Geothermally warmed soils reveal persistent increases in the respiratory costs of soil microbes contributing to substantial C losses

Abstract

Increasing temperatures can accelerate soil organic matter decomposition and release large amounts of CO2 to the atmosphere, potentially inducing positive warming feedbacks. Alterations to the temperature sensitivity and physiological functioning of soil microorganisms may play a key role in these carbon (C) losses. Geothermally active areas in Iceland provide stable and continuous soil temperature gradients to test this hypothesis, encompassing the full range of warming scenarios projected by the Intergovernmental Panel on Climate Change for the northern region. We took soils from these geothermal sites seven years after the onset of warming and incubated them at varying temperatures and substrate availability conditions to detect persistent alterations of microbial physiology to long-term warming. Seven years of continuous warming ranging from 1.8 to 15.9 ºC triggered a 8.6 to 58.0 % decrease on the C concentrations in the topsoil (0-10 cm) of these sub-arctic silt-loam Andosols. The sensitivity of microbial respiration to temperature (Q10) was not altered. However, soil microbes showed a persistent increase in their microbial metabolic quotients (microbial respiration per unit of microbial biomass) and a subsequent diminished C retention in biomass. After an initial depletion of labile soil C upon soil warming, increasing energy costs of metabolic maintenance and resource acquisition led to a weaker capacity of C stabilization in the microbial biomass of warmer soils. This mechanism contributes to our understanding of the acclimated response of soil respiration to in situ soil warming at the ecosystem level, despite a lack of acclimation at the physiological level. Persistent increases in the respiratory costs of soil microbes in response to warming constitute a fundamental process that should be incorporated into climate change-C cycling models.

Central metabolic responses of microorganisms to years and decades of soil warming

“…Warmed soils differed from their ambient counterparts (Fig. 1b); total, dissolved organic, and microbial C, N, and P concentrations were lower in the warmed soils, mirroring previous studies that also report lower substrate concentrations and microbial biomass contents in the warmed soils at the same site [15][16][17][18] . Soil pH ranged from 4.4 to 6.0 and was slightly higher in the warmed soils (P < 0.05, n = 16, Pcorr > 0.1, Supplementary Table 1 and 2 for absolute values and significant differences, respectively).…”

“…The effects of long-term and short-to medium-term soil warming on abiotic and biotic properties and processes at these sites have been described in a range of publications. For example, Walker et al 16 , Marañón-Jiménez et al 17,18 , and Poeplau et al 19 identified considerable soil environmental changes in the warmed grassland plots, including reductions in topsoil C and nitrogen (N) pools by about 40% and decreased soil aggregation. These changes were accompanied by lower soil microbial biomass but higher soil respiration rates per unit of microbial biomass 16 , contradicting the concept of a physiological acclimation of microorganisms 16 .…”

Abiotic CO&lt;sub&gt;2&lt;/sub&gt; sources confound interpretation of temperature responses of in situ respiration in geothermally warmed forest soils of Iceland

“…acclimation" of CO2 effluxes at the higher soil temperatures, as suggested also in other laboratory studies in ForHot project by Marañón-Jiménez et al (2018) and Walker et al (2018).…”

“…First indirect support for this hypothesis comes from a study by Poeplau et al (2019) showing a strong warming-induced depletion of carbon concentration in the soils of these geothermal areas. However, soil microbial respiration rates were, contrary to the aforementioned hypothesis, reduced in these warmed soil as shown in recent laboratory incubation experiments (Marañón-Jiménez et al, 2018) most likely due to the reduced carbon contents in warmed soils and a subsequent decline in microbial biomass; however, mass-specific respiration rates increased with warming (Walker et al, 2018). Temperature effects 45 on soil respiration are thus highly complex and they need to be studied in the field to fully elucidate the interactions of plants, soil, and climatic variation.…”

“…There can be a large overestimation of the biogenic CO2 efflux when the corresponding isotopic data are not considered. Source partitioning of CO2 will be critical for field studies; laboratory studies are not impacted by the geothermal CO2 sources from deep-origin (Marañón-Jiménez et al, 2018;Walker et al, 2018;Maljanen et al, 2018).…”