A risk assessment framework for the future of forest microbiomes in a changing climate

Nature

A risk assessment framework for the future of forest microbiomes in a changing climate"


Play all audios:

Loading...

ABSTRACT Microbes inhabiting the above- and belowground tissues of forest trees and soils play a critical role in the response of forest ecosystems to global climate change. However,


generalizations about the vulnerability of the forest microbiome to climate change have been challenging due to responses that are often context dependent. Here we apply a risk assessment


framework to evaluate microbial community vulnerability to climate change across forest ecosystems. We define factors that determine exposure risk and processes that amplify or buffer


sensitivity to change, and describe feedback mechanisms that will modulate this exposure and sensitivity as climatic change progresses. This risk assessment approach unites microbial ecology


and forest ecology to develop a more comprehensive understanding of forest vulnerability in the twenty-first century. Access through your institution Buy or subscribe This is a preview of


subscription content, access via your institution ACCESS OPTIONS Access through your institution Access Nature and 54 other Nature Portfolio journals Get Nature+, our best-value


online-access subscription $29.99 / 30 days cancel any time Learn more Subscribe to this journal Receive 12 print issues and online access $209.00 per year only $17.42 per issue Learn more


Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to local taxes which are calculated during checkout ADDITIONAL ACCESS OPTIONS:


* Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS FOREST MICROBIOME AND GLOBAL CHANGE Article 20 March 2023


FUNGAL COMMUNITY COMPOSITION PREDICTS FOREST CARBON STORAGE AT A CONTINENTAL SCALE Article Open access 16 March 2024 UNVEILING AFRICAN RAINFOREST COMPOSITION AND VULNERABILITY TO GLOBAL


CHANGE Article 21 April 2021 REFERENCES * Strassburg, B. B. N. et al. Global priority areas for ecosystem restoration. _Nature_ 586, 724–729 (2020). Article  CAS  Google Scholar  * Miner, K.


et al. The co-production of knowledge for climate science. _Nat. Clim. Change_ 13, 307–308 (2023). Article  Google Scholar  * Terrer, C. et al. A trade-off between plant and soil carbon


storage under elevated CO2. _Nature_ 591, 599–603 (2021). THIS META-ANALYSIS DOCUMENTS THAT MYCORRHIZAL ASSOCIATIONS DICTATE ECOSYSTEM CARBON STORAGE UNDER ELEVATED CO2. TRADE-OFFS ABOVE-


AND BELOWGROUND ARE IMPORTANT FOR MODELLING CARBON SEQUESTRATION DYNAMICS. Article  CAS  Google Scholar  * Haraway, D. Anthropocene, Capitalocene, Plantationocene, Chthulucene: making kin.


_Environ. Humanit._ 6, 159–165 (2015). Article  Google Scholar  * Brodribb, T. J., Powers, J., Cochard, H. & Choat, B. Hanging by a thread? Forests and drought. _Science_ 368, 261–266


(2020). Article  CAS  Google Scholar  * Anderegg, W. R. L. et al. A climate risk analysis of Earth’s forests in the 21st century. _Science_ 377, 1099–1103 (2022). Article  CAS  Google


Scholar  * Dudney, J. et al. Nonlinear shifts in infectious rust disease due to climate change. _Nat. Commun._ 12, 5102 (2021). Article  CAS  Google Scholar  * Allsup, C. M., George, I.


& Lankau, R. A. Shifting microbial communities can enhance tree tolerance to changing climates. _Science_ 380, 835–840 (2023). THIS LARGE-SCALE FIELD EXPERIMENT DEMONSTRATES HOW


INOCULATION OF TREE SEEDLINGS WITH COLD- OR DROUGHT-ADAPTED SOIL MICROBIAL COMMUNITIES CAN PROMOTE SEEDLING SURVIVAL AND DROUGHT STRESS TOLERANCE. MYCORRHIZAL FUNCTIONAL TRAITS MAY HELP


MEDIATE PLANT STRESS. Article  CAS  Google Scholar  * Pellitier, P. T., Ibáñez, I., Zak, D. R., Argiroff, W. A. & Acharya, K. Ectomycorrhizal access to organic nitrogen mediates CO2


fertilization response in a dominant temperate tree. _Nat. Commun._ 12, 5403 (2021). Article  CAS  Google Scholar  * Pérez-Valera, E., Verdú, M., Navarro-Cano, J. A. & Goberna, M. Soil


microbiome drives the recovery of ecosystem functions after fire. _Soil Biol. Biochem._ 149, 107948 (2020). Article  Google Scholar  * Filialuna, O. & Cripps, C. Evidence that


pyrophilous fungi aggregate soil after forest fire. _For. Ecol. Manag._ 498, 119579 (2021). Article  Google Scholar  * Liu, X. et al. Responses of soil labile organic carbon to a simulated


hurricane disturbance in a tropical wet forest. _Forests_ 9, 420 (2018). Article  Google Scholar  * Venturini, A. M. et al. Increased soil moisture intensifies the impacts of


forest-to-pasture conversion on methane emissions and methane-cycling communities in the Eastern Amazon. _Environ. Res._ 212, 113139 (2022). Article  CAS  Google Scholar  * García-Palacios,


P. et al. Evidence for large microbial-mediated losses of soil carbon under anthropogenic warming. _Nat. Rev. Earth Environ._ 2, 507–517 (2021). Article  Google Scholar  * Shade, A. et al.


Fundamentals of microbial community resistance and resilience. _Front. Microbiol._ 3, 417 (2012). Article  Google Scholar  * Kearns, P. J. & Shade, A. Trait-based patterns of microbial


dynamics in dormancy potential and heterotrophic strategy: case studies of resource-based and post-press succession. _ISME J._ 12, 2575–2581 (2018). Article  CAS  Google Scholar  * Jansson,


J. K. & Hofmockel, K. S. Soil microbiomes and climate change. _Nat. Rev. Microbiol._ 18, 35–46 (2020). Article  CAS  Google Scholar  * Baldrian, P., López-Mondéjar, R. & Kohout, P.


Forest microbiome and global change. _Nat. Rev. Microbiol._ 21, 487–501 (2023). * Steidinger, B. S. et al. Climatic controls of decomposition drive the global biogeography of forest-tree


symbioses. _Nature_ 569, 404–408 (2019). Article  CAS  Google Scholar  * Bui, A. et al. Soil fungal community composition and functional similarity shift across distinct climatic conditions.


_FEMS Microbiol. Ecol._ 96, fiaa193 (2020). * Bahram, M. et al. Structure and function of the global topsoil microbiome. _Nature_ 560, 233–237 (2018). Article  CAS  Google Scholar  *


Willing, C. E., Pierroz, G., Coleman‐Derr, D. & Dawson, T. E. The generalizability of water-deficit on bacterial community composition; site-specific water-availability predicts the


bacterial community associated with coast redwood roots. _Mol. Ecol._ 29, 4721–4734 (2020). Article  CAS  Google Scholar  * Cavicchioli, R. et al. Scientists’ warning to humanity:


microorganisms and climate change. _Nat. Rev. Microbiol._ 17, 569–586 (2019). Article  CAS  Google Scholar  * Rudgers, J. A. et al. Climate disruption of plant–microbe interactions. _Annu.


Rev. Ecol. Evol. Syst_. 51, 561–586 (2020). * Lladó, S., López-Mondéjar, R. & Baldrian, P. Forest soil bacteria: diversity, involvement in ecosystem processes, and response to global


change. _Microbiol. Mol. Biol. Rev._ 81, e00063-16 (2017). Article  Google Scholar  * Wan, J. & Crowther, T. W. Uniting the scales of microbial biogeochemistry with trait-based


modelling. _Funct. Ecol._ 36, 1457–1472 (2022). THIS PERSPECTIVE IDENTIFIES CONCEPTUAL AND EMPIRICAL CHALLENGES NECESSARY TO INTEGRATE MICROBIAL TRAITS INTO MODELS OF FOREST RESPONSES TO


CLIMATE CHANGE. A FOCUS ON SCALING LAWS, AND MICROBIAL PHYSIOLOGY AS MEASURED BY NEW ’OMICS TECHNIQUES, PRESENTS OPPORTUNITIES FOR NEW CLASSES OF PREDICTIVE MODELS. Article  CAS  Google


Scholar  * Mishra, A., Singh, L. & Singh, D. Unboxing the black box—one step forward to understand the soil microbiome: a systematic review. _Microb. Ecol._ 85, 669–683 (2023). Article 


Google Scholar  * Mitchard, E. T. A. The tropical forest carbon cycle and climate change. _Nature_ 559, 527–534 (2018). Article  CAS  Google Scholar  * _Kyoto Protocol to the United Nations


Framework Convention on Climate Change_ 2303 UNTS 162 (United Nations, 1997). * De Frenne, P. et al. Forest microclimates and climate change: importance, drivers and future research agenda.


_Glob. Change Biol._ 27, 2279–2297 (2021). Article  Google Scholar  * Poorter, L., Bongers, L. & Bongers, F. Architecture of 54 moist-forest tree species: traits, trade-offs, and


functional groups. _Ecology_ 87, 1289–1301 (2006). Article  Google Scholar  * Piovesan, G. & Biondi, F. On tree longevity. _New Phytol._ 231, 1318–1337 (2021). Article  Google Scholar  *


Averill, C., Turner, B. L. & Finzi, A. C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. _Nature_ 505, 543–545 (2014). Article  CAS  Google


Scholar  * Baldrian, P. Forest microbiome: diversity, complexity and dynamics. _FEMS Microbiol. Rev._ 41, 109–130 (2017). CAS  Google Scholar  * Epihov, D. Z. et al. Legume–microbiome


interactions unlock mineral nutrients in regrowing tropical forests. _Proc. Natl Acad. Sci. USA_ 118, e2022241118 (2021). * Rodriguez, R. J., White, J. F. Jr, Arnold, A. E. & Redman, R.


S. Fungal endophytes: diversity and functional roles. _New Phytol._ 182, 314–330 (2009). Article  CAS  Google Scholar  * Fierer, N. Embracing the unknown: disentangling the complexities of


the soil microbiome. _Nat. Rev. Microbiol._ 15, 579–590 (2017). Article  CAS  Google Scholar  * Pérez-Izquierdo, L. et al. Plant intraspecific variation modulates nutrient cycling through


its below ground rhizospheric microbiome. _J. Ecol._ 107, 1594–1605 (2019). Article  Google Scholar  * Bennett, J. A. et al. Plant–soil feedbacks and mycorrhizal type influence temperate


forest population dynamics. _Science_ 355, 181–184 (2017). Article  CAS  Google Scholar  * Peay, K. G. Timing of mutualist arrival has a greater effect on _Pinus muricata_ seedling growth


than interspecific competition. _J. Ecol._ 106, 514–523 (2018). Article  Google Scholar  * Van Nuland, M. E., Ke, P.-J., Wan, J. & Peay, K. G. Mycorrhizal nutrient acquisition strategies


shape tree competition and coexistence dynamics. _J. Ecol._ 111, 564–577 (2023). Article  Google Scholar  * Lehmann, J. et al. Persistence of soil organic carbon caused by functional


complexity. _Nat. Geosci._ 13, 529–534 (2020). Article  CAS  Google Scholar  * Fernandez, C. W., Heckman, K., Kolka, R. & Kennedy, P. G. Melanin mitigates the accelerated decay of


mycorrhizal necromass with peatland warming. _Ecol. Lett._ 22, 498–505 (2019). Article  Google Scholar  * Arnold, A. E. & Engelbrecht, B. M. J. Fungal endophytes nearly double minimum


leaf conductance in seedlings of a neotropical tree species. _J. Trop. Ecol._ 23, 369–372 (2007). Article  Google Scholar  * Moyes, A. B. et al. Evidence for foliar endophytic nitrogen


fixation in a widely distributed subalpine conifer. _New Phytol._ 210, 657–668 (2016). Article  CAS  Google Scholar  * Zheng, M. et al. Effects of human disturbance activities and


environmental change factors on terrestrial nitrogen fixation. _Glob. Change Biol._ 26, 6203–6217 (2020). Article  Google Scholar  * Williams, S. E., Shoo, L. P., Isaac, J. L., Hoffmann, A.


A. & Langham, G. Towards an integrated framework for assessing the vulnerability of species to climate change. _PLoS Biol._ 6, e325 (2008). THIS PAPER DEVELOPS A VULNERABILITY ASSESSMENT


FRAMEWORK FOR SPECIES IN A CLIMATE CHANGE CONTEXT. IT INTEGRATES BIOTIC AND ABIOTIC FACTORS THAT HELP TO DETERMINE SPECIES’ VULNERABILITY, BROADLY DEFINED. Article  Google Scholar  * Malik,


A. A. et al. Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. _ISME J._ 14, 1–9 (2020). THIS PAPER UPDATES SOME OF THE TRAIT-BASED


FRAMEWORKS ORIGINALLY DEVELOPED FOR PLANTS AND APPLIES THEM TO MICROBES THAT INFLUENCE SOIL CARBON CYCLING. CLUSTERING MICROBIAL TRAITS CAN HELP PROMOTE ACCURATE PREDICTIONS OF


BIOGEOCHEMICAL FLUXES UNDER CLIMATE CHANGE. Article  CAS  Google Scholar  * Bender, E. A., Case, T. J. & Gilpin, M. E. Perturbation experiments in community ecology: theory and practice.


_Ecology_ 65, 1–13 (1984). Article  Google Scholar  * Allison, S. D. & Martiny, J. B. H. Resistance, resilience, and redundancy in microbial communities. _Proc. Natl Acad. Sci. USA_


105, 11512–11519 (2008). Article  CAS  Google Scholar  * Whitman, T. et al. Soil bacterial and fungal response to wildfires in the Canadian boreal forest across a burn severity gradient.


_Soil Biol. Biochem._ 138, 107571 (2019). Article  CAS  Google Scholar  * Pulido-Chavez, M. F., Alvarado, E. C., DeLuca, T. H., Edmonds, R. L. & Glassman, S. I. High-severity wildfire


reduces richness and alters composition of ectomycorrhizal fungi in low-severity adapted ponderosa pine forests. _For. Ecol. Manag._ 485, 118923 (2021). Article  Google Scholar  * Scheffer,


M., Carpenter, S., Foley, J. A., Folke, C. & Walker, B. Catastrophic shifts in ecosystems. _Nature_ 413, 591–596 (2001). Article  CAS  Google Scholar  * Smith, S. E. & Read, D. J.


_Mycorrhizal Symbiosis_ (Academic, 2010). * Schimel, J. P. Life in dry soils: effects of drought on soil microbial communities and processes. _Annu. Rev. Ecol. Evol. Syst._ 49, 409–432


(2018). Article  Google Scholar  * Martiny, J. B. H. et al. Investigating the eco‐evolutionary response of microbiomes to environmental change. _Ecol. Lett._ 26, S81–S90 (2023). Article 


Google Scholar  * Zhou, J. et al. Temperature mediates continental-scale diversity of microbes in forest soils. _Nat. Commun._ 7, 12083 (2016). Article  CAS  Google Scholar  * Iversen, C.


M., Ledford, J. & Norby, R. J. CO2 enrichment increases carbon and nitrogen input from fine roots in a deciduous forest. _New Phytol._ 179, 837–847 (2008). Article  CAS  Google Scholar 


* Norby, R. J. & Zak, D. R. Ecological lessons from free-air CO2 enrichment (FACE) experiments. _Annu. Rev. Ecol. Evol. Syst._ 42, 181–203 (2011). * Heinemeyer, A., Ineson, P., Ostle, N.


& Fitter, A. H. Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature. _New


Phytol._ 171, 159–170 (2006). Article  CAS  Google Scholar  * Olsrud, M., Carlsson, B. Å., Svensson, B. M., Michelsen, A. & Melillo, J. M. Responses of fungal root colonization, plant


cover and leaf nutrients to long-term exposure to elevated atmospheric CO2 and warming in a subarctic birch forest understory. _Glob. Change Biol._ 16, 1820–1829 (2010). Article  Google


Scholar  * Ikeda, K. et al. Snowfall and snowpack in the Western U.S. as captured by convection permitting climate simulations: current climate and pseudo global warming future climate.


_Clim. Dyn._ 57, 2191–2215 (2021). Article  Google Scholar  * Millar, C. I. & Stephenson, N. L. Temperate forest health in an era of emerging megadisturbance. _Science_ 349, 823–826


(2015). Article  CAS  Google Scholar  * König, S. et al. Spatiotemporal disturbance characteristics determine functional stability and collapse risk of simulated microbial ecosystems. _Sci.


Rep._ 8, 9488 (2018). Article  Google Scholar  * Barnes, I. et al. New _Ceratocystis_ species associated with rapid death of _Metrosideros polymorpha_ in Hawai’i. _Persoonia_ 40, 154–181


(2018). Article  CAS  Google Scholar  * Reich, P. B. et al. Even modest climate change may lead to major transitions in boreal forests. _Nature_ 608, 540–545 (2022). Article  CAS  Google


Scholar  * Livne-Luzon, S. et al. High resilience of the mycorrhizal community to prescribed seasonal burnings in eastern Mediterranean woodlands. _Mycorrhiza_ 31, 203–216 (2021). THIS STUDY


INVESTIGATES HOW THE TIMING OF FIRE CAN HAVE DIFFERING IMPACTS ON FUNGAL COMMUNITIES, PROBABLY RELATED TO PERIODS OF DORMANCY VERSUS ACTIVE GROWTH. Article  Google Scholar  * Wang, J. et


al. Changing lengths of the four seasons by global warming. _Geophys. Res. Lett._ 48, e2020GL091753 (2021). Article  Google Scholar  * Gallinat, A. S., Primack, R. B. & Wagner, D. L.


Autumn, the neglected season in climate change research. _Trends Ecol. Evol._ 30, 169–176 (2015). Article  Google Scholar  * Gange, A. C., Gange, E. G., Sparks, T. H. & Boddy, L. Rapid


and recent changes in fungal fruiting patterns. _Science_ 316, 71 (2007). Article  CAS  Google Scholar  * Kauserud, H. et al. Warming-induced shift in European mushroom fruiting phenology.


_Proc. Natl Acad. Sci. USA_ 109, 14488–14493 (2012). Article  CAS  Google Scholar  * Anderson, M. K. & Lake, F. K. California Indian ethnomycology and associated forest management. _J.


Ethnobiol._ 33, 33–85 (2013). Article  Google Scholar  * _Karuk Climate Adaptation Plan_ (Karuk Tribe, 2019). * Hernandez, J., Meisner, J., Jacobs, L. A. & Rabinowitz, P. M. Re-centering


Indigenous Knowledge in climate change discourse. _PLoS Clim._ 1, e0000032 (2022). Article  Google Scholar  * Gervers, K. A., Thomas, D. C., Roy, B. A., Spatafora, J. W. & Busby, P. E.


Crown closure affects endophytic leaf mycobiome compositional dynamics over time in _Pseudotsuga menziesii_ var. _menziesii_. _Fungal Ecol._ 57/58, 101155 (2022). Article  Google Scholar  *


Gora, E. M., Lucas, J. M. & Yanoviak, S. P. Microbial composition and wood decomposition rates vary with microclimate from the ground to the canopy in a tropical forest. _Ecosystems_ 22,


1206–1219 (2019). Article  CAS  Google Scholar  * Drake, J. E. et al. Trees tolerate an extreme heatwave via sustained transpirational cooling and increased leaf thermal tolerance. _Glob.


Change Biol._ 24, 2390–2402 (2018). Article  Google Scholar  * Bowman, E. A. & Arnold, A. E. Distributions of ectomycorrhizal and foliar endophytic fungal communities associated with


_Pinus ponderosa_ along a spatially constrained elevation gradient. _Am. J. Bot._ 105, 687–699 (2018). Article  Google Scholar  * Nelson, A. R. et al. Wildfire-dependent changes in soil


microbiome diversity and function. _Nat. Microbiol._ 7, 1419–1430 (2022). Article  CAS  Google Scholar  * Krah, F.-S. et al. Independent effects of host and environment on the diversity of


wood-inhabiting fungi. _J. Ecol._ 106, 1428–1442 (2018). Article  Google Scholar  * Van Nuland, M. E. et al. Warming and disturbance alter soil microbiome diversity and function in a


northern forest ecotone. _FEMS Microbiol. Ecol._ 96, fiaa108 (2020). Article  Google Scholar  * Giuggiola, A. et al. Competition for water in a xeric forest ecosystem—effects of understory


removal on soil micro-climate, growth and physiology of dominant Scots pine trees. _For. Ecol. Manag._ 409, 241–249 (2018). Article  Google Scholar  * Long, J. W., Lake, F. K. & Goode,


R. W. The importance of Indigenous cultural burning in forested regions of the Pacific West, USA. _For. Ecol. Manag._ 500, 119597 (2021). Article  Google Scholar  * Vandenkoornhuyse, P.,


Quaiser, A., Duhamel, M., Le Van, A. & Dufresne, A. The importance of the microbiome of the plant holobiont. _New Phytol._ 206, 1196–1206 (2015). Article  Google Scholar  * Dawson, T.


P., Jackson, S. T., House, J. I., Prentice, I. C. & Mace, G. M. Beyond predictions: biodiversity conservation in a changing climate. _Science_ 332, 53–58 (2011). Article  CAS  Google


Scholar  * Talbot, J. M. et al. Endemism and functional convergence across the North American soil mycobiome. _Proc. Natl Acad. Sci. USA_ 111, 6341–6346 (2014). Article  CAS  Google Scholar


  * Shu, W.-S. & Huang, L.-N. Microbial diversity in extreme environments. _Nat. Rev. Microbiol._ 20, 219–235 (2022). Article  CAS  Google Scholar  * Moeller, H. V., Dickie, I. A.,


Peltzer, D. A. & Fukami, T. Mycorrhizal co-invasion and novel interactions depend on neighborhood context. _Ecology_ 96, 2336–2347 (2015). Article  Google Scholar  * U’Ren, J. M. et al.


Host availability drives distributions of fungal endophytes in the imperilled boreal realm. _Nat. Ecol. Evol._ 3, 1430–1437 (2019). FOLIAR ENDOPHYTES DISPLAY HIGH FIDELITY TO THEIR PLANT


HOSTS ACROSS THE BOREAL FOREST. THIS STUDY SUGGESTS THAT CLIMATIC CHANGE MAY EXTIRPATE AVAILABLE HOSTS AND REDUCE THE DIVERSITY OF ENDOPHYTIC FUNGI. Article  Google Scholar  * Peay, K. G.,


Schubert, M. G., Nguyen, N. H. & Bruns, T. D. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. _Mol. Ecol._ 21, 4122–4136 (2012).


Article  Google Scholar  * Branco, S. et al. Genetic isolation between two recently diverged populations of a symbiotic fungus. _Mol. Ecol._ 24, 2747–2758 (2015). Article  CAS  Google


Scholar  * Evans, S. E., Allison, S. D. & Hawkes, C. V. Microbes, memory and moisture: predicting microbial moisture responses and their impact on carbon cycling. _Funct. Ecol._ 36,


1430–1441 (2022). Article  Google Scholar  * Dove, N. C., Taş, N. & Hart, S. C. Ecological and genomic responses of soil microbiomes to high-severity wildfire: linking community assembly


to functional potential. _ISME J._ 16, 1853–1863 (2022). USING A FIRE CHRONOSEQUENCE, THIS STUDY IDENTIFIED THE SUCCESSIONAL DYNAMICS OF BACTERIAL TRAITS AFTER WILDFIRE. METAGENOMIC


COMMUNITY PROFILING REVEALED THE PROLIFERATION OF GENES INVOLVED IN STRESS TOLERANCE AND THAT MICROBIAL COMMUNITIES DO NOT RECOVER ‘BASELINE’ FUNCTION FOR DECADES. Article  CAS  Google


Scholar  * Hawkes, C. V. & Keitt, T. H. Resilience vs. historical contingency in microbial responses to environmental change. _Ecol. Lett._ 18, 612–625 (2015). Article  Google Scholar  *


Nottingham, A. T., Meir, P., Velasquez, E. & Turner, B. L. Soil carbon loss by experimental warming in a tropical forest. _Nature_ 584, 234–237 (2020). Article  CAS  Google Scholar  *


Wang, C. et al. The temperature sensitivity of soil: microbial biodiversity, growth, and carbon mineralization. _ISME J._ 15, 2738–2747 (2021). Article  CAS  Google Scholar  * Meisner, A.,


Jacquiod, S., Snoek, B. L., ten Hooven, F. C. & van der Putten, W. H. Drought legacy effects on the composition of soil fungal and prokaryote communities. _Front. Microbiol._ 9, 294


(2018). Article  Google Scholar  * Bouskill, N. J. et al. Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. _ISME J._ 7,


384–394 (2013). Article  CAS  Google Scholar  * Fischer, M. S. et al. Pyrolyzed substrates induce aromatic compound metabolism in the post-fire fungus, _Pyronema domesticum_. _Front.


Microbiol._ 12, 3085 (2021). USING A MODEL ‘PYROPHILOUS’ FUNGAL SPECIES, THE AUTHORS DEMONSTRATE THAT _PYRONEMA_ IS NOT ONLY PREVALENT AFTER FIRE, BUT ACTUALLY ADAPTED TO BE ABLE TO


METABOLIZE PYROLYSED ORGANIC MATTER, A VERY RECALCITRANT FORM OF CARBON IN POST-FIRE SYSTEMS. Article  Google Scholar  * Smith, G. R., Edy, L. C. & Peay, K. G. Contrasting fungal


responses to wildfire across different ecosystem types. _Mol. Ecol._ 30, 844–854 (2021). Article  Google Scholar  * Bowd, E. J. et al. Direct and indirect effects of fire on microbial


communities in a pyrodiverse dry-sclerophyll forest. _J. Ecol._ 110, 1687–1703 (2022). Article  CAS  Google Scholar  * Enright, D. J., Frangioso, K. M., Isobe, K., Rizzo, D. M. &


Glassman, S. I. Mega-fire in redwood tanoak forest reduces bacterial and fungal richness and selects for pyrophilous taxa that are phylogenetically conserved. _Mol. Ecol._ 31, 2475–2493


(2022). * Bruns, T. D., Hale, M. L. & Nguyen, N. H. _Rhizopogon olivaceotinctus_ increases its inoculum potential in heated soil independent of competitive release from other


ectomycorrhizal fungi. _Mycologia_ 111, 936–941 (2019). Article  CAS  Google Scholar  * Kennedy, P. G., Higgins, L. M., Rogers, R. H. & Weber, M. G. Colonization–competition tradeoffs as


a mechanism driving successional dynamics in ectomycorrhizal fungal communities. _PLoS ONE_ 6, e25126 (2011). Article  CAS  Google Scholar  * Bardgett, R. D. & Caruso, T. Soil microbial


community responses to climate extremes: resistance, resilience and transitions to alternative states. _Phil. Trans. R. Soc. B_ 375, 20190112 (2020). Article  CAS  Google Scholar  * Miller,


J. E. D., Root, H. T. & Safford, H. D. Altered fire regimes cause long-term lichen diversity losses. _Glob. Change Biol._ 24, 4909–4918 (2018). Article  Google Scholar  * Metz, M. R.,


Varner, J. M., Frangioso, K. M., Meentemeyer, R. K. & Rizzo, D. M. Unexpected redwood mortality from synergies between wildfire and an emerging infectious disease. _Ecology_ 94,


2152–2159 (2013). Article  Google Scholar  * Robinson, J. M. et al. Rapid laboratory measurement of the temperature dependence of soil respiration and application to changes in three diverse


soils through the year. _Biogeochemistry_ 133, 101–112 (2017). Article  CAS  Google Scholar  * Bradford, M. A. et al. Cross-biome patterns in soil microbial respiration predictable from


evolutionary theory on thermal adaptation. _Nat. Ecol. Evol._ 3, 223–231 (2019). Article  Google Scholar  * Malik, A. A. & Bouskill, N. J. Drought impacts on microbial trait distribution


and feedback to soil carbon cycling. _Funct. Ecol._ 36, 1442–1456 (2022). Article  CAS  Google Scholar  * Chomicki, G., Werner, G. D. A., West, S. A. & Kiers, E. T. Compartmentalization


drives the evolution of symbiotic cooperation. _Phil. Trans. R. Soc. B_ 375, 20190602 (2020). Article  CAS  Google Scholar  * Willing, C. E. et al. Keep your friends close: host


compartmentalisation of microbial communities facilitates decoupling from effects of habitat fragmentation. _Ecol. Lett._ 24, 2674–2686 (2021). Article  Google Scholar  * Maynard, D. S. et


al. Consistent trade-offs in fungal trait expression across broad spatial scales. _Nat. Microbiol._ 4, 846–853 (2019). Article  CAS  Google Scholar  * Pounds, J. A. & Puschendorf, R.


Clouded futures. _Nature_ 427, 107–109 (2004). Article  CAS  Google Scholar  * Khan, Z. et al. Growth enhancement and drought tolerance of hybrid poplar upon inoculation with endophyte


consortia. _Curr. Plant Biol._ 6, 38–47 (2016). Article  Google Scholar  * Nimmo, D. G., Mac Nally, R., Cunningham, S. C., Haslem, A. & Bennett, A. F. Vive la résistance: reviving


resistance for 21st century conservation. _Trends Ecol. Evol._ 30, 516–523 (2015). Article  CAS  Google Scholar  * Cregger, M. A. et al. The _Populus_ holobiont: dissecting the effects of


plant niches and genotype on the microbiome. _Microbiome_ 6, 31 (2018). Article  CAS  Google Scholar  * Rigling, D. & Prospero, S. _Cryphonectria parasitica_, the causal agent of


chestnut blight: invasion history, population biology and disease control. _Mol. Plant Pathol._ 19, 7–20 (2017). Article  Google Scholar  * Agan, A. et al. The relationship between fungal


diversity and invasibility of a foliar niche—the case of ash dieback. _J. Fungi_ 6, 150 (2020). Article  CAS  Google Scholar  * Gehring, C. A., Sthultz, C. M., Flores-Rentería, L., Whipple,


A. V. & Whitham, T. G. Tree genetics defines fungal partner communities that may confer drought tolerance. _Proc. Natl Acad. Sci. USA_ 114, 11169–11174 (2017). Article  CAS  Google


Scholar  * Lustenhouwer, N. et al. A trait-based understanding of wood decomposition by fungi. _Proc. Natl Acad. Sci. USA_ 117, 11551–11558 (2020). Article  CAS  Google Scholar  *


Alvarez-Manjarrez, J. & Garibay-Orijel, R. Resilience of soil fungal community to hurricane Patricia (category 4). _For. Ecol. Manag._ 498, 119550 (2021). Article  Google Scholar  *


Erlandson, S. R. et al. Transcriptional acclimation and spatial differentiation characterize drought response by the ectomycorrhizal fungus _Suillus pungens_. _New Phytol._ 243, 1910–1913


(2021). THIS STUDY USED TRANSCRIPTOMICS TO IDENTIFY THAT FUNGAL GENES ASSOCIATED WITH STRESS TOLERANCE ARE UPREGULATED UNDER EXPERIMENTAL DROUGHT CONDITIONS AND THAT GENES ASSOCIATED WITH


RESOURCE ACQUISITION ARE DOWNREGULATED. Google Scholar  * Romero-Olivares, A. L., Meléndrez-Carballo, G., Lago-Lestón, A. & Treseder, K. K. Soil metatranscriptomes under long-term


experimental warming and drying: fungi allocate resources to cell metabolic maintenance rather than decay. _Front. Microbiol._ 10, 1914 (2019). Article  Google Scholar  * Lennon, J. T. &


Jones, S. E. Microbial seed banks: the ecological and evolutionary implications of dormancy. _Nat. Rev. Microbiol._ 9, 119–130 (2011). Article  CAS  Google Scholar  * Glassman, S. I.,


Levine, C. R., DiRocco, A. M., Battles, J. J. & Bruns, T. D. Ectomycorrhizal fungal spore bank recovery after a severe forest fire: some like it hot. _ISME J._ 10, 1228–1239 (2016).


Article  Google Scholar  * Gei, M. et al. Legume abundance along successional and rainfall gradients in Neotropical forests. _Nat. Ecol. Evol._ 2, 1104–1111 (2018). Article  Google Scholar 


* Kou-Giesbrecht, S. & Menge, D. Nitrogen-fixing trees could exacerbate climate change under elevated nitrogen deposition. _Nat. Commun._ 10, 1493 (2019). Article  Google Scholar  *


Mason, R. E. et al. Evidence, causes, and consequences of declining nitrogen availability in terrestrial ecosystems. _Science_ 376, eabh3767 (2022). Article  CAS  Google Scholar  *


Pellegrini, A. F. A. et al. Fire effects on the persistence of soil organic matter and long-term carbon storage. _Nat. Geosci._ 15, 5–13 (2022). Article  CAS  Google Scholar  *


Delgado-Baquerizo, M. et al. The proportion of soil-borne pathogens increases with warming at the global scale. _Nat. Clim. Change_ 10, 550–554 (2020). THIS STUDY IDENTIFIES HOW WARMING CAN


INCREASE THE ABUNDANCE OF FUNGAL PATHOGENS IN SOIL. HIGH-RESOLUTION MAPPING EFFORTS ON SOIL FUNGI CAN PROMOTE TARGETED INTERVENTIONS FOR AGRICULTURAL SYSTEMS. Article  Google Scholar  *


Pfender, W. F. & Vollmer, S. S. Freezing temperature effect on survival of _Puccinia graminis_ subsp. _graminicola_ in _Festuca arundinacea_ and _Lolium perenne_. _Plant Dis._ 83,


1058–1062 (1999). Article  CAS  Google Scholar  * Steidinger, B. S. et al. Ectomycorrhizal fungal diversity predicted to substantially decline due to climate changes in North American


Pinaceae forests. _J. Biogeogr._ 47, 772–782 (2020). Article  Google Scholar  * Yuan, Z. et al. Divergent above- and below-ground biodiversity pathways mediate disturbance impacts on


temperate forest multifunctionality. _Glob. Change Biol._ 27, 2883–2894 (2021). Article  Google Scholar  * Corrales, A., Mangan, S. A., Turner, B. L. & Dalling, J. W. An ectomycorrhizal


nitrogen economy facilitates monodominance in a neotropical forest. _Ecol. Lett._ 19, 383–392 (2016). Article  Google Scholar  * Dudenhöffer, J.-H., Luecke, N. C. & Crawford, K. M.


Changes in precipitation patterns can destabilize plant species coexistence via changes in plant–soil feedback. _Nat. Ecol. Evol._ 6, 546–554 (2022). Article  Google Scholar  * Konopka, A.,


Lindemann, S. & Fredrickson, J. Dynamics in microbial communities: unraveling mechanisms to identify principles. _ISME J._ 9, 1488–1495 (2015). Article  Google Scholar  * Gao, C. et al.


Co-occurrence networks reveal more complexity than community composition in resistance and resilience of microbial communities. _Nat. Commun._ 13, 3867 (2022). Article  CAS  Google Scholar 


* Qin, C., Pellitier, P. T., Van Nuland, M. E., Peay, K. G. & Zhu, K. Niche modelling predicts that soil fungi occupy a precarious climate in boreal forests. _Glob. Ecol. Biogeogr._ 32,


1127–1139 (2023). Article  Google Scholar  * Walkup, J. et al. The predictive power of phylogeny on growth rates in soil bacterial communities. _ISME Commun._ 3, 73 (2023). Article  Google


Scholar  * Salipante, S. J. et al. Performance comparison of Illumina and Ion Torrent next-generation sequencing platforms for 16S rRNA-based bacterial community profiling. _Appl. Environ.


Microbiol._ 80, 7583–7591 (2014). Article  Google Scholar  * Bruns, T. D. & Taylor, J. W. Comment on ‘Global assessment of arbuscular mycorrhizal fungus diversity reveals very low


endemism’. _Science_ 351, 826 (2016). Article  CAS  Google Scholar  * Johnson, J. S. et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. _Nat.


Commun._ 10, 5029 (2019). Article  Google Scholar  * Tedersoo, L. et al. Best practices in metabarcoding of fungi: from experimental design to results. _Mol. Ecol._ 31, 2769–2795 (2022).


Article  Google Scholar  * Philippot, L., Griffiths, B. S. & Langenheder, S. Microbial community resilience across ecosystems and multiple disturbances. _Microbiol. Mol. Biol. Rev._ 85,


00026-20 (2021). * Nevison, C., Hess, P., Goodale, C., Zhu, Q. & Vira, J. Nitrification, denitrification, and competition for soil N: evaluation of two Earth system models against


observations. _Ecol. Appl._ 32, e2528 (2022). * Bradford, M. A. et al. Quantifying microbial control of soil organic matter dynamics at macrosystem scales. _Biogeochemistry_ 156, 19–40


(2021). Article  Google Scholar  * Baskaran, P. et al. Modelling the influence of ectomycorrhizal decomposition on plant nutrition and soil carbon sequestration in boreal forest ecosystems.


_New Phytol._ 213, 1452–1465 (2017). Article  CAS  Google Scholar  * Ovaskainen, O. & Abrego, N. _Joint Species Distribution Modelling: with Applications in R (Ecology, Biodiversity and


Conservation)_ (Cambridge Univ. Press, 2020). * Abrego, N., Dunson, D., Halme, P., Salcedo, I. & Ovaskainen, O. Wood-inhabiting fungi with tight associations with other species have


declined as a response to forest management. _Oikos_ 126, 269–275 (2017). Download references ACKNOWLEDGEMENTS We thank J. Dudney, R. Cruz de Hoyos, A. Guzman and R. Jackson for helpful


feedback on this manuscript, and A. Venturini for help with translating our abstract into Portuguese for our readership. Additionally, we would like to thank D. Martinez for her input on


potential synergies between Indigenous and Western science in the context of this article. AUTHOR INFORMATION Author notes * These authors contributed equally: C. E. Willing, P. T.


Pellitier. AUTHORS AND AFFILIATIONS * Department of Biology, Stanford University, Stanford, CA, USA C. E. Willing, P. T. Pellitier, M. E. Van Nuland, J. Alvarez-Manjarrez, L. Berrios, K. N.


Chin, L. M. Villa, J. J. Yeam & K. G. Peay * University of Washington, School of Environmental and Forest Sciences, Seattle, WA, USA C. E. Willing * Society for the Protection of


Underground Networks (SPUN), Dover, DE, USA M. E. Van Nuland * Micología Integral, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico J. Alvarez-Manjarrez *


Karuk Tribe, Happy Camp, CA, USA S. D. Bourque & W. Tripp * Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ, USA V. O. Leshyk Authors * C. E. Willing


View author publications You can also search for this author inPubMed Google Scholar * P. T. Pellitier View author publications You can also search for this author inPubMed Google Scholar *


M. E. Van Nuland View author publications You can also search for this author inPubMed Google Scholar * J. Alvarez-Manjarrez View author publications You can also search for this author


inPubMed Google Scholar * L. Berrios View author publications You can also search for this author inPubMed Google Scholar * K. N. Chin View author publications You can also search for this


author inPubMed Google Scholar * L. M. Villa View author publications You can also search for this author inPubMed Google Scholar * J. J. Yeam View author publications You can also search


for this author inPubMed Google Scholar * S. D. Bourque View author publications You can also search for this author inPubMed Google Scholar * W. Tripp View author publications You can also


search for this author inPubMed Google Scholar * V. O. Leshyk View author publications You can also search for this author inPubMed Google Scholar * K. G. Peay View author publications You


can also search for this author inPubMed Google Scholar CONTRIBUTIONS C.E.W., P.T.P. and K.G.P. jointly conceived of the paper. C.E.W. and P.T.P. jointly wrote the paper with input from all


co-authors. C.E.W. and P.T.P. share first authorship. C.E.W., L.M.V., S.D.B. and W.T. conceived of and wrote Box 1. V.O.L. designed Fig. 1 with input from C.E.W. and P.T.P. C.E.W. designed


Fig. 2 with input from M.E.V.N. and P.T.P. Figure 3 was designed by M.E.V.N., C.E.W. and J.A.-M. P.T.P. wrote Box 2 with input from call co-authors. Figure 4 was designed by C.E.W. and


P.T.P. All authors have read and approved the final version of the paper. CORRESPONDING AUTHORS Correspondence to C. E. Willing or P. T. Pellitier. ETHICS DECLARATIONS COMPETING INTERESTS


The authors declare no competing interests. PEER REVIEW PEER REVIEW INFORMATION _Nature Climate Change_ thanks Eleonora Egidi, Kevin Newsham and the other, anonymous, reviewer(s) for their


contribution to the peer review of this work. ADDITIONAL INFORMATION PUBLISHER’S NOTE Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional


affiliations. SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION Spanish and Portuguese translations of the abstract. RIGHTS AND PERMISSIONS Springer Nature or its licensor (e.g. a society


or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version


of this article is solely governed by the terms of such publishing agreement and applicable law. Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Willing, C.E., Pellitier, P.T.,


Van Nuland, M.E. _et al._ A risk assessment framework for the future of forest microbiomes in a changing climate. _Nat. Clim. Chang._ 14, 448–461 (2024).


https://doi.org/10.1038/s41558-024-02000-7 Download citation * Received: 15 September 2022 * Accepted: 25 March 2024 * Published: 29 April 2024 * Issue Date: May 2024 * DOI:


https://doi.org/10.1038/s41558-024-02000-7 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not


currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative


Trending News

Evolution of genes and genomes on the drosophila phylogeny

ABSTRACT Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and se...

Attack of the genomes | Nature

How many genome sequences do you need to characterize a model organism? For _Drosophila,_ Heidi Ledford finds, a dozen i...

P53 regulates maternal reproduction through lif

ABSTRACT Extensive studies have shown that p53 is important in tumour prevention1. However, little is known about its no...

Door opened to nuclear portals

The gate keepers of a cell?s nucleus are mapped out. Access through your institution Buy or subscribe This is a preview ...

Us deliberates on embryonic stem cells, cloning

Access through your institution Buy or subscribe In a speech televised in August from his Texas home, US President Georg...

Latests News

A risk assessment framework for the future of forest microbiomes in a changing climate

ABSTRACT Microbes inhabiting the above- and belowground tissues of forest trees and soils play a critical role in the re...

Mindhunter: who is serial killer jerry brudos? Who plays him?

Mindhunter is based on the true-crime book Mindhunter: Inside the FBI’s Elite Serial Crime Unit written by John E. Dougl...

Should a professor lose her job for tweeting horrible things?

If historians of the future want to grasp the poisonous character of public debate in the first two years of the Trump a...

The principles of quantum mechanics

ABSTRACT THIS is the second edition of the celebrated book that appeared five years ago, which has been perhaps the most...

Page Not Found

很抱歉,你所访问的页面已不存在了。 如有疑问,请电邮[email protected] 你仍然可选择浏览首页或以下栏目内容 : 新闻 生活 娱乐 财经 体育 视频 播客 新报业媒体有限公司版权所有(公司登记号:202120748H)...

Top