Soil nutrient amendment increases the potential for inter-kingdom resource competition among foliar endophytes

Authors: HANSEN, ZOE - University Of Minnesota; Fulcher, Michael; WORNSON, NICK - University Of Minnesota; SPAWN-LEE, SETH - University Of Wisconsin; JOHNSON, MITCH - University Of Minnesota; SONG, ZEWEI - University Of Minnesota; MICHALSKA-SMITH, MATTHEW - University Of Minnesota; MAY, GEORGIANA - University Of Minnesota; SEABLOOM, ERIC - University Of Minnesota; BORER, ELIZABETH - University Of Minnesota; KINKEL, LINDA - University Of Minnesota

Submitted to: ISME Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/24/2024
Publication Date: 11/13/2024
Citation: Hansen, Z.A., Fulcher, M.R., Wornson, N., Spawn-Lee, S.A., Johnson, M., Song, Z., Michalska-Smith, M.J., May, G., Seabloom, E.W., Borer, E.T., Kinkel, L.L. 2024. Soil nutrient amendment increases the potential for inter-kingdom resource competition among foliar endophytes. ISME Communications. https://doi.org/10.1093/ismeco/ycae130.
DOI: https://doi.org/10.1093/ismeco/ycae130

Interpretive Summary: Microbes that live within plant leaves contribute to large scale ecosystem processes including nutrient cycling and plant productivity. The redistribution of global nutrient supplies for agricultural and industrial purposes may alter the function of these communities, potentially impacting ecosystem stability. In this long-term study, continuous soil fertilization significantly altered the composition, function, and predicted interactions of microbes that inhabit a native prairie grass (big bluestem). The results suggest large-scale nutrient depositions influence the function of microbial communities contained within plants. Scientists studying the ecology and evolution of fungi and bacteria from plant tissue can use this information to predict changes in other microbial communities.

Technical Abstract: Foliar endophytes play crucial roles in large-scale ecosystem functions through their impacts on plant productivity, decomposition, and nutrient cycling. The possible effects of environmental nutrient supply on the growth and carbon use of endophytic microbes have critical implications for these processes. However, the impacts of soil nutrient supply on foliar endophytic community composition and function are not fully understood. Here, we examined the effects of long-term elevated supply of nitrogen, phosphorus, potassium, and micronutrients (NPKµ) on the taxonomic composition and carbon use phenotypes of bacterial and fungal foliar endophytes inhabiting the prairie grass Andropogon gerardii. We hypothesized that elevated soil nutrients (i) alter both taxonomic composition and carbon use profiles of foliar endophytes, and (ii) significantly shift niche overlap (a proxy for potential resource competition) among microbes within leaves. We observed slight changes in taxonomic composition and carbon use patterns of fungal, but not bacterial, endophytes of A. gerardii growing at high nutrient supply (NPKµ-amendment) versus ambient conditions. Fungal endophytes from plants experiencing NPKµ-amendment had significantly smaller niche widths and distinct carbon use profiles compared to those from control plots and demonstrated greater specialization across carbon sources. Niche overlap between bacterial and fungal endophytes increased with plot nutrient supply, suggesting increased potential for inter-kingdom resource competition. Collectively, this work shows that soil nutrient enrichment alters the composition and functional phenotypes of foliar fungal endophyte communities and substantially increases the potential for inter-kingdom resource competition among culturable bacterial and fungal endophytes.