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Research article2022Peer reviewedOpen access

Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests

Law, Simon; Serrano, Alonso; Daguerre, Yohann; Sundh, John; Schneider, Andreas N.; Stangl, Zsofia Réka; Stangl , Zsofia Reka; Castro, David; Grabherr, Manfred G.; Näsholm, Torgny; Street, Nathaniel R.; Hurry, Vaughan

Abstract

Carbon storage and cycling in boreal forests—the largest terrestrial carbon store—ismoderated by complex interactions between trees and soil microorganisms. However,existing methods limit our ability to predict how changes in environmental conditionswill alter these associations and the essential ecosystem services they provide. To addressthis, we developed a metatranscriptomic approach to analyze the impact of nutrientenrichment on Norway sprucefine roots and the community structure, function, andtree–microbe coordination of over 350 root-associated fungal species. In response toaltered nutrient status, host trees redefined their relationship with the fungal commu-nity by reducing sugar efflux carriers and enhancing defense processes. This resulted ina profound restructuring of the fungal community and a collapse in functional coordi-nation between the tree and the dominant Basidiomycete species, and an increase infunctional coordination with versatile Ascomycete species. As such, there was a func-tional  shift  in  community  dominance  from  Basidiomycetes  species,  with  importantroles in enzymatically cycling recalcitrant carbon, to Ascomycete species that have mela-nized cell walls that are highly resistant to degradation. These changes were accompa-nied  by  prominent  shifts  in  transcriptional  coordination  between  over  60  predictedfungal effectors, with more than 5,000 Norway spruce transcripts, providing mechanis-tic insight into the complex molecular dialogue coordinating host trees and their fungalpartners. The host–microbe dynamics captured by this study functionally inform howthese complex and  sensitive biological  relationships may mediate  the carbon  storagepotential of boreal soils under changing nutrient conditions.

Keywords

metatranscriptome; host–microbe; ectomycorrhiza; carbon storage; fungal effectors

Published in

Proceedings of the National Academy of Sciences of the United States of America
2022, Volume: 119, number: 26, article number: e2118852119