Differences in microbial community response to nitrogen fertilization result in unique enzyme shifts between arbuscular and ectomycorrhizal‐dominated soils

• Published in: Global change biology Vol. 27; no. 10; pp. 2049 - 2060
• Main Authors: Carrara, Joseph E., Walter, Christopher A., Freedman, Zachary B., Hostetler, Ashley N., Hawkins, Jennifer S., Fernandez, Ivan J., Brzostek, Edward R.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01-05-2021
• Subjects: arbuscular mycorrhizal fungi; Arbuscular mycorrhizas; Bacteria; Biological fertilization; Carbon cycle; Community composition; Composition; Cycles; Deposition; ectomycorrhizal fungi; Ectomycorrhizas; Enzymatic activity; Enzyme activity; Enzymes; Extracellular; extracellular enzymes; Extracellular matrix; Fertilization; Forest soils; Fungi; Maine; metatranscriptomics; microbial community; Microbiomes; Microbiota; Microorganisms; Mining; Mycorrhizae; Nitrogen; nitrogen fertilization; Nutrient cycles; Organic matter; Organic soils; Rhizosphere; Soil; Soil Microbiology; Soil microorganisms; Soil organic matter; Soil testing; Soils; Trees; Watersheds; Maine; nitrogen fertilization; microbial community; arbuscular mycorrhizal fungi; extracellular enzymes; metatranscriptomics; ectomycorrhizal fungi
• ISSN: 1354-1013; 1365-2486
• DOI: 10.1111/gcb.15523

While the effect of nitrogen (N) deposition on belowground carbon (C) cycling varies, emerging evidence shows that forest soils dominated by trees that associate with ectomycorrhizal fungi (ECM) store more C than soils dominated by trees that associate with arbuscular mycorrhizae (AM) with increasing N deposition. We hypothesized that this is due to unique nutrient cycling responses to N between AM and ECM‐dominated soils. ECM trees primarily obtain N through fungal mining of soil organic matter subsidized by root‐C. As such, we expected the largest N‐induced responses of C and N cycling to occur in ECM rhizospheres and be driven by fungi. Conversely, as AM trees rely on bacterial scavengers in bulk soils to cycle N, we predicted the largest AM responses to be driven by shifts in bacteria and occur in bulk soils. To test this hypothesis, we measured microbial community composition, metatranscriptome profiles, and extracellular enzyme activity in bulk, rhizosphere, and organic horizon (OH) soils in AM and ECM‐dominated soils at Bear Brook Watershed in Maine, USA. After 27 years of N fertilization, fungal community composition shifted across ECM soils, but bacterial communities shifted across AM soils. These shifts were mirrored by enhanced C relative to N mining enzyme activities in both mycorrhizal types, but this occurred in different soil fractions. In ECM stands these shifts occurred in rhizosphere soils, but in AM stands they occurred in bulk soils. Additionally, ECM OH soils exhibited the opposite response with declines in C relative to N mining. As rhizosphere soils account for only a small portion of total soil volume relative to bulk soils, coupled with declines in C to N enzyme activity in ECM OH soils, we posit that this may partly explain why ECM soils store more C than AM soils as N inputs increase.
Long‐term nitrogen fertilization shifted soil bacterial community composition in forest stands dominated by trees that associate with arbuscular mycorrhizae (AM), but shifted fungal community composition in stands dominated by trees that associate with ectomycorrhizae (ECM). These unique microbial community changes were coupled with enhanced carbon relative to nitrogen mining enzyme activities in AM bulk soils and ECM rhizosphere soils. These mycorrhizal type‐specific responses to long‐term nitrogen fertilization may help to explain variability in soil carbon responses across nitrogen fertilization and observational studies.