Cultivation and molecular profiling reveal ammonia-oxidizing archaea as skin commensals

Ammonia-oxidizing archaea (AOA) have repeatedly been detected with molecular methods on human skin, yet their persistence, physiological traits, and adaptations remain poorly understood. This is mostly owed to a lack of cultured representatives of AOA taxa from healthy human skin. Using a customized enrichment scheme, we cultivated two autotrophic strains, Candidatus Nitrosocosmicus epidermidis and Ca. Nitrosocosmicus unguis, from human skin samples. Genomic analyses revealed specific adaptations for skin colonization, including genomic islands, and expanded gene families linked to interactions with host proteins, and signaling pathways, distinguishing these AOA from their soil-dwelling relatives. Profiling of >700 samples from 8 body sites in cross-sectional and longitudinal cohorts consistently validated the detection of Ca. Nitrosocosmicus species with up to 100% prevalence in a longitudinal cohort, particularly in sebaceous areas. Co-occurrence patterns with specific bacterial taxa reinforce their role as stable components of the skin microbiome. Our results establish Ca. Nitrosocosmicus species as common skin commensals that are evolutionarily capable of transitioning from soil to human skin. They likely play a critical role in the skin ecosystem by recovering nitrogen from the sebum through utilization of urea and ammonia. This sheds new light on the role of archaeal species in maintaining the nitrogen balance in the human skin microbiome, which might be of importance in maintaining healthy skin.