Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi

Elizabeth M. Entwistle, Donald R. Zak, William A. Argiroff

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66 Scopus citations

Abstract

Atmospheric nitrogen (N) deposition has increased dramatically since preindustrial times and continues to increase across many regions of the Earth. In temperate forests, this agent of global change has increased soil carbon (C) storage, but the mechanisms underlying this response are not understood. One long-standing hypothesis proposed to explain the accumulation of soil C proposes that higher inorganic N availability may suppress both the activity and abundance of fungi that decay lignin and other polyphenols in soil. In field studies, elevated rates of N deposition have reduced the activity of enzymes mediating lignin decay, but a decline in the abundance of lignolytic fungi has not been definitively documented to date. Here, we tested the hypothesis that elevated rates of anthropogenic N deposition reduce the abundance of lignolytic fungi. We conducted a field experiment in which we compared fungal communities colonizing low-lignin, high-lignin, and wood substrates in a northern hardwood forest that is part of a long-term N deposition experiment. We reasoned that if lignolytic fungi decline under experimental N deposition, this effect should be most evident among fungi colonizing high-lignin and wood substrates. Using molecular approaches, we provide evidence that anthropogenic N deposition reduces the relative abundance of lignolytic fungi on both wood and a high-lignin substrate. Furthermore, experimental N deposition increased total fungal abundance on a low-lignin substrate, reduced fungal abundance on wood, and had no significant effect on fungal abundance on a high-lignin substrate. We simultaneously examined these responses in the surrounding soil and forest floor, in which we did not observe significant reductions in the relative abundance of lignolytic fungi or in the size of the fungal community; however, we did detect a change in community composition in the forest floor that appears to be driven by a shift away from lignolytic fungi and towards cellulolytic fungi. Our results provide direct evidence that reductions in the abundance of lignolytic fungi are part of the mechanism by which anthropogenic N deposition increases soil C storage.

Original languageEnglish
Pages (from-to)225-244
Number of pages20
JournalEcological Monographs
Volume88
Issue number2
DOIs
StatePublished - May 2018
Externally publishedYes

Funding

This work was supported by funding from the United States Department of Energy Biological and Environmental Research program. Maintenance of our long-term N deposition project is supported by the National Science Foundation Long-term Research in Environmental Biology program. Donald Zak, along with collaborators, established the Michigan Gradient Project and has overseen the continuation of this long-term research project since 1994. Elizabeth Entwistle and Donald Zak co-designed the field experiment presented in this manuscript. As principal investigator on this project, Donald Zak conceived the larger project funding this particular piece of research, provided intellectual input throughout this project, and edited drafts of this manuscript. Elizabeth Entwistle created the protocols for DNA extraction and sequencing, performed the bioinformatic and statistical analyses, and wrote the manuscript. William Argiroff created standards, optimized, performed, and assembled the data for quantitative PCR. He also was heavily involved in fungal community PCR and sequencing efforts and designed our protocol for cleaning up PCR products. The authors would like to acknowledge the invaluable assistance of several people. Rima Upchurch assisted with litter bag assembly and deployment. Seongjun Kim assisted with mass loss measurements and sample processing. Karl Romanowicz and Andrew Warner extracted DNA from our samples. We thank them for their important roles in this project. We also thank Drs. Lauren Cline, Gregory Dick, Timothy James, and Inés Ibánez for their feedback on earlier versions of this manuscript.

FundersFunder number
National Science Foundation Long-Term Research in Environmental Biology Program
United States Department of Energy Biological and Environmental Research program
National Science Foundation1251529

    Keywords

    • Agaricomycetes
    • atmospheric N deposition
    • decomposition
    • forest
    • forest floor
    • fungal communities
    • fungi
    • lignin
    • nitrogen
    • soil C
    • soil organic matter

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