Nitrogen cycling microbiomes are structured by plant mycorrhizal associations with consequences for nitrogen oxide fluxes in forests

Ryan M. Mushinski, Zachary C. Payne, Jonathan D. Raff, Matthew E. Craig, Sally E. Pusede, Douglas B. Rusch, Jeffrey R. White, Richard P. Phillips

Research output: Contribution to journalArticlepeer-review

45 Scopus citations

Abstract

Volatile nitrogen oxides (N2O, NO, NO2, HONO, …) can negatively impact climate, air quality, and human health. Using soils collected from temperate forests across the eastern United States, we show microbial communities involved in nitrogen (N) cycling are structured, in large part, by the composition of overstory trees, leading to predictable N-cycling syndromes, with consequences for emissions of volatile nitrogen oxides to air. Trees associating with arbuscular mycorrhizal (AM) fungi promote soil microbial communities with higher N-cycle potential and activity, relative to microbial communities in soils dominated by trees associating with ectomycorrhizal (ECM) fungi. Metagenomic analysis and gene expression studies reveal a 5 and 3.5 times greater estimated N-cycle gene and transcript copy numbers, respectively, in AM relative to ECM soil. Furthermore, we observe a 60% linear decrease in volatile reactive nitrogen gas flux (NOy ≡ NO, NO2, HONO) as ECM tree abundance increases. Compared to oxic conditions, gas flux potential of N2O and NO increase significantly under anoxic conditions for AM soil (30- and 120-fold increase), but not ECM soil—likely owing to small concentrations of available substrate ((Formula presented.)) in ECM soil. Linear mixed effects modeling shows that ECM tree abundance, microbial process rates, and geographic location are primarily responsible for variation in peak potential NOy flux. Given that nearly all tree species associate with either AM or ECM fungi, our results indicate that the consequences of tree species shifts associated with global change may have predictable consequences for soil N cycling.

Original languageEnglish
Pages (from-to)1068-1082
Number of pages15
JournalGlobal Change Biology
Volume27
Issue number5
DOIs
StatePublished - Mar 2021

Funding

We thank John Poehlman, Jeremy Boshears, and colleagues in Indiana University Chemistry's Engineering and Technical Groups for help designing and building the automated chamber sampling system used in this study. We also thank Meghan Midgley for establishing the Moores Creek research plots at Indiana University's Research and Teaching Preserve (funded by Agriculture and Food Research Initiative Competitive Grant 2013‐67011‐21095 from the US Department of Agriculture National Institute of Food and Agriculture) as well as Laura Podzikowski, Mark Sheehan, Katilyn Beidler, and Elizabeth Huenupi for maintaining and fertilizing the Moores Creek plots since 2015. We also thank Edward Brzostek and his lab at West Virginia University for assistance in sampling the 54 gradient plots. Sequencing support was provided by the US Department of Energy Joint Genome Institute (JGI), a DOE Office of Science User Facility, which is supported by the Office of Science of the United States Department of Energy under Contract No. DE‐AC02‐05CH11231. We especially thank the staff at the JGI, including Nicole Shapiro and Natalia Ivanova for assistance with sequencing and bioinformatic analyses. We also thank Ayumi Hyodo and the Stable Isotopes for Biosphere Sciences laboratory at Texas A&M University for help with soil elemental analysis. Financial support for this study came from the US Department of Energy, Office of Science, Early Career Research Program from Subsurface Biogeochemical Research Program (Award DE‐SC0014443 to J.D.R.). R.M.M. was supported by Indiana University's Integrated Program in the Environment and the O'Neill School of Public and Environmental Affairs as well as a postdoctoral fellowship from the US Department of Agriculture National Institute of Food and Agriculture (grant no. 2018‐08037). Z.C.P. was supported by NSF Grant AGS‐1352375. M.E.C was supported by Oak Ridge National Laboratory, which is operated by UT‐Battelle, LLC, under contract DE‐AC05‐00OR22725 with the United States Department of Energy. We also thank Peter Homyak and an anonymous reviewer for extremely helpful feedback.

FundersFunder number
O'Neill School of Public and Environmental Affairs2018‐08037
Office of Science of the United States Department of EnergyDE‐AC02‐05CH11231
US Department of Energy Joint Genome Institute
National Science FoundationAGS‐1352375
U.S. Department of Energy
National Institute of Food and Agriculture
Office of ScienceDE‐SC0014443
Oak Ridge National LaboratoryDE‐AC05‐00OR22725
Indiana University2013‐67011‐21095
Joint Genome Institute

    Keywords

    • forest soils
    • metagenomes
    • mycorrhizae
    • nitrogen cycle
    • nitrous oxide
    • reactive nitrogen oxides

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