Warming drives a ‘hummockification’ of microbial communities associated with decomposing mycorrhizal fungal necromass in peatlands

Maillard, François; Fernandez, Christopher W.; Mundra, Sunil; Heckman, Katherine A.; Kolka, Randall K.; Kauserud, Håvard; Kennedy, Peter G.

doi:10.1111/nph.17755

Warming drives a ‘hummockification’ of microbial communities associated with decomposing mycorrhizal fungal necromass in peatlands

Journal Article · Fri Sep 24 00:00:00 EDT 2021 · New Phytologist

DOI:https://doi.org/10.1111/nph.17755· OSTI ID:1982918

^[1]; ^[2]; ^[3]; ^[4]; Kolka, Randall K. ^[5]; Kauserud, Håvard ^[6]; Kennedy, Peter G. ^[1]

Univ. of Minnesota, St. Paul, MN (United States)
Univ. of Minnesota, St. Paul, MN (United States); Michigan State Univ., East Lansing, MI (United States)
Univ. of Oslo (Norway); United Arab Emirates Univ., Al Ain (United Arab Emirates)
USDA Forest Service, Houghton, MI (United States). Northern Research Station
USDA Forest Service, Grand Rapids, MN (United States). Northern Research Station
Univ. of Oslo (Norway)

Dead fungal mycelium (necromass) represents a critical component of soil carbon (C) and nutrient cycles. Assessing how the microbial communities associated with decomposing fungal necromass change as global temperatures rise will help in determining how these belowground organic matter inputs contribute to ecosystem responses. Here, in this study, we characterized the structure of bacterial and fungal communities associated with multiple types of decaying mycorrhizal fungal necromass incubated within mesh bags across a 9°C whole ecosystem temperature enhancement in a boreal peatland. We found major taxonomic and functional shifts in the microbial communities present on decaying mycorrhizal fungal necromass in response to warming. These changes were most pronounced in hollow microsites, which showed convergence towards the necromass-associated microbial communities present in unwarmed hummocks. We also observed a high colonization of ericoid mycorrhizal fungal necromass by fungi from the same genera as the necromass. These results indicate that microbial communities associated with mycorrhizal fungal necromass decomposition are likely to change significantly with future climate warming, which may have strong impacts on soil biogeochemical cycles in peatlands. Additionally, the high enrichment of congeneric fungal decomposers on ericoid mycorrhizal necromass may help to explain the increase in ericoid shrub dominance in warming peatlands.

View Accepted Manuscript (DOE)

Research Organization:: US Department of Energy (USDOE), Washington, DC (United States). Office of Science, Biological and Environmental Research (BER)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI ID:: 1982918

Alternate ID(s):: OSTI ID: 1826804

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 6 Vol. 234; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (65)

The stoichiometry of carbon and nutrients in peat formation: C and nutrients in peat Wang, Meng; Moore, Tim R.; Talbot, Julie Global Biogeochemical Cycles, Vol. 29, Issue 2 https://doi.org/10.1002/2014GB005000	journal	February 2015
Rapid loss of an ecosystem engineer: Sphagnum decline in an experimentally warmed bog Norby, Richard J.; Childs, Joanne; Hanson, Paul J. Ecology and Evolution, Vol. 9, Issue 22 https://doi.org/10.1002/ece3.5722	journal	October 2019
Decomposition in Boreal Peatlands Moore, Tim; Basiliko, Nate Boreal Peatland Ecosystems https://doi.org/10.1007/978-3-540-31913-9_7	book	January 2006
Litter Decomposition in Temperate Peatland Ecosystems: The Effect of Substrate and Site Moore, Tim R.; Bubier, Jill L.; Bledzki, Leszek Ecosystems, Vol. 10, Issue 6 https://doi.org/10.1007/s10021-007-9064-5	journal	July 2007
Effects of water level and temperature on performance of four Sphagnum mosses Robroek, Bjorn J. M.; Limpens, Juul; Breeuwer, Angela Plant Ecology, Vol. 190, Issue 1 https://doi.org/10.1007/s11258-006-9193-5	journal	July 2006
The Impact of Experimental Temperature and Water Level Manipulation on Carbon Dioxide Release in a Poor Fen in Northern Poland Samson, Mateusz; Słowińska, Sandra; Słowiński, Michał Wetlands, Vol. 38, Issue 3 https://doi.org/10.1007/s13157-018-0999-4	journal	January 2018
Chitin as a nitrogen source for mycorrhizal fungi Leake, J. R.; Read, D. J. Mycological Research, Vol. 94, Issue 7 https://doi.org/10.1016/S0953-7562(09)81318-X	journal	October 1990
Decreased summer water table depth affects peatland vegetation Breeuwer, Angela; Robroek, Bjorn J. M.; Limpens, Juul Basic and Applied Ecology, Vol. 10, Issue 4 https://doi.org/10.1016/j.baae.2008.05.005	journal	July 2009
An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology Nilsson, R. Henrik; Veldre, Vilmar; Hartmann, Martin Fungal Ecology, Vol. 3, Issue 4 https://doi.org/10.1016/j.funeco.2010.05.002	journal	November 2010
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild Nguyen, Nhu H.; Song, Zewei; Bates, Scott T. Fungal Ecology, Vol. 20 https://doi.org/10.1016/j.funeco.2015.06.006	journal	April 2016
Vertical distribution of fungi in hollows and hummocks of boreal peatlands Asemaninejad, Asma; Thorn, R. Greg; Lindo, Zoë Fungal Ecology, Vol. 27 https://doi.org/10.1016/j.funeco.2017.02.002	journal	June 2017
Rapid changes in the chemical composition of degrading ectomycorrhizal fungal necromass Ryan, Maeve E.; Schreiner, Kathryn M.; Swenson, Jenna T. Fungal Ecology, Vol. 45 https://doi.org/10.1016/j.funeco.2020.100922	journal	June 2020
The root-symbiotic Rhizoscyphus ericae aggregate and Hyaloscypha (Leotiomycetes) are congeneric: Phylogenetic and experimental evidence Fehrer, J.; Réblová, M.; Bambasová, V. Studies in Mycology, Vol. 92 https://doi.org/10.1016/j.simyco.2018.10.004	journal	March 2019
Rapid incorporation of carbon from ectomycorrhizal mycelial necromass into soil fungal communities Drigo, B.; Anderson, I. C.; Kannangara, G. S. K. Soil Biology and Biochemistry, Vol. 49 https://doi.org/10.1016/j.soilbio.2012.02.003	journal	June 2012
Microbial communities in natural and disturbed peatlands: A review Andersen, R.; Chapman, S. J.; Artz, R. R. E. Soil Biology and Biochemistry, Vol. 57 https://doi.org/10.1016/j.soilbio.2012.10.003	journal	February 2013
Initial melanin and nitrogen concentrations control the decomposition of ectomycorrhizal fungal litter Fernandez, Christopher W.; Koide, Roger T. Soil Biology and Biochemistry, Vol. 77 https://doi.org/10.1016/j.soilbio.2014.06.026	journal	October 2014
The decomposition of ectomycorrhizal fungal necromass Fernandez, Christopher W.; Langley, J. Adam; Chapman, Samantha Soil Biology and Biochemistry, Vol. 93 https://doi.org/10.1016/j.soilbio.2015.10.017	journal	February 2016
Nutrient content affects the turnover of fungal biomass in forest topsoil and the composition of associated microbial communities Brabcová, Vendula; Štursová, Martina; Baldrian, Petr Soil Biology and Biochemistry, Vol. 118 https://doi.org/10.1016/j.soilbio.2017.12.012	journal	March 2018
Climate change favours specific fungal communities in boreal peatlands Asemaninejad, Asma; Thorn, R. Greg; Branfireun, Brian A. Soil Biology and Biochemistry, Vol. 120 https://doi.org/10.1016/j.soilbio.2018.01.029	journal	May 2018
Observational Evidence of Recent Change in the Northern High-Latitude Environment Serreze, M. C.; Walsh, J. E.; Chapin III, F. S. Climatic Change, Vol. 46, Issue 1/2, p. 159-207 https://doi.org/10.1023/A:1005504031923	journal	January 2000
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea McDonald, Daniel; Price, Morgan N.; Goodrich, Julia The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.139	journal	December 2011
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Biogeochemical plant–soil microbe feedback in response to climate warming in peatlands Bragazza, Luca; Parisod, Julien; Buttler, Alexandre Nature Climate Change, Vol. 3, Issue 3 https://doi.org/10.1038/nclimate1781	journal	December 2012
Geographic range predicts photosynthetic and growth response to warming in co-occurring tree species Reich, Peter B.; Sendall, Kerrie M.; Rice, Karen Nature Climate Change, Vol. 5, Issue 2 https://doi.org/10.1038/nclimate2497	journal	January 2015
Latitudinal limits to the predicted increase of the peatland carbon sink with warming Gallego-Sala, Angela V.; Charman, Dan J.; Brewer, Simon Nature Climate Change, Vol. 8, Issue 10 https://doi.org/10.1038/s41558-018-0271-1	journal	September 2018
Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts Vrålstad, Trude; Schumacher, Trond; Taylor, Andy F. S. New Phytologist, Vol. 153, Issue 1 https://doi.org/10.1046/j.0028-646X.2001.00290.x	journal	January 2002
The biology of mycorrhiza in the Ericaceae. XX. Plant and mycorrhizal necromass as nitrogenous substrates for the ericoid mycorrhizal fungus Hymenoscyphus ericae and its host Kerley, Simon J.; Read, David J. New Phytologist, Vol. 139, Issue 2 https://doi.org/10.1046/j.1469-8137.1998.00189.x	journal	June 1998
Changes in temperature alter the relationship between biodiversity and ecosystem functioning García, Francisca C.; Bestion, Elvire; Warfield, Ruth Proceedings of the National Academy of Sciences, Vol. 115, Issue 43 https://doi.org/10.1073/pnas.1805518115	journal	October 2018
Peatland warming strongly increases fine-root growth Malhotra, Avni; Brice, Deanne J.; Childs, Joanne Proceedings of the National Academy of Sciences, Vol. 117, Issue 30 https://doi.org/10.1073/pnas.2003361117	journal	July 2020
Vertical stratification of peatland microbial communities follows a gradient of functional types across hummock–hollow microtopographies Asemaninejad, Asma; Thorn, R. Greg; Branfireun, Brian A. Écoscience, Vol. 26, Issue 3 https://doi.org/10.1080/11956860.2019.1595932	journal	April 2019
Pronounced and unavoidable impacts of low-end global warming on northern high-latitude land ecosystems Ito, Akihiko; Reyer, Christopher P. O.; Gädeke, Anne Environmental Research Letters, Vol. 15, Issue 4 https://doi.org/10.1088/1748-9326/ab702b	journal	March 2020
UCHIME improves sensitivity and speed of chimera detection Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C. Bioinformatics, Vol. 27, Issue 16 https://doi.org/10.1093/bioinformatics/btr381	journal	June 2011
PEAR: a fast and accurate Illumina Paired-End reAd mergeR Zhang, J.; Kobert, K.; Flouri, T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt593	journal	October 2013
Soil depth matters: shift in composition and inter-kingdom co-occurrence patterns of microorganisms in forest soils Mundra, Sunil; Kjønaas, O. Janne; Morgado, Luis N. FEMS Microbiology Ecology, Vol. 97, Issue 3 https://doi.org/10.1093/femsec/fiab022	journal	February 2021
Functional convergence in the decomposition of fungal necromass in soil and wood Maillard, François; Schilling, Jonathan; Andrews, Erin FEMS Microbiology Ecology, Vol. 96, Issue 2 https://doi.org/10.1093/femsec/fiz209	journal	December 2019
Mycelia‐derived C contributes more to nitrogen cycling than root‐derived C in ectomycorrhizal alpine forests Zhang, Ziliang; Phillips, Richard P.; Zhao, Wenqiang Functional Ecology, Vol. 33, Issue 2 https://doi.org/10.1111/1365-2435.13236	journal	November 2018
Understanding the dominant controls on litter decomposition Bradford, Mark A.; Berg, Björn; Maynard, Daniel S. Journal of Ecology, Vol. 104, Issue 1 https://doi.org/10.1111/1365-2745.12507	journal	November 2015
Melanization of mycorrhizal fungal necromass structures microbial decomposer communities Fernandez, Christopher W.; Kennedy, Peter G. Journal of Ecology, Vol. 106, Issue 2 https://doi.org/10.1111/1365-2745.12920	journal	February 2018
Substrate quality drives fungal necromass decay and decomposer community structure under contrasting vegetation types Beidler, Katilyn V.; Phillips, Richard P.; Andrews, Erin Journal of Ecology, Vol. 108, Issue 5 https://doi.org/10.1111/1365-2745.13385	journal	April 2020
First evidences that the ectomycorrhizal fungus Paxillus involutus mobilizes nitrogen and carbon from saprotrophic fungus necromass: Do ectomycorrhizal fungi degrade brown rot fungi? Akroume, Emila; Maillard, François; Bach, Cyrille Environmental Microbiology, Vol. 21, Issue 1 https://doi.org/10.1111/1462-2920.14440	journal	November 2018
Melanin mitigates the accelerated decay of mycorrhizal necromass with peatland warming Fernandez, Christopher W.; Heckman, Katherine; Kolka, Randall Ecology Letters, Vol. 22, Issue 3 https://doi.org/10.1111/ele.13209	journal	January 2019
The influence of temperature and water table position on carbon dioxide and methane emissions from laboratory columns of peatland soils Moore, T. R.; Dalva, M. Journal of Soil Science, Vol. 44, Issue 4 https://doi.org/10.1111/j.1365-2389.1993.tb02330.x	journal	December 1993
REVIEW: Mechanisms driving change: altered species interactions and ecosystem function through global warming: Ecosystem function under global warming Traill, Lochran W.; Lim, Matthew L. M.; Sodhi, Navjot S. Journal of Animal Ecology, Vol. 79, Issue 5 https://doi.org/10.1111/j.1365-2656.2010.01695.x	journal	May 2010
A new method for non-parametric multivariate analysis of variance: NON-PARAMETRIC MANOVA FOR ECOLOGY Anderson, Marti J. Austral Ecology, Vol. 26, Issue 1 https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x	journal	February 2001
The biology of mycorrhiza in the Ericaceae. XVIII. Chitin degradation by Hymenoscyphus ericae and transfer of chitin-nitrogen to the host plant Kerley, Simon J.; Read, David J. New Phytologist, Vol. 131, Issue 3 https://doi.org/10.1111/j.1469-8137.1995.tb03073.x	journal	November 1995
Carbon sequestration in peatland: patterns and mechanisms of response to climate change Belyea, Lisa R.; Malmer, Nils Global Change Biology, Vol. 10, Issue 7 https://doi.org/10.1111/j.1529-8817.2003.00783.x	journal	July 2004
New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities Ihrmark, Katarina; Bödeker, Inga T. M.; Cruz-Martinez, Karelyn FEMS Microbiology Ecology, Vol. 82, Issue 3 https://doi.org/10.1111/j.1574-6941.2012.01437.x	journal	July 2012
Towards a unified paradigm for sequence-based identification of fungi Kõljalg, Urmas; Nilsson, R. Henrik; Abarenkov, Kessy Molecular Ecology, Vol. 22, Issue 21 https://doi.org/10.1111/mec.12481	journal	September 2013
Genome‐based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles Lofgren, Lotus A.; Uehling, Jessie K.; Branco, Sara Molecular Ecology, Vol. 28, Issue 4 https://doi.org/10.1111/mec.14995	journal	February 2019
Root presence modifies the long‐term decomposition dynamics of fungal necromass and the associated microbial communities in a boreal forest Maillard, François; Kennedy, Peter G.; Adamczyk, Bartosz Molecular Ecology, Vol. 30, Issue 8 https://doi.org/10.1111/mec.15828	journal	March 2021
Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests Clemmensen, Karina E.; Finlay, Roger D.; Dahlberg, Anders New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13208	journal	December 2014
Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest Brzostek, Edward R.; Dragoni, Danilo; Brown, Zachary A. New Phytologist, Vol. 206, Issue 4 https://doi.org/10.1111/nph.13303	journal	January 2015
Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? Fernandez, Christopher W.; Kennedy, Peter G. New Phytologist, Vol. 209, Issue 4 https://doi.org/10.1111/nph.13648	journal	September 2015
Dead fungal mycelium in forest soil represents a decomposition hotspot and a habitat for a specific microbial community Brabcová, Vendula; Nováková, Monika; Davidová, Anna New Phytologist, Vol. 210, Issue 4 https://doi.org/10.1111/nph.13849	journal	February 2016
Accurate Estimation of Fungal Diversity and Abundance through Improved Lineage-Specific Primers Optimized for Illumina Amplicon Sequencing Taylor, D. Lee; Walters, William A.; Lennon, Niall J. Applied and Environmental Microbiology, Vol. 82, Issue 24 https://doi.org/10.1128/AEM.02576-16	journal	October 2016
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/AEM.03006-05	journal	July 2006
Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes Read, David J.; Leake, Jonathan R.; Perez-Moreno, Jesus Canadian Journal of Botany, Vol. 82, Issue 8 https://doi.org/10.1139/b04-123	journal	August 2004
BayesHammer: Bayesian clustering for error correction in single-cell sequencing Nikolenko, Sergey I.; Korobeynikov, Anton I.; Alekseyev, Max A. BMC Genomics, Vol. 14, Issue Suppl 1 https://doi.org/10.1186/1471-2164-14-S1-S7	journal	January 2013
LotuS: an efficient and user-friendly OTU processing pipeline Hildebrand, Falk; Tadeo, Raul; Voigt, Anita Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-30	journal	January 2014
Associations between species and groups of sites: indices and statistical inference Cáceres, Miquel De; Legendre, Pierre Ecology, Vol. 90, Issue 12 https://doi.org/10.1890/08-1823.1	journal	December 2009
Top-down control of soil fungal community composition by a globally distributed keystone consumer Crowther, Thomas W.; Stanton, David W. G.; Thomas, Stephen M. Ecology, Vol. 94, Issue 11 https://doi.org/10.1890/13-0197.1	journal	November 2013
Northern Peatlands: Role in the Carbon Cycle and Probable Responses to Climatic Warming Gorham, Eville Ecological Applications, Vol. 1, Issue 2 https://doi.org/10.2307/1941811	journal	May 1991
Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (≡ Hymenoscyphus ericae), Leotiomycetes Hambleton, Sarah; Sigler, Lynne Studies in Mycology, Vol. 53 https://doi.org/10.3114/sim.53.1.1	journal	January 2005
Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated CO ₂ atmosphere Hanson, Paul J.; Riggs, Jeffery S.; Nettles, W. Robert Biogeosciences, Vol. 14, Issue 4 https://doi.org/10.5194/bg-14-861-2017	journal	January 2017
VSEARCH: a versatile open source tool for metagenomics Rognes, Torbjørn; Flouri, Tomáš; Nichols, Ben PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2584	journal	January 2016

Similar Records

Substrate quality drives fungal necromass decay and decomposer community structure under contrasting vegetation types

Journal Article · Mon Mar 09 00:00:00 EDT 2020 · Journal of Ecology · OSTI ID:1802857

SPRUCE Fungal Necromass Litter Bag Decomposition Study in SPRUCE Experimental Plots, 2016-2018

Dataset · Mon Dec 31 23:00:00 EST 2018 · OSTI ID:1503589

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
SPRUCE
bog microtopography
climate change
decomposition
mycorrhizal residues
necromass congeneric colonization advantage
plant sciences

Warming drives a ‘hummockification’ of microbial communities associated with decomposing mycorrhizal fungal necromass in peatlands

Citation Formats

References (65)

Similar Records

Related Subjects