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24 páginas.- 14 figuras.- 5 tablas.- 136 referencias.- Supplementary data to this article can be found online athttps://doi.org/10.1016/j.scitotenv.2020.141218, 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. © 2020 Elsevier B.V., This work was supported by the Spanish Ministry of Economy and Competitiveness through projects PID2019-110603RB-I00 , CGL2016-78318-C2-1R and CGL2016-78318-C2-2R AEI/FEDER/UE, and with the scientific and technical contribution of the following projects: CGL2016-75590-P with ERDF funds, CGL2017-83931-C3-2-P and CGL2017-87216-C4-1-R , AEI / FEDER , UE. S. Cuezva was funded by the European Union's Horizon 2020 - Research and Innovation Framework Programme under the Marie Skłodowska-Curie grant agreement No 844535 — MIFLUKE. N. Otero was funded by the Serra Húnter Fellowship ( Generalitat de Catalunya , Spain). We thank to GERA-group of the Fire-fighters Service of Madrid Autonomous Region for the essential work on installing the system of tubes for air sampling and the Council of “Alhama de Murcia” for their technical assistance during fieldwork.