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Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests

Carbon storage and cycling in boreal forests—the largest terrestrial carbon store—is moderated by complex interactions between trees and soil microorganisms. However, existing methods limit our ability to predict how changes in environmental conditions will alter these associations and the essential...

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Autores principales: Law, Simon R., Serrano, Alonso R., Daguerre, Yohann, Sundh, John, Schneider, Andreas N., Stangl, Zsofia R., Castro, David, Grabherr, Manfred, Näsholm, Torgny, Street, Nathaniel R., Hurry, Vaughan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9245616/
https://www.ncbi.nlm.nih.gov/pubmed/35727987
http://dx.doi.org/10.1073/pnas.2118852119
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author Law, Simon R.
Serrano, Alonso R.
Daguerre, Yohann
Sundh, John
Schneider, Andreas N.
Stangl, Zsofia R.
Castro, David
Grabherr, Manfred
Näsholm, Torgny
Street, Nathaniel R.
Hurry, Vaughan
author_facet Law, Simon R.
Serrano, Alonso R.
Daguerre, Yohann
Sundh, John
Schneider, Andreas N.
Stangl, Zsofia R.
Castro, David
Grabherr, Manfred
Näsholm, Torgny
Street, Nathaniel R.
Hurry, Vaughan
author_sort Law, Simon R.
collection PubMed
description Carbon storage and cycling in boreal forests—the largest terrestrial carbon store—is moderated by complex interactions between trees and soil microorganisms. However, existing methods limit our ability to predict how changes in environmental conditions will alter these associations and the essential ecosystem services they provide. To address this, we developed a metatranscriptomic approach to analyze the impact of nutrient enrichment on Norway spruce fine roots and the community structure, function, and tree–microbe coordination of over 350 root-associated fungal species. In response to altered nutrient status, host trees redefined their relationship with the fungal community by reducing sugar efflux carriers and enhancing defense processes. This resulted in a profound restructuring of the fungal community and a collapse in functional coordination between the tree and the dominant Basidiomycete species, and an increase in functional coordination with versatile Ascomycete species. As such, there was a functional shift in community dominance from Basidiomycetes species, with important roles in enzymatically cycling recalcitrant carbon, to Ascomycete species that have melanized cell walls that are highly resistant to degradation. These changes were accompanied by prominent shifts in transcriptional coordination between over 60 predicted fungal effectors, with more than 5,000 Norway spruce transcripts, providing mechanistic insight into the complex molecular dialogue coordinating host trees and their fungal partners. The host–microbe dynamics captured by this study functionally inform how these complex and sensitive biological relationships may mediate the carbon storage potential of boreal soils under changing nutrient conditions.
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spelling pubmed-92456162022-07-01 Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests Law, Simon R. Serrano, Alonso R. Daguerre, Yohann Sundh, John Schneider, Andreas N. Stangl, Zsofia R. Castro, David Grabherr, Manfred Näsholm, Torgny Street, Nathaniel R. Hurry, Vaughan Proc Natl Acad Sci U S A Biological Sciences Carbon storage and cycling in boreal forests—the largest terrestrial carbon store—is moderated by complex interactions between trees and soil microorganisms. However, existing methods limit our ability to predict how changes in environmental conditions will alter these associations and the essential ecosystem services they provide. To address this, we developed a metatranscriptomic approach to analyze the impact of nutrient enrichment on Norway spruce fine roots and the community structure, function, and tree–microbe coordination of over 350 root-associated fungal species. In response to altered nutrient status, host trees redefined their relationship with the fungal community by reducing sugar efflux carriers and enhancing defense processes. This resulted in a profound restructuring of the fungal community and a collapse in functional coordination between the tree and the dominant Basidiomycete species, and an increase in functional coordination with versatile Ascomycete species. As such, there was a functional shift in community dominance from Basidiomycetes species, with important roles in enzymatically cycling recalcitrant carbon, to Ascomycete species that have melanized cell walls that are highly resistant to degradation. These changes were accompanied by prominent shifts in transcriptional coordination between over 60 predicted fungal effectors, with more than 5,000 Norway spruce transcripts, providing mechanistic insight into the complex molecular dialogue coordinating host trees and their fungal partners. The host–microbe dynamics captured by this study functionally inform how these complex and sensitive biological relationships may mediate the carbon storage potential of boreal soils under changing nutrient conditions. National Academy of Sciences 2022-06-21 2022-06-28 /pmc/articles/PMC9245616/ /pubmed/35727987 http://dx.doi.org/10.1073/pnas.2118852119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Law, Simon R.
Serrano, Alonso R.
Daguerre, Yohann
Sundh, John
Schneider, Andreas N.
Stangl, Zsofia R.
Castro, David
Grabherr, Manfred
Näsholm, Torgny
Street, Nathaniel R.
Hurry, Vaughan
Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests
title Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests
title_full Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests
title_fullStr Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests
title_full_unstemmed Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests
title_short Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests
title_sort metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9245616/
https://www.ncbi.nlm.nih.gov/pubmed/35727987
http://dx.doi.org/10.1073/pnas.2118852119
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