Implications for nitrogen and sulphur cycles: phylogeny and niche-range of in terrestrial aquifers.

Increasing evidence suggests are important contributors to aquatic and subsurface nitrogen and sulphur cycles. We determined the phylogenetic and ecological niche associations of colonizing terrestrial aquifers. compositions were determined across 59 groundwater wells. Distributions were strongly influenced by oxygen availability in groundwater, marked by a trade-off between aerobic (, ) and anaerobic (, unclassified) lineages. Seven metagenome-assembled genomes (MAGs), or populations, were recovered from a subset of wells, including three from the recently designated class 9FT-COMBO-42-15. Most were relatively more abundant and transcriptionally active in dysoxic groundwater. These MAGs were analysed with 743 other genomes. Results illustrate the predominance of certain lineages in aquifers (e.g. non-nitrifying , classes 9FT-COMBO-42-15 and UBA9217, and family UBA1546). These lineages are characterized by mechanisms for nitrate reduction and sulphur cycling, and, excluding , the Wood-Ljungdahl pathway, consistent with carbon-limited, low-oxygen, and sulphur-rich aquifer conditions. Class 9FT-COMBO-42-15 is a sister clade of and comprises two families spanning a transition in carbon fixation approaches: f_HDB-SIOIB13 encodes rTCA (like ) and f_9FT-COMBO-42-15 encodes Wood-Ljungdahl CO dehydrogenase (like and UBA9217). The 9FT-COMBO-42-15 family is further differentiated by its capacity for sulphur oxidation (via DsrABEFH and SoxXAYZB) and dissimilatory nitrate reduction to ammonium, and gene transcription indicated active coupling of nitrogen and sulphur cycles by f_9FT-COMBO-42-15 in dysoxic groundwater. Overall, results indicate that are widely distributed in groundwater and that oxygen availability drives the spatial differentiation of lineages with ecologically distinct roles related to nitrogen and sulphur metabolism.