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Summer Research Project 2021

  • Title: Going Underground Sub-project 1: Fungal responses to soil warming and nitrogen fertilization
  • Group Project Leader: Serita Frey
  • Mentors: Nikhil Chari; Mallory Choudoir; Kristen DeAngelis; Serita Frey; Adriana Romero-Olivares
  • Collaborators: Melissa Knorr; Relena Ribbons
  • Project Description:

    This is part of the group project, ‘Going Underground: Unearthing the Role of the Soil Microbiome in a Warmer, Fertilized World,’ which has the following overarching theme:

    Rising temperatures and atmospheric nitrogen deposition pose a threat to the health of forests in the Northeastern US where Harvard Forest is located. Mean annual temperature in the region has increased 1.5 °F since 1970. Although rates of atmospheric nitrogen deposition in the region have declined in recent years, decades-long deposition at rates of 4 to >8 kg N ha-1 yr-1 has resulted in a legacy of nitrogen-enriched soils. Previous research at Harvard Forest has documented that chronic soil warming and increased nitrogen loads alter soil microbial communities and the biogeochemical processes they mediate. We are particularly interested in microbial controls on soil organic matter (SOM) dynamics. SOM is the primary source of plant-available nutrients in terrestrial ecosystems; thus, the maintenance of SOM levels is critical for forest sustainability. Soils also represent the largest repository of carbon (C) in the biosphere and are an important source of carbon dioxide (CO2) to the atmosphere via microbial decomposition of organic materials. The overarching goal of this project is to examine microbial responses to soil warming and simulated nitrogen deposition and to understand how soil microbes influence SOM formation and stabilization.

    Since this summer program will be virtual, students on this project will utilize existing datasets to ask questions related to the overarching theme. Students will work with their mentor(s) early in the program to develop a research question and approach that meets their interests and skillset. Students should indicate which sub-project is of most interest: (Sub-project 1) Fungal responses to soil warming and nitrogen fertilization; (Sub-project 2) Microbial controls on root exudate C pathways in soil; or (Sub-project 3) Bacterial genomic signatures of warming-accelerated soil C loss (see full descriptions below). Students will meet daily to weekly with their primary mentor(s). The entire project team will meet every two weeks as a larger group to hear from collaborators and discuss progress and challenges.

    Sub-project 1: Fungal responses to soil warming and nitrogen fertilization (2 students; Mentors: Serita Frey, Adriana Romero-Olivares)

    Soil fungi play key roles in C and nutrient cycles, as decomposers of SOM and symbionts of plants. They drive decomposition in temperate forests as the primary producers of the extracellular enzymes that break down lignin and cellulose, two of the most abundant compounds in plant biomass. Soil fungi are sensitive to environmental change, with shifts in the fungal community in response to global change drivers having significant consequences for soil C storage and feedbacks to climate through soil C loss. Previous research at Harvard Forest has examined fungal community responses to soil warming and simulated N deposition individually and in combination (e.g., Anthony et al. in press; Morrison et al., 2018). We have generated more than ten fungal sequence datasets that are each associated with a suite of soil biogeochemical parameters (i.e., soil moisture, temperature, pH, inorganic N, N mineralization, total organic C and N, soil respiration, SOM chemistry; litter mass loss and chemistry; microbial biomass, growth, and extracellular enzyme activity). What we have not yet done is compare datasets across studies to look for general patterns or unique features. We have observed in our published studies that (1) certain fungal taxa are indicator species for a particular global change driver, (2) that unique taxa are present in control versus treatment plots, and (3) that unknown fungal taxa (i.e., sequences that cannot be identified using existing databases) become significantly more abundant in response to warming, N addition, or their combination. The goal of this sub-project will be for two students to explore these datasets to determine if there are generalizations that can be made in terms of how different global change drivers alter fungal diversity, community composition and the relative abundance of individual taxa (including unknowns), and how shifts in the fungal community are linked to soil function, particularly soil C gain or loss.

    This synthesis will require that the biogeochemical and fungal sequence datasets for each study be combined into one large database. All the fungal sequence data have already been processed to generate operational taxonomic units (OTUs), and these OTUs have been identified to the genus or species level where possible. However, we will re-examine how each dataset was previously analyzed to confirm that all datasets were processed in a consistent way and if necessary, will reanalyze the full dataset to generate a comparable list of fungal taxa across all studies. Fungi that can be identified taxonomically will be assigned guild annotations using FUNGuild. From there, we will examine how individual global change drivers and their combination influence fungal biomass, diversity, community composition, individual taxa (including unknowns), and functional guilds (i.e., saprotrophs, symbiotrophs, pathotrophs). Multiple approaches will be used to analyze the data: Linear mixed effects models will be used to assess whether the main effects of N addition, warming, invasion and their combinations have a significant effect on soil biogeochemical properties and processes, and fungal biomass, diversity, community composition, and taxon and functional guild relative abundances. Cohen’s d effect size will be calculated as a qualitative assessment of treatment effects on OTU relative abundance. Indicator species analysis will be used to test for fungal OTUs that have a large positive or negative response to the global change treatments. Variation in fungal communities across the aggregated dataset will be assessed on OTU relative abundances converted to Bray-Curtis dissimilarities, and several statistical approaches will be used to examine multivariate treatment effects on fungal and biogeochemical parameters.

    We are looking for students excited about microbiome science, ecosystem ecology, and soils. Interest and motivation are the main requirements. Experience, aptitude, or at least strong interest in data analysis and bioinformatics is desirable. Students will be expected to help one another with the different sub-projects, gaining exposure to all aspects of the overall project, thus collegiality and teamwork are also important expectations.

  • Readings:

    Abs, Elsa,, Scott R. Saleska, Regis Ferriere. Microbial evolution reshapes soil carbon feedbacks to climate change. bioRxiv 641399; doi:

    Anthony, M., K. Stinson, J. Moore, and S.D. Frey. 2020. Fungal responses to plant invasion are greater under soil warming than simulated nitrogen deposition. Oecologia (in press).

    Keiluweit, M., J.J. Bougoure, P.S. Nico, J. Pett-Ridge, P.K. Weber, and M. Kleber. 2015. Mineral protection of soil carbon counteracted by root exudates. Nature Climate Change 5: 588-595.

    Lavallee, J.M., J.L. Soong, M.F. Cotrufo. 2020. Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century. Global Change Biology. 26(1): 261-273.

    Melillo, J.M., S.D. Frey, K.M. DeAngelis, W. Werner, M. Bernard, F.P. Bowles, G. Pold, M.A. Knorr, and A.S. Grandy. 2017. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358, 101-105.

    Morrison, E.W., A. Pringle, L.T.A. van Diepen, and S.D. Frey. 2018. Simulated nitrogen deposition favors stress-tolerant fungi with low potential for decomposition. Soil Biology & Biochemistry 125: 75-85.

    Phillips, R.P., Finzi, A.F., and Bernhardt, E.S. 2011. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecology Letters 14(2):187-194.

    Pold, G., Billings, A.F., Blanchard, J.L., Burkhardt, D.B., Frey, S.D., Melillo, J.M., Schnabel, J., van Diepen, L.T. and DeAngelis, K.M., 2016. Long-term warming alters carbohydrate degradation potential in temperate forest soils. Appl. Environ. Microbiol., 82(22), pp.6518-6530.

  • Research Category: Soil Carbon and Nitrogen Dynamics, Physiological Ecology, Population Dynamics, and Species Interactions, Large Experiments and Permanent Plot Studies, Group Projects