期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：26
DOI：10.1073/pnas.2118852119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Advances in DNA sequencing have provided an unprecedented view of the complex microbial communities that populate global ecosystems. We present a metatranscriptomic analysis of samples from the boreal forest—the largest terrestrial carbon store—capturing the seasonally resolved transcriptomes of Norway spruce roots and more than 350 root-associated fungal species. Our findings link the functional response of host-trees to increased nutrient availability, with profound perturbations in the fungal community. Notably, we observed an exchange in prevalence and host-coordination of specialist ectomycorrhizal species critical for enzymatic cycling of recalcitrant carbon, to metabolically versatile species with resilient melanized cell walls. This research unites kingdom-spanning taxonomic and functional details of the boreal root microbiome, contributing a missing perspective toward modeling global carbon cycling.
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.
