Abstract

Climate warming may be exacerbated if rising temperatures stimulate losses of soil carbon to the atmosphere. The direction and magnitude of this carbon‐climate feedback are uncertain, largely due to lack of knowledge of the thermal adaptation of the physiology and composition of soil microbial communities. Here, we applied the macromolecular rate theory (MMRT) to describe the temperature response of the microbial decomposition of soil organic matter (SOM) in a natural long‐term warming experiment in a geothermally active area in New Zealand. Our objective was to test whether microbial communities adapt to long‐term warming with a shift in their composition and their temperature response that are consistent with evolutionary theory of trade‐offs between enzyme structure and function. We characterized the microbial community composition (using metabarcoding) and the temperature response of microbial decomposition of SOM (using MMRT) of soils sampled along transects of increasing distance from a geothermally active zone comprising two biomes (a shrubland and a grassland) and sampled at two depths (0–50 and 50–100 mm), such that ambient soil temperature and soil carbon concentration varied widely and independently. We found that the different environments were hosting microbial communities with distinct compositions, with thermophile and thermotolerant genera increasing in relative abundance with increasing ambient temperature. However, the ambient temperature had no detectable influence on the MMRT parameters or the relative temperature sensitivity of decomposition (Q 10). MMRT parameters were, however, strongly correlated with soil carbon concentration and carbon:nitrogen ratio. Our findings suggest that, while long‐term warming selects for warm‐adapted taxa, substrate quality and quantity exert a stronger influence than temperature in selecting for distinct thermal traits. The results have major implications for our understanding of the role of soil microbial processes in the long‐term effects of climate warming on soil carbon dynamics and will help increase confidence in carbon‐climate feedback projections.

Highlights

  • Microbial decomposition of soil organic matter (SOM) results in emissions of up to 60 Pg (1015 g) of carbon (C) per year as CO2 from soils to the atmosphere (Cavicchioli et al, 2019; Reay, 2007)—­approximately six times the current annual rate of anthropogenic emissions—­making it a key component in the global C cycle

  • The sampling strategy resulted in a full factorial design (3 thermal environments × 2 biomes × 2 depths), replicated three times, allowing us to disentangle the effects of substrate supply from those of long-­term warming on the temperature response of microbial decomposition of SOM

  • We characterized the temperature response of microbial decomposition of SOM and the composition of microbial communities from soils sampled at increasing distances from a geothermally heated depression in two biomes and at two sampling depths

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Summary

| INTRODUCTION

Microbial decomposition of soil organic matter (SOM) results in emissions of up to 60 Pg (1015 g) of carbon (C) per year as CO2 from soils to the atmosphere (Cavicchioli et al, 2019; Reay, 2007)—­approximately six times the current annual rate of anthropogenic emissions—­making it a key component in the global C cycle. The sampling strategy resulted in a full factorial design (3 thermal environments × 2 biomes × 2 depths), replicated three times, allowing us to disentangle the effects of substrate supply (as approximated from C concentration) from those of long-­term warming on the temperature response of microbial decomposition of SOM. Our specific objectives were to test the following hypotheses: (i) warming selects for microbial communities with distinct composition characterized by increasing relative abundance of thermophile and thermotolerant organisms and (ii) these communities have adapted to their environmental temperature in such a way that they have a higher Topt and a flatter temperature response (less negative ΔCP‡), in accordance with the ‘enzyme rigidity hypothesis’ (Alster et al, 2020; Arcus et al, 2016), leading to a lower relative temperature sensitivity

| MATERIALS AND METHODS
| RESULTS
Findings
| DISCUSSION
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