Biologically mediated release of endogenous N2O and NO2 gases in a hydrothermal, hypoxic subterranean environment

Abstract

The migration of geogenic gases in continental areas with geothermal activity and active faults is an important process releasing greenhouse gases (GHG) to the lower troposphere. In this respect, caves in hypogenic environments are natural laboratories to study the compositional evolution of deep-endogenous fluids through the Critical Zone. Vapour Cave (Alhama, Murcia, Spain) is a hypogenic cave formed by the upwelling of hydrothermal CO₂-rich fluids. Anomalous concentrations of N₂O and NO₂ were registered in the cave's subterranean atmosphere, averaging ten and five times the typical atmospheric backgrounds, respectively. We characterised the thermal conditions, gaseous compositions, sediments, and microbial communities at different depths in the cave. We did so to understand the relation between N-cycling microbial groups and the production and transformation of nitrogenous gases, as well as their coupled evolution with CO₂ and CH₄ during their migration through the Critical Zone to the lower troposphere. Our results showed an evident vertical stratification of selected microbial groups (Archaea and Bacteria) depending on the environmental parameters, including O₂, temperature, and GHG concentration. Both the N₂O isotope ratios and the predicted ecological functions of bacterial and archaeal communities suggest that N₂O and NO₂ emissions mainly depend on the nitrification by ammonia-oxidising microorganisms. Denitrification and abiotic reactions of the reactive intermediates NH₂OH, NO, and NO₂^- are also plausible according to the results of the phylogenetic analyses of the microbial communities. Nitrite-dependent anaerobic methane oxidation by denitrifying methanotrophs of the NC10 phylum was also identified as a post-genetic process during migration of this gas to the surface. To the best of our knowledge, our report provides, for the first time, evidence of a niche densely populated by Micrarchaeia, which represents more than 50% of the total archaeal abundance. This raises many questions on the metabolic behaviour of this and other archaeal phyla.

Keywords: Critical zone; Deep endogenous gas; Methane oxidation; Nitrification; Nitrogen dioxide; Nitrous oxide.