Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils
(2023) In mSystems 8(4).- Abstract
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... (More)
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. 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.
(Less)
- author
- Maillard, François LU ; Michaud, Talia J. ; See, Craig R. ; DeLancey, Lang C. ; Blazewicz, Steven J. ; Kimbrel, Jeffrey A. ; Pett-Ridge, Jennifer and Kennedy, Peter G.
- publishing date
- 2023-07
- type
- Contribution to journal
- publication status
- published
- keywords
- forests, fungi, KEYWORDS bacteria, quantitative stable-isotope probing, soil carbon and nitrogen cycling
- in
- mSystems
- volume
- 8
- issue
- 4
- article number
- e00390-23
- publisher
- American Society for Microbiology
- external identifiers
-
- scopus:85165172220
- pmid:37338274
- ISSN
- 2379-5077
- DOI
- 10.1128/msystems.00390-23
- language
- English
- LU publication?
- no
- additional info
- Publisher Copyright: Copyright © 2023 Maillard et al.
- id
- 6d92646f-9f10-4fc8-898f-4e96fb76a42f
- date added to LUP
- 2024-06-02 15:11:51
- date last changed
- 2024-06-16 15:52:38
@article{6d92646f-9f10-4fc8-898f-4e96fb76a42f,
abstract = {{<p>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 <sup>13</sup>C and <sup>15</sup>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 <sup>13</sup>C and <sup>15</sup>N soil inputs. A taxonomically and functionally diverse array of bacteria and fungi was enriched in <sup>13</sup>C and/or <sup>15</sup>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.</p>}},
author = {{Maillard, François and Michaud, Talia J. and See, Craig R. and DeLancey, Lang C. and Blazewicz, Steven J. and Kimbrel, Jeffrey A. and Pett-Ridge, Jennifer and Kennedy, Peter G.}},
issn = {{2379-5077}},
keywords = {{forests; fungi; KEYWORDS bacteria; quantitative stable-isotope probing; soil carbon and nitrogen cycling}},
language = {{eng}},
number = {{4}},
publisher = {{American Society for Microbiology}},
series = {{mSystems}},
title = {{Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils}},
url = {{http://dx.doi.org/10.1128/msystems.00390-23}},
doi = {{10.1128/msystems.00390-23}},
volume = {{8}},
year = {{2023}},
}