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 concentration and 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