Fungal community composition and genetic potential regulate fine root decay in northern temperate forests

William A. Argiroff, Donald R. Zak, Rima A. Upchurch, Peter T. Pellitier, Julia P. Belke

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

Abstract

Understanding how genetic differences among soil microorganisms regulate spatial patterns in litter decay remains a persistent challenge in ecology. Despite fine root litter accounting for ~50% of total litter production in forest ecosystems, far less is known about the microbial decay of fine roots relative to aboveground litter. Here, we evaluated whether fine root decay occurred more rapidly where fungal communities have a greater genetic potential for litter decay. Additionally, we tested if linkages between decay and fungal genes can be adequately captured by delineating saprotrophic and ectomycorrhizal fungal functional groups based on whether they have genes encoding certain ligninolytic class II peroxidase enzymes, which oxidize lignin and polyphenolic compounds. To address these ideas, we used a litterbag study paired with fungal DNA barcoding to characterize fine root decay rates and fungal community composition at the landscape scale in northern temperate forests, and we estimated the genetic potential of fungal communities for litter decay using publicly available genomes. Fine root decay occurred more rapidly where fungal communities had a greater genetic potential for decay, especially of cellulose and hemicellulose. Fine root decay was positively correlated with ligninolytic saprotrophic fungi and negatively correlated with ECM fungi with ligninolytic peroxidases, likely because these saprotrophic and ectomycorrhizal functional groups had the highest and lowest genetic potentials for plant cell wall degradation, respectively. These fungal variables overwhelmed direct environmental controls, suggesting fungal community composition and genetic variation are primary controls over fine root decay in temperate forests at regional scales.

Original languageEnglish
Pages (from-to)2005-2021
Number of pages17
JournalMolecular Ecology
Volume32
Issue number8
DOIs
StatePublished - Apr 2023
Externally publishedYes

Funding

We are grateful to Nisha Gudal, Liberty Woodside, Melissa Chen, Noor Ahmad, and Catherine Seguin for assistance with fine root processing. We also thank Diana Saum, Kirk Acharya, Samuel Schaffer‐Morrison, Jordan Matthews, Edith Juno, and Gwendolen Keller for field assistance. We thank Stuart Grandy for py‐GC/MS analysis of fine root samples. We are grateful to Deborah Goldberg and Inés Ibáñez for helpful comments on earlier versions of this manuscript, including insightful ideas about statistical analyses and conceptual framing. We also thank Timothy James for valuable comments on previous drafts of this manuscript and assistance with ITS2 barcoded primer protocols. We thank Christopher Blair, Christina Cartaciano, and Thomas Schmidt at the University of Michigan Microbiome Core for ITS2 sequencing. We are very grateful to Beth VanDusen and Jennifer Wen for assistance with characterization of soil chemistry, as well as Ojen's Alterations for litter bag construction. We also thank three anonymous reviewers for their constructive and insightful feedback on previous versions of this manuscript. This work was funded by the National Science Foundation, the School for Environment and Sustainability, and the University of Michigan Rackham Graduate School at the University of Michigan.

Keywords

  • ectomycorrhizal fungi
  • genes
  • lignin
  • plant cell wall degrading enzymes
  • plant litter decomposition
  • saprotrophic fungi

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