Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils

Maillard, François; Michaud, Talia J.; See, Craig R.; DeLancey, Lang C.; Blazewicz, Steven J.; Kimbrel, Jeffrey A.; Pett-Ridge, Jennifer; Kennedy, Peter G.

doi:10.1128/msystems.00390-23

Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils

Journal Article · Tue Jun 20 00:00:00 EDT 2023 · mSystems

DOI:https://doi.org/10.1128/msystems.00390-23· OSTI ID:2204112

Maillard, François ^[1]; Michaud, Talia J. ^[1]; See, Craig R. ^[1]; DeLancey, Lang C. ^[1]; Blazewicz, Steven J. ^[2]; Kimbrel, Jeffrey A. ^[2]; ^[3]; ^[1]

University of Minnesota, Saint Paul, MN (United States)
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Univ. of California, Merced, CA (United States)

Microbial necromass contributes significantly to both soil carbon (C) persistence and ecosystem nitrogen (N) availability, but quantitative estimates of C and N movement from necromass into soils and decomposer communities are lacking. Additionally, while melanin is known to slow fungal necromass decomposition, how it influences microbial C and N acquisition as well as elemental release into soils remains unclear. Here, we tracked decomposition of isotopically labeled low and high melanin fungal necromass and measured ¹³C and ¹⁵N accumulation in surrounding soils and microbial communities over 77 d in a temperate forest in Minnesota, USA. Mass loss was significantly higher from low melanin necromass, corresponding with greater ¹³C and ¹⁵N soil inputs. A taxonomically and functionally diverse array of bacteria and fungi was enriched in ¹³C and/or ¹⁵N at all sampling points, with enrichment being consistently higher on low melanin necromass and earlier in decomposition. Similar patterns of preferential C and N enrichment of many bacterial and fungal genera early in decomposition suggest that both microbial groups co-contribute to the rapid assimilation of resource-rich soil organic matter inputs. While overall richness of taxa enriched in C was higher than in N for both bacteria and fungi, there was a significant positive relationship between C and N in co-enriched taxa. Collectively, our results demonstrate that melanization acts as a key ecological trait mediating not only fungal necromass decomposition rate but also necromass C and N release and that both elements are rapidly co-utilized by diverse bacterial and fungal decomposers in natural settings.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 2204112

Report Number(s):: LLNL--JRNL-852819; 1080387

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 4 Vol. 8; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (64)

Estimating taxon‐specific population dynamics in diverse microbial communities Koch, Benjamin J.; McHugh, Theresa A.; Hayer, Michaela Ecosphere, Vol. 9, Issue 1 https://doi.org/10.1002/ecs2.2090	journal	January 2018
Fine root decomposition rates do not mirror those of leaf litter among temperate tree species Hobbie, Sarah E.; Oleksyn, Jacek; Eissenstat, David M. Oecologia, Vol. 162, Issue 2 https://doi.org/10.1007/s00442-009-1479-6	journal	October 2009
Soil drying procedure affects the DNA quantification of Lactarius vinosus but does not change the fungal community composition Castaño, Carles; Parladé, Javier; Pera, Joan Mycorrhiza, Vol. 26, Issue 8 https://doi.org/10.1007/s00572-016-0714-3	journal	June 2016
FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles Põlme, Sergei; Abarenkov, Kessy; Henrik Nilsson, R. Fungal Diversity, Vol. 105, Issue 1 https://doi.org/10.1007/s13225-020-00466-2	journal	November 2020
Inhibition of polysaccharases by melanin: Enzyme inhibition in relation to mycolysis Bull, Alan T. Archives of Biochemistry and Biophysics, Vol. 137, Issue 2 https://doi.org/10.1016/0003-9861(70)90448-0	journal	April 1970
Characterization of chitinase and chitobiase produced by the entomopathogenic fungus Metarhizium anisopliae St. Leger, R. J.; Cooper, R. M.; Charnley, A. K. Journal of Invertebrate Pathology, Vol. 58, Issue 3 https://doi.org/10.1016/0022-2011(91)90188-V	journal	November 1991
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
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
Soil carbon sequestration to mitigate climate change Lal, R. Geoderma, Vol. 123, Issue 1-2 https://doi.org/10.1016/j.geoderma.2004.01.032	journal	November 2004
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
Considering fungal:bacterial dominance in soils – Methods, controls, and ecosystem implications Strickland, Michael S.; Rousk, Johannes Soil Biology and Biochemistry, Vol. 42, Issue 9 https://doi.org/10.1016/j.soilbio.2010.05.007	journal	September 2010
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
Distributions of fungal melanin across species and soils Siletti, Cheta E.; Zeiner, Carolyn A.; Bhatnagar, Jennifer M. Soil Biology and Biochemistry, Vol. 113 https://doi.org/10.1016/j.soilbio.2017.05.030	journal	October 2017
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
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
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
Microbial utilization of simple and complex carbon compounds in a temperate forest soil Martinović, Tijana; Mašínová, Tereza; López-Mondéjar, Rubén Soil Biology and Biochemistry, Vol. 173 https://doi.org/10.1016/j.soilbio.2022.108786	journal	October 2022
Active populations and growth of soil microorganisms are framed by mean annual precipitation in three California annual grasslands Foley, Megan M.; Blazewicz, Steven J.; McFarlane, Karis J. Soil Biology and Biochemistry, Vol. 177 https://doi.org/10.1016/j.soilbio.2022.108886	journal	February 2023
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
Soil respiration and the global carbon cycle Schlesinger, William H.; Andrews, Jeffrey A. Biogeochemistry, Vol. 48, Issue 1, p. 7-20 https://doi.org/10.1023/A:1006247623877	journal	January 2000
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
Soil carbon storage informed by particulate and mineral-associated organic matter Cotrufo, M. Francesca; Ranalli, Maria Giovanna; Haddix, Michelle L. Nature Geoscience, Vol. 12, Issue 12 https://doi.org/10.1038/s41561-019-0484-6	journal	November 2019
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
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Two pantropical Ascomycetes: Chaetosphaeria cylindrospora sp. nov. and Rimaconus , a new genus for Lasiosphaeria jamaicensis Huhndorf, Sabine M.; Fernández, Fernando A.; Taylor, Joanne E. Mycologia, Vol. 93, Issue 6 https://doi.org/10.1080/00275514.2001.12063242	journal	November 2001
Destruction of Fungal Melanins by Ligninases ofPhanerochaete chrysosporiumand Other White Rot Fungi Butler, M. J.; Day, A. W. International Journal of Plant Sciences, Vol. 159, Issue 6 https://doi.org/10.1086/314093	journal	November 1998
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Self versus non-self: fungal cell wall degradation in Trichoderma Gruber, Sabine; Seidl-Seiboth, Verena Microbiology, Vol. 158, Issue 1 https://doi.org/10.1099/mic.0.052613-0	journal	January 2012
UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing Edgar, Robert C. BioRxiv https://doi.org/10.1101/081257	posted_content	October 2016
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
Taxonomic patterns in the nitrogen assimilation of soil prokaryotes: Nitrogen assimilation of soil prokaryotes Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert Environmental Microbiology, Vol. 20, Issue 3 https://doi.org/10.1111/1462-2920.14051	journal	March 2018
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
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
The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Cotrufo, M. Francesca; Wallenstein, Matthew D.; Boot, Claudia M. Global Change Biology, Vol. 19, Issue 4 https://doi.org/10.1111/gcb.12113	journal	February 2013
Conceptualizing soil organic matter into particulate and mineral‐associated forms to address global change in the 21st century Lavallee, Jocelyn M.; Soong, Jennifer L.; Cotrufo, M. Francesca Global Change Biology, Vol. 26, Issue 1 https://doi.org/10.1111/gcb.14859	journal	November 2019
Temperature sensitivity of SOM decomposition is linked with a K‐selected microbial community Li, Hui; Yang, Shan; Semenov, Mikhail V. Global Change Biology, Vol. 27, Issue 12 https://doi.org/10.1111/gcb.15593	journal	March 2021
Hyphae move matter and microbes to mineral microsites: Integrating the hyphosphere into conceptual models of soil organic matter stabilization See, Craig R.; Keller, Adrienne B.; Hobbie, Sarah E. Global Change Biology, Vol. 28, Issue 8 https://doi.org/10.1111/gcb.16073	journal	January 2022
Outcomes of fungal interactions are determined by soil invertebrate grazers: Grazers alter fungal community Crowther, Thomas W.; Boddy, Lynne; Jones, T. Hefin Ecology Letters, Vol. 14, Issue 11 https://doi.org/10.1111/j.1461-0248.2011.01682.x	journal	September 2011
Reciprocal carbon and nitrogen transfer between an ericaceous dwarf shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas Grelet, Gwen-Aëlle; Johnson, David; Paterson, Eric New Phytologist, Vol. 182, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.02813.x	journal	March 2009
Fungi growing on aromatic hydrocarbons: biotechnology's unexpected encounter with biohazard? Prenafeta-Boldú, Francesc X.; Summerbell, Richard; Sybren de Hoog, G. FEMS Microbiology Reviews, Vol. 30, Issue 1 https://doi.org/10.1111/j.1574-6976.2005.00007.x	journal	January 2006
Biology and applications of Clonostachys rosea Sun, Z. -B.; Li, S. -D.; Ren, Q. Journal of Applied Microbiology, Vol. 129, Issue 3 https://doi.org/10.1111/jam.14625	journal	March 2020
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
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
Global-Scale Similarities in Nitrogen Release Patterns During Long-Term Decomposition Parton, W.; Silver, W. L.; Burke, I. C. Science, Vol. 315, Issue 5810 https://doi.org/10.1126/science.1134853	journal	January 2007
Quantitative Microbial Ecology through Stable Isotope Probing Hungate, Bruce A.; Mau, Rebecca L.; Schwartz, Egbert Applied and Environmental Microbiology, Vol. 81, Issue 21 https://doi.org/10.1128/AEM.02280-15	journal	August 2015
Microbial rRNA Synthesis and Growth Compared through Quantitative Stable Isotope Probing with H ₂ ¹⁸ O Papp, Katerina; Hungate, Bruce A.; Schwartz, Egbert Applied and Environmental Microbiology, Vol. 84, Issue 8 https://doi.org/10.1128/AEM.02441-17	journal	February 2018
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
Stable Isotope Probing with 15N Achieved by Disentangling the Effects of Genome G+C Content and Isotope Enrichment on DNA Density Buckley, D. H.; Huangyutitham, V.; Hsu, S. -F. Applied and Environmental Microbiology, Vol. 73, Issue 10 https://doi.org/10.1128/AEM.02609-06	journal	March 2007
Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition Griffiths, R. I.; Whiteley, A. S.; O'Donnell, A. G. Applied and Environmental Microbiology, Vol. 66, Issue 12 https://doi.org/10.1128/AEM.66.12.5488-5491.2000	journal	December 2000
Stable-Isotope-Informed, Genome-Resolved Metagenomics Uncovers Potential Cross-Kingdom Interactions in Rhizosphere Soil Starr, Evan P.; Shi, Shengjing; Blazewicz, Steven J. mSphere, Vol. 6, Issue 5 https://doi.org/10.1128/mSphere.00085-21	journal	October 2021
Fungal melanins: a review Butler, M. J.; Day, A. W. Canadian Journal of Microbiology, Vol. 44, Issue 12 https://doi.org/10.1139/w98-119	journal	December 1998
Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil Blazewicz, Steven J.; Schwartz, Egbert; Firestone, Mary K. Ecology, Vol. 95, Issue 5 https://doi.org/10.1890/13-1031.1	journal	May 2014
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
Factors for Conversion of Fungal Biovolume Values to Biomass, Carbon and Nitrogen: Variation with Mycelial Ages, Growth Conditions, and Strains of Fungi from a Salt Marsh Newell, Steven Y.; Statzell-Tallman, Adele Oikos, Vol. 39, Issue 2 https://doi.org/10.2307/3544494	journal	August 1982
Fungal Melanin: What do We Know About Structure? Nosanchuk, Joshua D.; Stark, Ruth E.; Casadevall, Arturo Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01463	journal	December 2015
Escherichia coli Can Eat DNA as an Excellent Nitrogen Source to Grow Quickly Huang, Lili; Zhang, Yehui; Du, Xinmei Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.894849	journal	June 2022
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
Non-biological synthetic spike-in controls and the AMPtk software pipeline improve mycobiome data Palmer, Jonathan M.; Jusino, Michelle A.; Banik, Mark T. PeerJ, Vol. 6 https://doi.org/10.7717/peerj.4925	journal	January 2018

Similar Records

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

Journal Article · Sat Jun 22 20:00:00 EDT 2024 · Environmental Microbiology Reports · OSTI ID:2470372

Bacterial and fungal growth on fungal necromass and its diverse components: Shared profiles and divergent constraints revealed by high‐throughput phenotyping

Journal Article · Wed Jul 30 20:00:00 EDT 2025 · Functional Ecology · OSTI ID:2997205

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

Journal Article · Thu Sep 23 20:00:00 EDT 2021 · New Phytologist · OSTI ID:1982918

Related Subjects

54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
bacteria
forests
fungi
quantitative stable-isotope probing
soil carbon and nitrogen cycling

Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils

Citation Formats

References (64)

Similar Records

Related Subjects