5194/soil-9-261-2023, 2023
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A field experiment was conducted to compare and analyze the effects of combined application of biochar and nitrogen fertilizer on soil aggregate stability mechanism, the dynamic characteristics of aggregate organic carbon, and the microbial community structure in northeast black soil. We provide a scientific basis for formulating effective strategies to slow down soil quality degradation and ensure the sustainable development of the agroecosystem.
Talia Gabay, Eva Petrova, Osnat Gillor, Yaron Ziv, and Roey Angel
SOIL, 9, 231–242, https://doi.org/10.5194/soil-9-231-2023, https://doi.org/10.5194/soil-9-231-2023, 2023
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This paper evaluates bacterial growth in biocrusts after a large-scale mining disturbance in a hyperarid desert, using a stable isotope probing assay.
We discovered that biocrust bacteria from both natural and post-mining plots resumed photosynthetic activity but did not grow following hydration. Our paper provides insights into the effects of a large-scale disturbance (mining) on biocrusts and their response to hydration, with implications for biocrust restoration practices in Zin mines.
Huaihai Chen, Kayan Ma, Yu Huang, Qi Fu, Yingbo Qiu, Jiajiang Lin, Christopher W. Schadt, and Hao Chen
SOIL, 8, 297–308, https://doi.org/10.5194/soil-8-297-2022, https://doi.org/10.5194/soil-8-297-2022, 2022
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By analyzing and generalizing microbial taxonomic and functional profiles, we provide strong evidence that the degree of soil microbial functional redundancy differs significantly between “broad” and “narrow” functions across the globe. Future sequencing efforts will likely increase our confidence in comparative metagenomes and provide time-series information to further identify to what extent microbial functional redundancy regulates dynamic ecological fluxes across space and time.
Anne Daebeler, Eva Petrová, Elena Kinz, Susanne Grausenburger, Helene Berthold, Taru Sandén, Roey Angel, and the high-school students of biology project groups I, II, and
III from 2018–2019
SOIL, 8, 163–176, https://doi.org/10.5194/soil-8-163-2022, https://doi.org/10.5194/soil-8-163-2022, 2022
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In this citizen science project, we combined a standardised litter bag method (Tea Bag Index) with microbiome analysis of bacteria and fungi colonising the teabags to gain a holistic understanding of the carbon degradation dynamics in temperate European soils. Our method focuses only on the active part of the soil microbiome. The results show that about one-third of the prokaryotes and one-fifth of the fungal species (ASVs) in the soil were enriched in response to the presence of fresh OM.
Guoyu Lan, Chuan Yang, Zhixiang Wu, Rui Sun, Bangqian Chen, and Xicai Zhang
SOIL, 8, 149–161, https://doi.org/10.5194/soil-8-149-2022, https://doi.org/10.5194/soil-8-149-2022, 2022
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Forest conversion alters both bacterial and fungal soil networks: it reduces bacterial network complexity and enhances fungal network complexity. This is because forest conversion changes the soil pH and other soil properties, which alters the bacterial composition and subsequent network structure. Our study demonstrates the impact of forest conversion on soil network structure, which has important implications for ecosystem functions and the health of soil ecosystems in tropical regions.
Zijun Zhou, Zengqiang Li, Kun Chen, Zhaoming Chen, Xiangzhong Zeng, Hua Yu, Song Guo, Yuxian Shangguan, Qingrui Chen, Hongzhu Fan, Shihua Tu, Mingjiang He, and Yusheng Qin
SOIL, 7, 595–609, https://doi.org/10.5194/soil-7-595-2021, https://doi.org/10.5194/soil-7-595-2021, 2021
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Straw mulching is not always combined with no-till systems during conservation tillage. We explored the effects of long-term straw mulching on soil attributes with soil depths under a no-till system. Compared to straw removal, straw mulching had various effects on soil properties at different depths, the biggest difference occurring at the topsoil depth. Overall, straw mulch is highly recommended for use under the no-till system because of its benefits to soil fertility and bacterial abundance.
Munawwar A. Khan and Shams T. Khan
SOIL, 6, 513–521, https://doi.org/10.5194/soil-6-513-2020, https://doi.org/10.5194/soil-6-513-2020, 2020
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Soil is a renewable resource for purposes ranging from agriculture to mineralization. Soil microbiome plays vital roles in facilitating process like providing nutrients to plants, or their mobilization for plant uptake, consequently improving plant growth and productivity. Therefore, understanding of these microbial communities and their role in soil is crucial for exploring the possibility of using microbial community inoculants for improving desert soil fertility and agricultural potential.
Selvaraj Aravindh, Chinnappan Chinnadurai, and Dananjeyan Balachandar
SOIL, 6, 483–497, https://doi.org/10.5194/soil-6-483-2020, https://doi.org/10.5194/soil-6-483-2020, 2020
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Soil quality is important for functioning of the agricultural ecosystem to sustain productivity. It is combination of several physical, chemical, and biological attributes. In the present work, we developed a soil biological quality index, a sub-set of the soil quality index (SBQI) using six important biological variables. These variables were computed from long-term manurial experimental soils and transformed into a unitless 10-scaled SBQI. This will provide constraints of soil processes.
Frederick Büks, Nicolette Loes van Schaik, and Martin Kaupenjohann
SOIL, 6, 245–267, https://doi.org/10.5194/soil-6-245-2020, https://doi.org/10.5194/soil-6-245-2020, 2020
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Via anthropogenic input, microplastics (MPs) today represent a part of the soil organic matter. We analyzed studies on passive translocation, active ingestion, bioaccumulation and adverse effects of MPs on multicellular soil faunal life. These studies on a wide range of soil organisms found a recurring pattern of adverse effects on motility, growth, metabolism, reproduction, mortality and gut microbiome. However, the shape and type of the experimental MP often did not match natural conditions.
Marshall D. McDaniel and A. Stuart Grandy
SOIL, 2, 583–599, https://doi.org/10.5194/soil-2-583-2016, https://doi.org/10.5194/soil-2-583-2016, 2016
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Modern agriculture is dominated by monoculture crop production, having negative effects on soil biology. We used a 12-year crop rotation experiment to examine the effects of increasing crop diversity on soil microorganisms and their activity. Crop rotations increased microbial biomass by up to 112 %, and increased potential ability to supply nitrogen as much as 58 %, compared to monoculture corn. Collectively, our findings show that soil health is increased when crop diversity is increased.
Karen A. Thompson, Bill Deen, and Kari E. Dunfield
SOIL, 2, 523–535, https://doi.org/10.5194/soil-2-523-2016, https://doi.org/10.5194/soil-2-523-2016, 2016
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Dedicated bioenergy crops are required for future energy production; however the effects of land use change from traditional crops to biofuel crops on soil microbial communities, which drive greenhouse gas production, are largely unknown. We used quantitative PCR to enumerate these microbial communities to assess the sustainability of different bioenergy crops, including miscanthus and corn. We found that miscanthus may be a suitable crop for bioenergy production in variable Ontario conditions.
Georgina Key, Mike G. Whitfield, Julia Cooper, Franciska T. De Vries, Martin Collison, Thanasis Dedousis, Richard Heathcote, Brendan Roth, Shamal Mohammed, Andrew Molyneux, Wim H. Van der Putten, Lynn V. Dicks, William J. Sutherland, and Richard D. Bardgett
SOIL, 2, 511–521, https://doi.org/10.5194/soil-2-511-2016, https://doi.org/10.5194/soil-2-511-2016, 2016
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Enhancing soil health is key to providing ecosystem services and food security. There are often trade-offs to using a particular practice, or it is not fully understood. This work aimed to identify practices beneficial to soil health and gaps in our knowledge. We reviewed existing research on agricultural practices and an expert panel assessed their effectiveness. The three most beneficial practices used a mix of organic or inorganic material, cover crops, or crop rotations.
Mohammed Ahmed, Melanie Sapp, Thomas Prior, Gerrit Karssen, and Matthew Alan Back
SOIL, 2, 257–270, https://doi.org/10.5194/soil-2-257-2016, https://doi.org/10.5194/soil-2-257-2016, 2016
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This review covers the history and advances made in the area of nematode taxonomy. It highlights the success and limitations of the classical approach to nematode taxonomy and provides reader with a bit of background to the applications of protein and DNA-based methods for identification nematodes. The review also outlines the pros and cons of the use of DNA barcoding in nematology and explains how DNA metabarcoding has been applied in nematology through next-generation sequencing.
E. Ashley Shaw, Karolien Denef, Cecilia Milano de Tomasel, M. Francesca Cotrufo, and Diana H. Wall
SOIL, 2, 199–210, https://doi.org/10.5194/soil-2-199-2016, https://doi.org/10.5194/soil-2-199-2016, 2016
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We investigated fire's effects on root decomposition and carbon (C) flow to the soil food web. We used 13C-labeled dead roots buried in microcosms constructed from two burn treatment soils (annual and infrequent burn). Our results showed greater root decomposition and C flow to the soil food web for the annual burn compared to infrequent burn treatment. Thus, roots are a more important C source for decomposers in annually burned areas where surface plant litter is frequently removed by fire.
E. Gagnarli, D. Goggioli, F. Tarchi, S. Guidi, R. Nannelli, N. Vignozzi, G. Valboa, M. R. Lottero, L. Corino, and S. Simoni
SOIL, 1, 527–536, https://doi.org/10.5194/soil-1-527-2015, https://doi.org/10.5194/soil-1-527-2015, 2015
M.-A. de Graaff, J. Adkins, P. Kardol, and H. L. Throop
SOIL, 1, 257–271, https://doi.org/10.5194/soil-1-257-2015, https://doi.org/10.5194/soil-1-257-2015, 2015
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...