Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization

Joseph E. Carrara, Christopher A. Walter, Jennifer S. Hawkins, William T. Peterjohn, Colin Averill, Edward R. Brzostek

Research output: Contribution to journalArticlepeer-review

96 Scopus citations


Atmospheric nitrogen (N) deposition has enhanced soil carbon (C) stocks in temperate forests. Most research has posited that these soil C gains are driven primarily by shifts in fungal community composition with elevated N leading to declines in lignin degrading Basidiomycetes. Recent research, however, suggests that plants and soil microbes are dynamically intertwined, whereby plants send C subsidies to rhizosphere microbes to enhance enzyme production and the mobilization of N. Thus, under elevated N, trees may reduce belowground C allocation leading to cascading impacts on the ability of microbes to degrade soil organic matter through a shift in microbial species and/or a change in plant–microbe interactions. The objective of this study was to determine the extent to which couplings among plant, fungal, and bacterial responses to N fertilization alter the activity of enzymes that are the primary agents of soil decomposition. We measured fungal and bacterial community composition, root–microbial interactions, and extracellular enzyme activity in the rhizosphere, bulk, and organic horizon of soils sampled from a long-term (>25 years), whole-watershed, N fertilization experiment at the Fernow Experimental Forest in West Virginia, USA. We observed significant declines in plant C investment to fine root biomass (24.7%), root morphology, and arbuscular mycorrhizal (AM) colonization (55.9%). Moreover, we found that declines in extracellular enzyme activity were significantly correlated with a shift in bacterial community composition, but not fungal community composition. This bacterial community shift was also correlated with reduced AM fungal colonization indicating that declines in plant investment belowground drive the response of bacterial community structure and function to N fertilization. Collectively, we find that enzyme activity responses to N fertilization are not solely driven by fungi, but instead reflect a whole ecosystem response, whereby declines in the strength of belowground C investment to gain N cascade through the soil environment.

Original languageEnglish (US)
Pages (from-to)2721-2734
Number of pages14
JournalGlobal change biology
Issue number6
StatePublished - Jun 2018

Bibliographical note

Funding Information:
We acknowledge Mary Beth Adams, Tom Schuler, and the US Forest Service staff at the Fernow Experimental Forest for logistical assistance and access to the experimental watersheds and the LTSP site. This work was also supported by the National Science Foundation Graduate Research Fellowship to Joseph Carrara under Grant No. DGE-1102689, and by the Long-Term Research in Environmental Biology (LTREB) program at the National Science Foundation (Grant Nos. DEB-0417678 and DEB-1019522) to William Peterjohn. Colin Averill was supported by the NOAA Climate and Global Change Postdoctoral Fellowship Program, administered by Cooperative Programs for the Advancement of Earth System Science (CPAESS), University Corporation for Atmospheric Research (UCAR), Boulder, Colorado, USA. We acknowledge the WVU Genomics Core Facility, Morgantown WV for support provided to help make this publication possible. We also thank Leah Baldinger, Brittany Carver, Mark Burnham, Hannah Hedrick, Jennifer Mangano, and Catherine Sesa for assistance in the field and in the laboratory.

Publisher Copyright:
© 2018 John Wiley & Sons Ltd


  • arbuscular mycorrhizal fungi
  • belowground carbon allocation
  • extracellular enzymes
  • microbial community
  • nitrogen fertilization
  • plant–microbial interactions


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