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

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 pan...

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Autores principales:	Ryan A. Blaustein, Alexander G. McFarland, Sarah Ben Maamar, Alberto Lopez, Sarah Castro-Wallace, Erica M. Hartmann
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	International Space Station bacterial adaptation built environment microbiome pangenome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/74631cad07bd4832b8f47af22590266d
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spelling	oai:doaj.org-article:74631cad07bd4832b8f47af22590266d2021-12-02T18:15:45ZPangenomic Approach To Understanding Microbial Adaptations within a Model Built Environment, the International Space Station, Relative to Human Hosts and Soil10.1128/mSystems.00281-182379-5077https://doaj.org/article/74631cad07bd4832b8f47af22590266d2019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00281-18https://doaj.org/toc/2379-5077ABSTRACT 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. Author Video: An author video summary of this article is available.Ryan A. BlausteinAlexander G. McFarlandSarah Ben MaamarAlberto LopezSarah Castro-WallaceErica M. HartmannAmerican Society for MicrobiologyarticleInternational Space Stationbacterial adaptationbuilt environment microbiomepangenomeMicrobiologyQR1-502ENmSystems, Vol 4, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	International Space Station bacterial adaptation built environment microbiome pangenome Microbiology QR1-502
spellingShingle	International Space Station bacterial adaptation built environment microbiome pangenome Microbiology QR1-502 Ryan A. Blaustein Alexander G. McFarland Sarah Ben Maamar Alberto Lopez Sarah Castro-Wallace Erica M. Hartmann Pangenomic Approach To Understanding Microbial Adaptations within a Model Built Environment, the International Space Station, Relative to Human Hosts and Soil
description	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. Author Video: An author video summary of this article is available.
format	article
author	Ryan A. Blaustein Alexander G. McFarland Sarah Ben Maamar Alberto Lopez Sarah Castro-Wallace Erica M. Hartmann
author_facet	Ryan A. Blaustein Alexander G. McFarland Sarah Ben Maamar Alberto Lopez Sarah Castro-Wallace Erica M. Hartmann
author_sort	Ryan A. Blaustein
title	Pangenomic Approach To Understanding Microbial Adaptations within a Model Built Environment, the International Space Station, Relative to Human Hosts and Soil
title_short	Pangenomic Approach To Understanding Microbial Adaptations within a Model Built Environment, the International Space Station, Relative to Human Hosts and Soil
title_full	Pangenomic Approach To Understanding Microbial Adaptations within a Model Built Environment, the International Space Station, Relative to Human Hosts and Soil
title_fullStr	Pangenomic Approach To Understanding Microbial Adaptations within a Model Built Environment, the International Space Station, Relative to Human Hosts and Soil
title_full_unstemmed	Pangenomic Approach To Understanding Microbial Adaptations within a Model Built Environment, the International Space Station, Relative to Human Hosts and Soil
title_sort	pangenomic approach to understanding microbial adaptations within a model built environment, the international space station, relative to human hosts and soil
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/74631cad07bd4832b8f47af22590266d
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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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