Genomic analysis reveals the presence of emerging pathogenic Klebsiella lineages aboard the International Space Station

Klebsiella species, such as Klebsiella pneumoniae, Klebsiella aerogenes, and Klebsiella quasipneumoniae, are opportunistic pathogens that commonly cause infections in humans. Hypervirulent Klebsiella pneumoniae (hvKP) is a subgroup of K. pneumoniae, which has gained attention due to its global dissemination, its capacity to cause invasive infections in community settings among immunocompetent individuals, and its escalating antibiotic resistance levels. Our study presents the first comprehensive phenotypic and genotypic analysis including mobile genetic elements (MGEs) of Klebsiella isolates from the International Space Station (ISS). The genomes of K. pneumoniae, K. aerogenes, and K. quasipneumoniae offered insights into their antimicrobial resistance, virulence, thermotolerance, disinfectant resistance, and MGEs. All isolates were part of emerging pathogenic lineages with K. quasipneumoniae ST138 presenting spatial and temporal persistence aboard the ISS, possibly due to its genotypic profile encoding for numerous resistance genes to disinfectants and heavy metals. We also report on the isolation of a yersiniabactin-encoding K. pneumoniae, belonging to the emerging high-risk ST101 clone, aboard the ISS. A potential dissemination of hvKp strains on ISS might pose a risk to the immunocompromised crew members. Moreover, MGEs containing virulent loci could enable horizontal gene transfer to other benign microorganisms on the ISS, possibly enhancing their virulence potential. Additionally, some Klebsiella genomes exhibited genetic divergence from their respective lineages, which we hypothesize results from the unique spaceflight associated environmental pressures. These findings underscore the need to monitor microbial communities in space to comprehend their survival mechanisms and implications for human health. IMPORTANCE The International Space Station (ISS) is a unique, hermetically sealed environment, subject to environmental pressures not encountered on Earth, including microgravity and radiation (cosmic ionising/UV). While bacteria's adaptability during spaceflight remains elusive, recent research suggests that it may be species and even clone-specific. Considering the documented spaceflight-induced suppression of the human immune system, a deper understanding of the genomics of potential human pathogens in space could shed light on species and lineages of medical astromicrobiological significance. In this study, we used hybrid assembly methods and comparative genomics to deliver a comprehensive genomic characterization of 10 Klebsiella isolates retrieved from the ISS. Our analysis unveiled that Klebsiella quasipneumoniae ST138 demonstrates both spatial and temporal persistence aboard the ISS, showing evidence of genomic divergence from its Earth-based ST138 lineage. Moreover, we characterized plasmids from Klebsiella species of ISS origin, which harbored genes for disinfectant resistance and enhanced thermotolerance, suggestin possible adaptive advantages. Furthermore, we identified a mobile genetic element containing a hypervirulence-associated locus belonging to a Klebsiella pneumoniae isolate of the "high-risk" ST101 clone. Our work provides insights into the adaptability and persistence of Klebsiella species during spaceflight, highlighting the importance of understanding the dynamics of potential pathogenic bacteria in such environments.