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. 2019 Jan 8;4(1):e00281-18.
doi: 10.1128/mSystems.00281-18. eCollection Jan-Feb 2019.

Pangenomic Approach To Understanding Microbial Adaptations Within a Model Built Environment, the International Space Station, Relative to Human Hosts and Soil

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Free PMC article

Pangenomic Approach To Understanding Microbial Adaptations Within a Model Built Environment, the International Space Station, Relative to Human Hosts and Soil

Ryan A Blaustein et al. mSystems. .
Free PMC article

Abstract

Understanding underlying mechanisms involved in microbial persistence in the built environment (BE) is essential for strategically mitigating potential health risks. To test the hypothesis that BEs impose selective pressures resulting in characteristic adaptive responses, we performed a pangenomics meta-analysis leveraging 189 genomes (accessed from GenBank) of two epidemiologically important taxa, Bacillus cereus and Staphylococcus aureus, isolated from various origins: the International Space Station (ISS; a model BE), Earth-based BEs, soil, and humans. Our objectives were to (i) identify differences in the pangenomic composition of generalist and host-associated organisms, (ii) characterize genes and functions involved in BE-associated selection, and (iii) identify genomic signatures of ISS-derived strains of potential relevance for astronaut health. The pangenome of B. cereus was more expansive than that of S. aureus, which had a dominant core component. Genomic contents of both taxa significantly correlated with isolate origin, demonstrating an importance for biogeography and potential niche adaptations. ISS/BE-enriched functions were often involved in biosynthesis, catabolism, materials transport, metabolism, and stress response. Multiple origin-enriched functions also overlapped across taxa, suggesting conserved adaptive processes. We further characterized two mobile genetic elements with local neighborhood genes encoding biosynthesis and stress response functions that distinctively associated with B. cereus from the ISS. Although antibiotic resistance genes were present in ISS/BE isolates, they were also common in counterparts elsewhere. Overall, despite differences in microbial lifestyle, some functions appear common to remaining viable in the BE, and those functions are not typically associated with direct impacts on human health. IMPORTANCE The built environment contains a variety of microorganisms, some of which pose critical human health risks (e.g., hospital-acquired infection, antibiotic resistance dissemination). We uncovered a combination of complex biological functions that may play a role in bacterial survival under the presumed selective pressures in a model built environment-the International Space Station-by using an approach to compare pangenomes of bacterial strains from two clinically relevant species (B. cereus and S. aureus) isolated from both built environments and humans. Our findings suggest that the most crucial bacterial functions involved in this potential adaptive response are specific to bacterial lifestyle and do not appear to have direct impacts on human health.

Keywords: International Space Station; bacterial adaptation; built environment microbiome; pangenome.

Figures

FIG 1
FIG 1
Pangenome summary statistics. (A and B) Histogram distributions of cloud, shell, and core genes. Pie chart displays numbers of total genes with percentages in parentheses. (C) Power-law fit to the mean number of new genes per genome (bold points) after 100 pangenome permutations (i.e., background points). Θ < 1 indicates that the pangenome is in the “open” state (79).
FIG 2
FIG 2
Heterogeneity in gene presence/absence among ISS-associated B. cereus (A) and S. aureus (B) strains. Symbol shape or color corresponds to sample area and date.
FIG 3
FIG 3
Bacterial species-level genomic diversity (i.e., gene presence/absence and core gene variants) correlates with strain origin. B. cereus and S. aureus are represented in the I and II panels, respectively. (A) Total gene counts for each fraction of the pangenome by strain origin: built environment-Earth (BE-E), -spacecraft (BE-SC), culture-Earth (Cul-E), -spacecraft (Cul-SC), human, and soil samples. BE-SC samples were taken aboard the ISS; Cul-SC samples were clonal isolates sent to space aboard the Shenzhou VIII. (B) PCoA for gene presence/absence among strains. Color/shape corresponds to sample origin. (C) Phylogenetic tree constructed from core gene codon alignment with midpoint rooting. ISS-, human-, and BE-E-sourced strains from the work of Checinska Sielaff et al. (29) and the Wallace and Voorhies data set (Table S1) are shaded in blue, yellow, and gray, respectively.
FIG 4
FIG 4
Strain origin-enriched gene products. The heat map displays all function enrichments with FDR q <0.001 for B. cereus (left) and S. aureus (right). Heat color corresponds to percentage of genomes per origin type containing at least 1 gene encoding the listed product. Row colors indicate the biological process group for gene products. On the S. aureus panel, the functions associated with the staphylococcal cassette chromosome mec (IWG-SCC 2009) are shaded.
FIG 5
FIG 5
Overlap in gene products across taxa. (A) Numbers of shared and distinct functions encoded in the pangenomes, core genomes, and accessory genomes of B. cereus (blue) and S. aureus (red). (B) Shared accessory gene products across taxa that significantly correlated (P < 0.01 and FDR q <0.1) with strain origin for origins containing n ≥ 3 strains (i.e., B. cereus: ISS, human, soil; S. aureus: ISS, BE-Earth, human, human-MRSA). Each segment corresponds to the differences in percentage of strains (blue, B. cereus; red, S. aureus) isolated from the ISS-BE and human samples (i.e., putatively commensal S. aureus only, not MRSA) encoding the gene product. For example, functions with both segments in the same direction demonstrate association with the same origin or vice versa for segments in the opposite direction.

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