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

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 de...

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Autores principales: Maillard, François, Michaud, Talia J., See, Craig R., DeLancey, Lang C., Blazewicz, Steven J., Kimbrel, Jeffrey A., Pett-Ridge, Jennifer, Kennedy, Peter G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469842/
https://www.ncbi.nlm.nih.gov/pubmed/37338274
http://dx.doi.org/10.1128/msystems.00390-23
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author Maillard, François
Michaud, Talia J.
See, Craig R.
DeLancey, Lang C.
Blazewicz, Steven J.
Kimbrel, Jeffrey A.
Pett-Ridge, Jennifer
Kennedy, Peter G.
author_facet Maillard, François
Michaud, Talia J.
See, Craig R.
DeLancey, Lang C.
Blazewicz, Steven J.
Kimbrel, Jeffrey A.
Pett-Ridge, Jennifer
Kennedy, Peter G.
author_sort Maillard, François
collection PubMed
description 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 (13)C and (15)N 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 (13)C and (15)N soil inputs. A taxonomically and functionally diverse array of bacteria and fungi was enriched in (13)C and/or (15)N 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. IMPORTANCE: Recent studies indicate that microbial dead cells, particularly those of fungi, play an important role in long-term carbon persistence in soils. Despite this growing recognition, how the resources within dead fungal cells (also known as fungal necromass) move into decomposer communities and soils are poorly quantified, particularly in studies based in natural environments. In this study, we found that the contribution of fungal necromass to soil carbon and nitrogen availability was slowed by the amount of melanin present in fungal cell walls. Further, despite the overall rapid acquisition of carbon and nitrogen from necromass by a diverse range of both bacteria and fungi, melanization also slowed microbial uptake of both elements. Collectively, our results indicate that melanization acts as a key ecological trait mediating not only fungal necromass decomposition rate, but also necromass carbon and nitrogen release into soil as well as microbial resource acquisition.
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spelling pubmed-104698422023-09-01 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. mSystems Research Article 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 (13)C and (15)N 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 (13)C and (15)N soil inputs. A taxonomically and functionally diverse array of bacteria and fungi was enriched in (13)C and/or (15)N 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. IMPORTANCE: Recent studies indicate that microbial dead cells, particularly those of fungi, play an important role in long-term carbon persistence in soils. Despite this growing recognition, how the resources within dead fungal cells (also known as fungal necromass) move into decomposer communities and soils are poorly quantified, particularly in studies based in natural environments. In this study, we found that the contribution of fungal necromass to soil carbon and nitrogen availability was slowed by the amount of melanin present in fungal cell walls. Further, despite the overall rapid acquisition of carbon and nitrogen from necromass by a diverse range of both bacteria and fungi, melanization also slowed microbial uptake of both elements. Collectively, our results indicate that melanization acts as a key ecological trait mediating not only fungal necromass decomposition rate, but also necromass carbon and nitrogen release into soil as well as microbial resource acquisition. American Society for Microbiology 2023-06-20 /pmc/articles/PMC10469842/ /pubmed/37338274 http://dx.doi.org/10.1128/msystems.00390-23 Text en Copyright © 2023 Maillard et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Maillard, François
Michaud, Talia J.
See, Craig R.
DeLancey, Lang C.
Blazewicz, Steven J.
Kimbrel, Jeffrey A.
Pett-Ridge, Jennifer
Kennedy, Peter G.
Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils
title Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils
title_full Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils
title_fullStr Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils
title_full_unstemmed Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils
title_short Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils
title_sort melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469842/
https://www.ncbi.nlm.nih.gov/pubmed/37338274
http://dx.doi.org/10.1128/msystems.00390-23
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