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Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition

Forests accumulate and store large amounts of carbon (C), and a substantial fraction of this stock is contained in deadwood. This transient pool is subject to decomposition by deadwood-associated organisms, and in this process it contributes to CO(2) emissions. Although fungi and bacteria are known...

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Autores principales: Tláskal, Vojtěch, Brabcová, Vendula, Větrovský, Tomáš, Jomura, Mayuko, López-Mondéjar, Rubén, Oliveira Monteiro, Lummy Maria, Saraiva, João Pedro, Human, Zander Rainier, Cajthaml, Tomáš, Nunes da Rocha, Ulisses, Baldrian, Petr
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7901482/
https://www.ncbi.nlm.nih.gov/pubmed/33436515
http://dx.doi.org/10.1128/mSystems.01078-20
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author Tláskal, Vojtěch
Brabcová, Vendula
Větrovský, Tomáš
Jomura, Mayuko
López-Mondéjar, Rubén
Oliveira Monteiro, Lummy Maria
Saraiva, João Pedro
Human, Zander Rainier
Cajthaml, Tomáš
Nunes da Rocha, Ulisses
Baldrian, Petr
author_facet Tláskal, Vojtěch
Brabcová, Vendula
Větrovský, Tomáš
Jomura, Mayuko
López-Mondéjar, Rubén
Oliveira Monteiro, Lummy Maria
Saraiva, João Pedro
Human, Zander Rainier
Cajthaml, Tomáš
Nunes da Rocha, Ulisses
Baldrian, Petr
author_sort Tláskal, Vojtěch
collection PubMed
description Forests accumulate and store large amounts of carbon (C), and a substantial fraction of this stock is contained in deadwood. This transient pool is subject to decomposition by deadwood-associated organisms, and in this process it contributes to CO(2) emissions. Although fungi and bacteria are known to colonize deadwood, little is known about the microbial processes that mediate carbon and nitrogen (N) cycling in deadwood. In this study, using a combination of metagenomics, metatranscriptomics, and nutrient flux measurements, we demonstrate that the decomposition of deadwood reflects the complementary roles played by fungi and bacteria. Fungi were found to dominate the decomposition of deadwood and particularly its recalcitrant fractions, while several bacterial taxa participate in N accumulation in deadwood through N fixation, being dependent on fungal activity with respect to deadwood colonization and C supply. Conversely, bacterial N fixation helps to decrease the constraints of deadwood decomposition for fungi. Both the CO(2) efflux and N accumulation that are a result of a joint action of deadwood bacteria and fungi may be significant for nutrient cycling at ecosystem levels. Especially in boreal forests with low N stocks, deadwood retention may help to improve the nutritional status and fertility of soils. IMPORTANCE Wood represents a globally important stock of C, and its mineralization importantly contributes to the global C cycle. Microorganisms play a key role in deadwood decomposition, since they possess enzymatic tools for the degradation of recalcitrant plant polymers. The present paradigm is that fungi accomplish degradation while commensalist bacteria exploit the products of fungal extracellular enzymatic cleavage, but this assumption was never backed by the analysis of microbial roles in deadwood. This study clearly identifies the roles of fungi and bacteria in the microbiome and demonstrates the importance of bacteria and their N fixation for the nutrient balance in deadwood as well as fluxes at the ecosystem level. Deadwood decomposition is shown as a process where fungi and bacteria play defined, complementary roles.
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spelling pubmed-79014822021-02-24 Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition Tláskal, Vojtěch Brabcová, Vendula Větrovský, Tomáš Jomura, Mayuko López-Mondéjar, Rubén Oliveira Monteiro, Lummy Maria Saraiva, João Pedro Human, Zander Rainier Cajthaml, Tomáš Nunes da Rocha, Ulisses Baldrian, Petr mSystems Research Article Forests accumulate and store large amounts of carbon (C), and a substantial fraction of this stock is contained in deadwood. This transient pool is subject to decomposition by deadwood-associated organisms, and in this process it contributes to CO(2) emissions. Although fungi and bacteria are known to colonize deadwood, little is known about the microbial processes that mediate carbon and nitrogen (N) cycling in deadwood. In this study, using a combination of metagenomics, metatranscriptomics, and nutrient flux measurements, we demonstrate that the decomposition of deadwood reflects the complementary roles played by fungi and bacteria. Fungi were found to dominate the decomposition of deadwood and particularly its recalcitrant fractions, while several bacterial taxa participate in N accumulation in deadwood through N fixation, being dependent on fungal activity with respect to deadwood colonization and C supply. Conversely, bacterial N fixation helps to decrease the constraints of deadwood decomposition for fungi. Both the CO(2) efflux and N accumulation that are a result of a joint action of deadwood bacteria and fungi may be significant for nutrient cycling at ecosystem levels. Especially in boreal forests with low N stocks, deadwood retention may help to improve the nutritional status and fertility of soils. IMPORTANCE Wood represents a globally important stock of C, and its mineralization importantly contributes to the global C cycle. Microorganisms play a key role in deadwood decomposition, since they possess enzymatic tools for the degradation of recalcitrant plant polymers. The present paradigm is that fungi accomplish degradation while commensalist bacteria exploit the products of fungal extracellular enzymatic cleavage, but this assumption was never backed by the analysis of microbial roles in deadwood. This study clearly identifies the roles of fungi and bacteria in the microbiome and demonstrates the importance of bacteria and their N fixation for the nutrient balance in deadwood as well as fluxes at the ecosystem level. Deadwood decomposition is shown as a process where fungi and bacteria play defined, complementary roles. American Society for Microbiology 2021-01-12 /pmc/articles/PMC7901482/ /pubmed/33436515 http://dx.doi.org/10.1128/mSystems.01078-20 Text en Copyright © 2021 Tláskal 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
Tláskal, Vojtěch
Brabcová, Vendula
Větrovský, Tomáš
Jomura, Mayuko
López-Mondéjar, Rubén
Oliveira Monteiro, Lummy Maria
Saraiva, João Pedro
Human, Zander Rainier
Cajthaml, Tomáš
Nunes da Rocha, Ulisses
Baldrian, Petr
Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition
title Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition
title_full Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition
title_fullStr Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition
title_full_unstemmed Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition
title_short Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition
title_sort complementary roles of wood-inhabiting fungi and bacteria facilitate deadwood decomposition
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7901482/
https://www.ncbi.nlm.nih.gov/pubmed/33436515
http://dx.doi.org/10.1128/mSystems.01078-20
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