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

Abstract

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.

Shifts in bacterial traits under chronic nitrogen deposition align with soil processes in arbuscular, but not ectomycorrhizal‐associated trees

“…More specifically, in AM soils, the majority of taxa had lower C and N assimilation under N deposition, producing lower CWM that mirrored the reductions in soil respiration and 15 N mineralization (Figures 2 and 4). The tight coupling between individual anabolism and soil‐level catabolic processes confirms the important role that bacteria play in soil functioning in AM soils (Carrara et al., 2021). This suggests that taxon‐specific C and N assimilation rates may be an appropriate measure to connect microbial communities with ecosystems functions (Malik et al., 2020; Morrissey et al., 2023).…”

“…In contrast, we did not see a similar agreement between CWM and soil process rates in ECM systems. The apparent decoupling between CWM traits and soil process in ECM soils may be because (1) the inclusion of fungi is necessary to connect microbial traits with soil process (either mycorrhiza or saprotrophs, Averill et al., 2014; Carrara et al., 2021); or (2) C and N use efficiencies differed among taxa, or in response to N deposition in the ECM soils. Under N deposition in the ECM soil, trait values were highly skewed (Figure 3) indicating a small number of taxa may have played a disproportionate role in C and N processing.…”

Habitat partitioning of soil microbial communities along an elevation gradient: from plant root to landscape scale

“…Furthermore, the three species selected in this study have different mycorrhizal associations, which will influence their contribution to bacterial and fungal community structures. As recently reported by Carrara et al (2021), AMF plants primarily depend on saprotrophic bacteria for mineral N acquisition, whereas in ECM/ERM hosts, most of the N uptake comes from organic pools and is carried out by fungal symbionts. These differences in resource acquisition strategies are likely to affect microbial communities in the rhizosphere niche, directly or indirectly through changes in litter chemistry (Cheeke et al 2017).…”

Applying molecular and genetic methods to trees and their fungal communities

“…Meta-transcriptomic analyses under long-term anthropogenic N deposition (over 16 years) into maple forest floors indicated significant shifts in fungal community expression of fungal CAZyme gene profiles under influence of N, along with increases in abundances of Ascomycta as compared to Basidiomycota (typically less prominent in abundance in forest soils than the ascomycetes; Chaithaisong et al 2022 ), decreases in expression of ligninolytic genes, and reduced litter decay in moderately decomposed O horizons (Hesse et al 2015 ). Shifts in hardwood forest ECM-species communities correlated with C and N cycling in N-fertilized forest soils, with enhanced relative C to N mining activities by ECM in rhizosphere soils and by AM-species in bulk soils (Carrara et al 2021 ). Long-term soil warming in a boreal Picea mariana forest resulted in changed fungal soil communities with more stress-tolerant taxa and allocation of their carbon resources to fungal cell metabolic maintenance at expense of litter decomposition (Romero-Olivares et al 2019 ).…”