Fungi rather than bacteria drive early mass loss from fungal necromass regardless of particle size

Pérez‐Pazos, Eduardo; Beidler, Katilyn V.; Narayanan, Achala; Beatty, Briana H.; Maillard, François; Bancos, Alexandra; Heckman, Katherine A.; Kennedy, Peter G.

doi:10.1111/1758-2229.13280

Title: Fungi rather than bacteria drive early mass loss from fungal necromass regardless of particle size

Journal Article · Sun Jun 23 00:00:00 UTC 2024 · Environmental Microbiology Reports

DOI: https://doi.org/10.1111/1758-2229.13280 · OSTI ID:2470372

^[1]; Beidler, Katilyn V. ^[1]; Narayanan, Achala ^[1]; Beatty, Briana H. ^[1]; Maillard, François ^[2]; Bancos, Alexandra ^[1]; Heckman, Katherine A. ^[3]; Kennedy, Peter G. ^[1]

Univ. of Minnesota, St. Paul, MN (United States)
Lund Univ. (Sweden)
USDA Forest Service, Houghton, MI (United States)

Microbial necromass is increasingly recognized as an important fast-cycling component of the long-term carbon present in soils. To better understand how fungi and bacteria individually contribute to the decomposition of fungal necromass, three particle sizes (>500, 250–500, and <250 μm) of Hyaloscypha bicolor necromass were incubated in laboratory microcosms inoculated with individual strains of two fungi and two bacteria. Decomposition was assessed after 15 and 28 days via necromass loss, microbial respiration, and changes in necromass pH, water content, and chemistry. To examine how fungal–bacterial interactions impact microbial growth on necromass, single and paired cultures of bacteria and fungi were grown in microplates containing necromass-infused media. Microbial growth was measured after 5 days through quantitative PCR. Regardless of particle size, necromass colonized by fungi had higher mass loss and respiration than both bacteria and uninoculated controls. Fungal colonization increased necromass pH, water content, and altered chemistry, while necromass colonized by bacteria remained mostly unaltered. Bacteria grew significantly more when co-cultured with a fungus, while fungal growth was not significantly affected by bacteria. Collectively, our results suggest that fungi act as key early decomposers of fungal necromass and that bacteria may require the presence of fungi to actively participate in necromass decomposition.

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Research Organization:: Univ. of Minnesota, St. Paul, MN (United States)

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

OSTI ID:: 2470372

Journal Information:: Environmental Microbiology Reports, Journal Name: Environmental Microbiology Reports Journal Issue: 3 Vol. 16; ISSN 1758-2229

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United States

Language:: English

References (65)

Principles of Terrestrial Ecosystem Ecology Chapin, F. Stuart; Matson, Pamela A.; Vitousek, Peter M. https://doi.org/10.1007/978-1-4419-9504-9	book	September 2011
Mycorrhizal roots slow the decay of belowground litters in a temperate hardwood forest Beidler, Katilyn V.; Oh, Young E.; Pritchard, Seth G. Oecologia, Vol. 197, Issue 3 https://doi.org/10.1007/s00442-021-05051-1	journal	October 2021
Biogeochemical Hot Spots and Hot Moments at the Interface of Terrestrial and Aquatic Ecosystems McClain, Michael E.; Boyer, Elizabeth W.; Dent, C. Lisa Ecosystems, Vol. 6, Issue 4 https://doi.org/10.1007/s10021-003-0161-9	journal	June 2003
Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Prescott, Cindy E. Biogeochemistry, Vol. 101, Issue 1-3 https://doi.org/10.1007/s10533-010-9439-0	journal	April 2010
Interactions between leaf litter quality, particle size, and microbial community during the earliest stage of decay Rinkes, Zachary L.; DeForest, Jared L.; Grandy, A. Stuart Biogeochemistry, Vol. 117, Issue 1 https://doi.org/10.1007/s10533-013-9872-y	journal	June 2013
Ecology of ligninolytic fungi associated with leaf litter decomposition Osono, Takashi Ecological Research, Vol. 22, Issue 6 https://doi.org/10.1007/s11284-007-0390-z	journal	June 2007
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Reduced particle size of plant material does not stimulate decomposition, but affects the microbivorous microfauna Vestergaard, Peter; Rønn, Regin; Christensen, Søren Soil Biology and Biochemistry, Vol. 33, Issue 12-13 https://doi.org/10.1016/S0038-0717(01)00107-9	journal	October 2001
Mechanisms and ecological implications of the movement of bacteria in soil Yang, Pu; van Elsas, Jan Dirk Applied Soil Ecology, Vol. 129 https://doi.org/10.1016/j.apsoil.2018.04.014	journal	August 2018
Fungal necromass presents a high potential for Mercury immobilization in soil Maillard, François; Pflender, Stéphane; Heckman, Katherine A. Chemosphere, Vol. 311 https://doi.org/10.1016/j.chemosphere.2022.136994	journal	January 2023
Living in a fungal world: impact of fungi on soil bacterial niche development Boer, Wietse de; Folman, Larissa B.; Summerbell, Richard C. FEMS Microbiology Reviews, Vol. 29, Issue 4 https://doi.org/10.1016/j.femsre.2004.11.005	journal	September 2005
Morphology and enzyme production of Trichoderma reesei Rut C-30 are affected by the physical and structural characteristics of cellulosic substrates Peciulyte, Ausra; Anasontzis, George E.; Karlström, Katarina Fungal Genetics and Biology, Vol. 72 https://doi.org/10.1016/j.fgb.2014.07.011	journal	November 2014
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
Real-Time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDα) genes from Gram positive and Gram negative bacteria in soil and sediment samples Cébron, Aurélie; Norini, Marie-Paule; Beguiristain, Thierry Journal of Microbiological Methods, Vol. 73, Issue 2 https://doi.org/10.1016/j.mimet.2008.01.009	journal	May 2008
Particle size alters litter diversity effects on decomposition Tiunov, Alexei V. Soil Biology and Biochemistry, Vol. 41, Issue 1 https://doi.org/10.1016/j.soilbio.2008.09.017	journal	January 2009
Soil aggregation: Influence on microbial biomass and implications for biological processes Gupta, Vadakattu V. S. R.; Germida, James J. Soil Biology and Biochemistry, Vol. 80 https://doi.org/10.1016/j.soilbio.2014.09.002	journal	January 2015
Microbial hotspots and hot moments in soil: Concept & review Kuzyakov, Yakov; Blagodatskaya, Evgenia Soil Biology and Biochemistry, Vol. 83 https://doi.org/10.1016/j.soilbio.2015.01.025	journal	April 2015
Understanding mechanisms of soil biota involvement in soil aggregation: A way forward with saprobic fungi? Lehmann, Anika; Rillig, Matthias C. Soil Biology and Biochemistry, Vol. 88 https://doi.org/10.1016/j.soilbio.2015.06.006	journal	September 2015
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
Mycelium- and root-derived C inputs differ in their impacts on soil organic C pools and decomposition in forests Zhang, Ziliang; Xiao, Juan; Yuan, Yuanshuang Soil Biology and Biochemistry, Vol. 123 https://doi.org/10.1016/j.soilbio.2018.05.015	journal	August 2018
The afterlife effects of fungal morphology: Contrasting decomposition rates between diffuse and rhizomorphic necromass Certano, Amanda K.; Fernandez, Christopher W.; Heckman, Katherine A. Soil Biology and Biochemistry, Vol. 126 https://doi.org/10.1016/j.soilbio.2018.08.002	journal	November 2018
Soil textural heterogeneity impacts bacterial but not fungal diversity Seaton, Fiona M.; George, Paul B. L.; Lebron, Inma Soil Biology and Biochemistry, Vol. 144 https://doi.org/10.1016/j.soilbio.2020.107766	journal	May 2020
Metagenomics and stable isotope probing reveal the complementary contribution of fungal and bacterial communities in the recycling of dead biomass in forest soil López-Mondéjar, Rubén; Tláskal, Vojtěch; Větrovský, Tomáš Soil Biology and Biochemistry, Vol. 148 https://doi.org/10.1016/j.soilbio.2020.107875	journal	September 2020
Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter Angst, Gerrit; Mueller, Kevin E.; Nierop, Klaas G. J. Soil Biology and Biochemistry, Vol. 156 https://doi.org/10.1016/j.soilbio.2021.108189	journal	May 2021
Microbial necromass as the source of soil organic carbon in global ecosystems Wang, Baorong; An, Shaoshan; Liang, Chao Soil Biology and Biochemistry, Vol. 162 https://doi.org/10.1016/j.soilbio.2021.108422	journal	November 2021
Knowns and unknowns of the soil fungal necrobiome Kennedy, Peter G.; Maillard, François Trends in Microbiology, Vol. 31, Issue 2 https://doi.org/10.1016/j.tim.2022.08.011	journal	February 2023
21st Century Guidebook to Fungi Moore, David; Robson, Geoffrey D.; Trinci, Anthony P. J. https://doi.org/10.1017/9781108776387	book	January 2020
Beyond the : variation in the intra- and interspecific scaling of metabolic rate in animals Glazier, Douglas S. Biological Reviews, Vol. 80, Issue 04 https://doi.org/10.1017/S1464793105006834	journal	August 2005
Taking the Fungal Highway: Mobilization of Pollutant-Degrading Bacteria by Fungi Kohlmeier, Stefanie; Smits, Theo H. M.; Ford, Roseanne M. Environmental Science & Technology, Vol. 39, Issue 12 https://doi.org/10.1021/es047979z	journal	June 2005
Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling López-Mondéjar, Ruben; Brabcová, Vendula; Štursová, Martina The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0084-2	journal	February 2018
Plant-associated fungi support bacterial resilience following water limitation Hestrin, Rachel; Kan, Megan; Lafler, Marissa The ISME Journal, Vol. 16, Issue 12 https://doi.org/10.1038/s41396-022-01308-6	journal	September 2022
Life and death in the soil microbiome: how ecological processes influence biogeochemistry Sokol, Noah W.; Slessarev, Eric; Marschmann, Gianna L. Nature Reviews Microbiology, Vol. 20, Issue 7 https://doi.org/10.1038/s41579-022-00695-z	journal	February 2022
Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture Woo, Sheridan L.; Hermosa, Rosa; Lorito, Matteo Nature Reviews Microbiology, Vol. 21, Issue 5 https://doi.org/10.1038/s41579-022-00819-5	journal	November 2022
Tradeoffs in hyphal traits determine mycelium architecture in saprobic fungi Lehmann, Anika; Zheng, Weishuang; Soutschek, Katharina Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-50565-7	journal	October 2019
Soil microbial biomass—what do the numbers really mean? Dalal, R. C. Australian Journal of Experimental Agriculture, Vol. 38, Issue 7 https://doi.org/10.1071/EA97142	journal	January 1998
Defining a core microbial necrobiome associated with decomposing fungal necromass Cantoran, Anahi; Maillard, François; Baldrian, Petr FEMS Microbiology Ecology, Vol. 99, Issue 9 https://doi.org/10.1093/femsec/fiad098	journal	August 2023
Revisiting life strategy concepts in environmental microbial ecology Ho, Adrian; Lonardo, D. Paolo Di; Bodelier, Paul L. E. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fix006	journal	January 2017
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
Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution Janusz, Grzegorz; Pawlik, Anna; Sulej, Justyna FEMS Microbiology Reviews, Vol. 41, Issue 6 https://doi.org/10.1093/femsre/fux049	journal	October 2017
Metarhizium: jack of all trades, master of many St. Leger, Raymond J.; Wang, Jonathan B. Open Biology, Vol. 10, Issue 12 https://doi.org/10.1098/rsob.200307	journal	December 2020
The entomopathogenic fungus Metarhizium anisopliae alters ambient pH, allowing extracellular protease production and activity St Leger, Raymond J.; Screen, Steven E.; Nelson, Judd O. Microbiology, Vol. 145, Issue 10 https://doi.org/10.1099/00221287-145-10-2691	journal	October 1999
Distinct carbon fractions drive a generalisable two‐pool model of fungal necromass decomposition See, Craig R.; Fernandez, Chris W.; Conley, Anna M. Functional Ecology, Vol. 35, Issue 3 https://doi.org/10.1111/1365-2435.13728	journal	December 2020
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
Feeding on fungi: genomic and proteomic analysis of the enzymatic machinery of bacteria decomposing fungal biomass Starke, Robert; Morais, Daniel; Větrovský, Tomáš Environmental Microbiology, Vol. 22, Issue 11 https://doi.org/10.1111/1462-2920.15183	journal	August 2020
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
Quantitative assessment of microbial necromass contribution to soil organic matter Liang, Chao; Amelung, Wulf; Lehmann, Johannes Global Change Biology, Vol. 25, Issue 11 https://doi.org/10.1111/gcb.14781	journal	August 2019
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts Gardes, M.; Bruns, T. D. Molecular Ecology, Vol. 2, Issue 2 https://doi.org/10.1111/j.1365-294X.1993.tb00005.x	journal	April 1993
Bacterial mycophagy: definition and diagnosis of a unique bacterial–fungal interaction Leveau, Johan H. J.; Preston, Gail M. New Phytologist, Vol. 177, Issue 4 https://doi.org/10.1111/j.1469-8137.2007.02325.x	journal	December 2007
Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure: Effects of AM mycelial exudates on soil bacteria Toljander, Jonas F.; Lindahl, BjÃ¶rn D.; Paul, Leslie R. FEMS Microbiology Ecology, Vol. 61, Issue 2 https://doi.org/10.1111/j.1574-6941.2007.00337.x	journal	August 2007
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
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
Warming drives a ‘hummockification’ of microbial communities associated with decomposing mycorrhizal fungal necromass in peatlands Maillard, François; Fernandez, Christopher W.; Mundra, Sunil New Phytologist, Vol. 234, Issue 6 https://doi.org/10.1111/nph.17755	journal	October 2021
Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest Clemmensen, K. E.; Bahr, A.; Ovaskainen, O. Science, Vol. 339, Issue 6127 https://doi.org/10.1126/science.1231923	journal	March 2013
Ambient pH Is a Major Determinant in the Expression of Cuticle-Degrading Enzymes and Hydrophobin by Metarhizium anisopliae St. Leger, Raymond J.; Joshi, Lokesh; Roberts, Donald Applied and Environmental Microbiology, Vol. 64, Issue 2 https://doi.org/10.1128/AEM.64.2.709-713.1998	journal	February 1998
16S ribosomal DNA amplification for phylogenetic study. Weisburg, W. G.; Barns, S. M.; Pelletier, D. A. Journal of Bacteriology, Vol. 173, Issue 2 https://doi.org/10.1128/jb.173.2.697-703.1991	journal	January 1991
The Mycelium as a Network Fricker, Mark D.; Heaton, Luke L. M.; Jones, Nick S. Microbiology Spectrum, Vol. 5, Issue 3 https://doi.org/10.1128/microbiolspec.funk-0033-2017	journal	June 2017
Contribution of mycorrhizae and soil fungi to nutrient cycling in a Douglas-fir ecosystem Fogel, Robert; Hunt, Gary Canadian Journal of Forest Research, Vol. 13, Issue 2 https://doi.org/10.1139/x83-031	journal	April 1983
Mycorrhizal Fungi as Mediators of Soil Organic Matter Dynamics Frey, Serita D. Annual Review of Ecology, Evolution, and Systematics, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110617-062331	journal	November 2019
Validation and Application of a PCR Primer Set to Quantify Fungal Communities in the Soil Environment by Real-Time Quantitative PCR Chemidlin Prévost-Bouré, Nicolas; Christen, Richard; Dequiedt, Samuel PLoS ONE, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pone.0024166	journal	September 2011
Welcome to the Tidyverse Wickham, Hadley; Averick, Mara; Bryan, Jennifer Journal of Open Source Software, Vol. 4, Issue 43 https://doi.org/10.21105/joss.01686	journal	November 2019
Fate of Decomposed Fungal Cell Wall Material in Organic Horizons of Old-Growth Douglas-fir Forest Soils Zeglin, Lydia H.; Myrold, David D. Soil Science Society of America Journal, Vol. 77, Issue 2 https://doi.org/10.2136/sssaj2012.0204	journal	March 2013
Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources Mooshammer, Maria; Wanek, Wolfgang; Zechmeister-Boltenstern, Sophie Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00022	journal	January 2014
Burkholderia terrae BS001 migrates proficiently with diverse fungal hosts through soil and provides protection from antifungal agents Nazir, Rashid; Tazetdinova, Diana I.; van Elsas, Jan Dirk Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00598	journal	November 2014
Fungal alkaline proteases and their potential applications in different industries Pawar, Kadambari Subhash; Singh, Paras Nath; Singh, Sanjay Kumar Frontiers in Microbiology, Vol. 14 https://doi.org/10.3389/fmicb.2023.1138401	journal	March 2023

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