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

ABSTRACT 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 CO2 emissions. Although fungi and bacteria are...

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Autores principales:	Vojtěch Tláskal, Vendula Brabcová, Tomáš Větrovský, Mayuko Jomura, Rubén López-Mondéjar, Lummy Maria Oliveira Monteiro, João Pedro Saraiva, Zander Rainier Human, Tomáš Cajthaml, Ulisses Nunes da Rocha, Petr Baldrian
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	bacteria deadwood decomposition forest ecosystems fungi metatranscriptomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d3294a94e14f400184261ed37a16311b
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spelling	oai:doaj.org-article:d3294a94e14f400184261ed37a16311b2021-12-02T19:22:16ZComplementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition10.1128/mSystems.01078-202379-5077https://doaj.org/article/d3294a94e14f400184261ed37a16311b2021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01078-20https://doaj.org/toc/2379-5077ABSTRACT 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 CO2 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 CO2 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.Vojtěch TláskalVendula BrabcováTomáš VětrovskýMayuko JomuraRubén López-MondéjarLummy Maria Oliveira MonteiroJoão Pedro SaraivaZander Rainier HumanTomáš CajthamlUlisses Nunes da RochaPetr BaldrianAmerican Society for Microbiologyarticlebacteriadeadwooddecompositionforest ecosystemsfungimetatranscriptomicsMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacteria deadwood decomposition forest ecosystems fungi metatranscriptomics Microbiology QR1-502
spellingShingle	bacteria deadwood decomposition forest ecosystems fungi metatranscriptomics Microbiology QR1-502 Vojtěch Tláskal Vendula Brabcová Tomáš Větrovský Mayuko Jomura Rubén López-Mondéjar Lummy Maria Oliveira Monteiro João Pedro Saraiva Zander Rainier Human Tomáš Cajthaml Ulisses Nunes da Rocha Petr Baldrian Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition
description	ABSTRACT 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 CO2 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 CO2 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.
format	article
author	Vojtěch Tláskal Vendula Brabcová Tomáš Větrovský Mayuko Jomura Rubén López-Mondéjar Lummy Maria Oliveira Monteiro João Pedro Saraiva Zander Rainier Human Tomáš Cajthaml Ulisses Nunes da Rocha Petr Baldrian
author_facet	Vojtěch Tláskal Vendula Brabcová Tomáš Větrovský Mayuko Jomura Rubén López-Mondéjar Lummy Maria Oliveira Monteiro João Pedro Saraiva Zander Rainier Human Tomáš Cajthaml Ulisses Nunes da Rocha Petr Baldrian
author_sort	Vojtěch Tláskal
title	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_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_sort	complementary roles of wood-inhabiting fungi and bacteria facilitate deadwood decomposition
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/d3294a94e14f400184261ed37a16311b
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Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition

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