Multidrug-resistant Acinetobacter pittii is adapting to and exhibiting succession aboard the International Space Station

Monitoring adaptation of microorganisms to the extreme environment of the International Space Station (ISS) is crucial to understanding microbial evolution and determining how to protect astronauts from potential infections. Acinetobacter pittii is an opportunistic nosocomial pathogen that was recently isolated from two different missions aboard the ISS. Here, we report how ISS-associated A. pittii (N = 25 genomes) has formed its own genetically and functionally discrete clade distinct from earth-bound isolates (N = 291 genomes). By searching in 403 longitudinal environmental and host-associated ISS metagenomes, we observed that A. pittii is exhibiting succession and increasing in abundance and prevalence over the period of time, being identified in >2X more metagenomic samples in back to back missions. ISS-strains are multidrug resistant and continuously acquire functions that enable them to survive in harsh environments, including transcriptional regulators and the toxin-antitoxin system RelBE (present in 40% of isolates from Microbial Tracking Mission 1 [MT1] and 94% of isolates from MT2). Finally, we executed a comparative-genomics-driven microbial association study to identify a core set of 59 "ISS-associated gene clusters" that have been acquired by A. pittii. Overall, these results indicated a step forward in understanding how microorganisms might evolve in extreme and resource-limited human built environments.