Non-living respiration: another breath in the soil

Containing about three times more carbon (C) than the atmosphere (600-800 PgC) or the Earth’s vegetation, soils are crucial C pools for climate change mitigation. The CO₂ flux (~110 PgC yr⁻¹) from soils is the largest terrestrial C source to the atmosphere and is about ten times the annual emissions from burning fossil fuels (IPCC 2021). A small change in soil CO₂ flux can significantly alter the atmospheric CO₂ concentrationand potentially amplify global warming.A complete and reliable identification of soil processes likely to affect soil C balance and CO₂ flux is essential to predict future atmospheric CO₂ concentrations.

The current scientific consensus is that the dominant component of the soil CO₂ flux is heterotrophic microbial respiration. However, this paradigm is challenged by recurrent observations of substantial and persistent CO₂ emissions in soil microcosms where sterilization treatments (e.g. γ-irradiations) reduced microbial activities to an undetectable level. To address this shortcoming, we postulated that non-cellular respiratory pathways in soils are capable of performing the complete oxidation of organic matter to CO₂. This hypothesis was enhanced (i) by the detection of an isotopic signature of soil CO₂ flux (δ¹³C-CO₂ up to −75.4 ± 2.8 ‰) incompatible with a cell-derived respiration and (ii) by the release of ¹³C-CO₂ in sterilized soils supplied with ¹³C-glucose (Maire et al. 2013; Kéraval et al. 2016; 2018).

Overall our work highlights that non-cellular respiration accounts for 16 to 48 % of CO₂ fluxes from sterilized soils worldwide with contrasted physical and chemical properties. We have also demonstrated that sterilized soils have a high and persistent potential for electron transfer and form self-sustaining systems that can maintain CO₂ emissions for more than 6 years without external input. Furthermore, untargeted metabolite profiling carried out using proton nuclear magnetic resonance (¹H NMR) spectroscopy revealed that non-living soils have an orderly exometabolome dynamics supporting the idea that non-stochastic scenarios mimicking biochemical transformations (i.e. Krebs cycle, fermentation) occurred in sterilized soils (Bouquet, Keraval et al. in prep).

• Maire, V. et al, 2013. An unknown oxidative metabolism substantially contributes to soil CO₂emissions, Biogeosciences, 10, 1155–1167, https://doi.org/10.5194/bg-10-1155-2013,
• Kéraval, B., et al, 2016. Soil carbon dioxide emissions controlled by an extracellular oxidative metabolism identifiable by its isotope signature, Biogeosciences, 13, 6353–6362, https://doi.org/10.5194/bg-13-6353-2016, 2016
• Kéraval, B. et al, 2018. Cellular and non-cellular mineralization of organic carbon in soils with contrasted physicochemical properties. Soil Biol. Biochem. 125, 286–289. doi:10.1016/j. soilbio.2018.07.02
• Bouquet, C., et al. in prep. Non-living respiration : another breath in the soil