Climate drivers alter nitrogen availability in surface peat and decouple N₂ fixation from CH₄ oxidation in the Sphagnum moss microbiome

Abstract

Peat mosses (Sphagnum spp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits. Sphagnum mosses harbor a diverse assemblage of microbial partners, including N2‐fixing (diazotrophic) and CH4‐oxidizing (methanotrophic) taxa that support ecosystem function by regulating transformations of carbon and nitrogen. Here, we investigate the response of the Sphagnum phytobiome (plant + constituent microbiome + environment) to a gradient of experimental warming (+0°C to +9°C) and elevated CO2 (+500 ppm) in an ombrotrophic peatland in northern Minnesota (USA). By tracking changes in carbon (CH4, CO2) and nitrogen (NH4‐N) cycling from the belowground environment up to Sphagnum and its associated microbiome, we identified a series of cascading impacts to the Sphagnum phytobiome triggered by warming and elevated CO2. Under ambient CO2, warming increased plant‐available NH4‐N in surface peat, excess N accumulated in Sphagnum tissue, and N2 fixation activity decreased. Elevated CO2 offset the effects of warming, disrupting the accumulation of N in peat and Sphagnum tissue. Methane concentrations in porewater increased with warming irrespective of CO2 treatment, resulting in a ~10× rise in methanotrophic activity within Sphagnum from the +9°C enclosures. Warming's divergent impacts on diazotrophy and methanotrophy caused these processes to become decoupled at warmer temperatures, as evidenced by declining rates of methane‐induced N2 fixation and significant losses of keystone microbial taxa. In addition to changes in the Sphagnum microbiome, we observed ~94% mortality of Sphagnum between the +0°C and +9°C treatments, possibly due to the interactive effects of warming on N‐availability and competition from vascular plant species. Collectively, these results highlight the vulnerability of the Sphagnum phytobiome to rising temperatures and atmospheric CO2 concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.

Temperature and CO2 interactively drive shifts in the compositional and functional structure of peatland protist communities

“…Petro et al. (2023) recently found similar interactive effects of warming and elevated CO 2 on N. Elevated temperature and ambient CO 2 conditions produced the accumulation of nitrogen and a reduction in N 2 fixation, which was reversed under elevated CO 2 conditions. This in turn altered N immobilization by microorganisms, likely leading to a change in microbial food web dynamics.…”

“…Furthermore, while earth-system models may predict range shifts in Sphagnum spp. (Ma et al, 2022), our findings indicate that the combined effects of elevated carbon dioxide and temperature may alter the symbiotic moss microbiome in unexpected ways-ways that could affect the distribution of Sphagnum and peatlands in the future (Carrell et al, 2019;Carrell, Velickovič, et al, 2022;Petro et al, 2023). Given the diverse energy acquisition strategies of peatland protists and their predominant distribitions in the mid-and high-latitudes of the Northern hemisphere-especially sensitive to climate change (Frolking et al, 2011;Gorham et.…”

Responses of vascular plant fine roots and associated microbial communities to whole‐ecosystem warming and elevated CO2 in northern peatlands

“…Sphagnum-dominated peatlands are predominantly located at high latitudes, which are expected to experience greater temperature increases with climate change (Collins et al, 2013), and the response of northern peatlands to rising temperatures threatens to release their large carbon stores (Davidson & Janssens, 2006;Bradshaw & Warkentin, 2015). Observed changes with warming in northern peatlands include Sphagnum moss mortality (Jassey et al, 2013;Norby et al, 2019;Petro et al, 2023), and water table drawdowns due to enhanced evapotranspiration (Hanson et al, 2020). These changes are accompanied by increased fine-root growth of vascular plants (Malhotra et al, 2020;Bucher et al, 2023), which may, in turn, stimulate the release of labile organic carbon into the peat (D'Andrilli et al, 2010), and ultimately increase nitrogen and phosphorus availability (Laiho Ó 2024 The Authors New Phytologist Ó 2024 New Phytologist Foundation New Phytologist (2024) 242: 1333-1347 1333 www.newphytologist.com This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.…”

“…Therefore, plants that are fertilized by elevated CO 2 (eCO 2 ) can considerably impact peatland biogeochemical cycles. As such, eCO 2 may offset the increase in plant‐available nitrogen, typical of warmed peatlands (Iversen et al ., 2023; Petro et al ., 2023), and together, warming and eCO 2 could intensify OM degradation and accelerate carbon turnover rates (Ofiti et al ., 2022). Nutrient availability, and especially nitrogen, influences ECM fungal community composition (Lilleskov et al ., 2019), and trait‐based approaches have been particularly useful to understand the response of ECM fungi to eCO 2 .…”

Shading contributes to Sphagnum decline in response to warming

“…There was little response to the treatments in the first year of exposure ( 2016), but the response became apparent in the second and third years, with little change after that (Figure S1b,c). The loss of cover was the primary contributor to the decline in NPP (Norby et al, 2019;Petro et al, 2023).…”