Soil carbon dioxide emissions controlled by an extracellular oxidative metabolism identifiable by its isotope signature

Soil heterotrophic respiration is a major determinant of the carbon (C) cycle and its interactions with climate. Given the complexity of the respiratory machinery, it is traditionally considered that oxidation of organic C into carbon dioxide (CO2) strictly results from intracellular metabolic processes. Here we show that C mineralization can operate in soils deprived of all observable cellular forms. Moreover, the process responsible for CO2 emissions in sterilized soils induced a strong C isotope fractionation (up to 50 ‰) incompatible with respiration of cellular origin. The supply of 13C glucose in sterilized soil led to the release of 13CO2 suggesting the presence of respiratory-like metabolism (glycolysis, decarboxylation reaction, chain of electron transfer) carried out by soil-stabilized enzymes, and by soil mineral and metal catalysts. These findings indicate that CO2 emissions from soils can have two origins: (1) from the well-known respiration of soil heterotrophic microorganisms and (2) from an extracellular oxidative metabolism (EXOMET) or, at least, catabolism. These two metabolisms should be considered separately when studying effects of environmental factors on the C cycle because the likelihood is that they do not obey the same laws and they respond differently to abiotic factors.