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Characterization of metagenome-assembled genomes from the International Space Station

BACKGROUND: Several investigations on the microbial diversity and functional properties of the International Space Station (ISS) environment were carried out to understand the influence of spaceflight conditions on the microbial population. However, metagenome-assembled genomes (MAGs) of ISS samples...

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Autores principales: Singh, Nitin K., Wood, Jason M., Patane, Jose, Moura, Livia Maria Silva, Lombardino, Jonathan, Setubal, João Carlos, Venkateswaran, Kasthuri
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10233975/
https://www.ncbi.nlm.nih.gov/pubmed/37264385
http://dx.doi.org/10.1186/s40168-023-01545-7
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author Singh, Nitin K.
Wood, Jason M.
Patane, Jose
Moura, Livia Maria Silva
Lombardino, Jonathan
Setubal, João Carlos
Venkateswaran, Kasthuri
author_facet Singh, Nitin K.
Wood, Jason M.
Patane, Jose
Moura, Livia Maria Silva
Lombardino, Jonathan
Setubal, João Carlos
Venkateswaran, Kasthuri
author_sort Singh, Nitin K.
collection PubMed
description BACKGROUND: Several investigations on the microbial diversity and functional properties of the International Space Station (ISS) environment were carried out to understand the influence of spaceflight conditions on the microbial population. However, metagenome-assembled genomes (MAGs) of ISS samples are yet to be generated and subjected to various genomic analyses, including phylogenetic affiliation, predicted functional pathways, antimicrobial resistance, and virulence characteristics. RESULTS: In total, 46 MAGs were assembled from 21 ISS environmental metagenomes, in which metaSPAdes yielded 20 MAGs and metaWRAP generated 26 MAGs. Among 46 MAGs retrieved, 18 bacterial species were identified, including one novel genus/species combination (Kalamiella piersonii) and one novel bacterial species (Methylobacterium ajmalii). In addition, four bins exhibited fungal genomes; this is the first-time fungal genomes were assembled from ISS metagenomes. Phylogenetic analyses of five bacterial species showed ISS-specific evolution. The genes pertaining to cell membranes, such as transmembrane transport, cell wall organization, and regulation of cell shape, were enriched. Variations in the antimicrobial-resistant (AMR) and virulence genes of the selected 20 MAGs were characterized to predict the ecology and evolution of biosafety level (BSL) 2 microorganisms in space. Since microbial virulence increases in microgravity, AMR gene sequences of MAGs were compared with genomes of respective ISS isolates and corresponding type strains. Among these 20 MAGs characterized, AMR genes were more prevalent in the Enterobacter bugandensis MAG, which has been predominantly isolated from clinical samples. MAGs were further used to analyze if genes involved in AMR and biofilm formation of viable microbes in ISS have variation due to generational evolution in microgravity and radiation pressure. CONCLUSIONS: Comparative analyses of MAGs and whole-genome sequences of related ISS isolates and their type strains were characterized to understand the variation related to the microbial evolution under microgravity. The Pantoea/Kalamiella strains have the maximum single-nucleotide polymorphisms found within the ISS strains examined. This may suggest that Pantoea/Kalamiella strains are much more subjective to microgravity changes. The reconstructed genomes will enable researchers to study the evolution of genomes under microgravity and low-dose irradiation compared to the evolution of microbes here on Earth. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01545-7.
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spelling pubmed-102339752023-06-02 Characterization of metagenome-assembled genomes from the International Space Station Singh, Nitin K. Wood, Jason M. Patane, Jose Moura, Livia Maria Silva Lombardino, Jonathan Setubal, João Carlos Venkateswaran, Kasthuri Microbiome Research BACKGROUND: Several investigations on the microbial diversity and functional properties of the International Space Station (ISS) environment were carried out to understand the influence of spaceflight conditions on the microbial population. However, metagenome-assembled genomes (MAGs) of ISS samples are yet to be generated and subjected to various genomic analyses, including phylogenetic affiliation, predicted functional pathways, antimicrobial resistance, and virulence characteristics. RESULTS: In total, 46 MAGs were assembled from 21 ISS environmental metagenomes, in which metaSPAdes yielded 20 MAGs and metaWRAP generated 26 MAGs. Among 46 MAGs retrieved, 18 bacterial species were identified, including one novel genus/species combination (Kalamiella piersonii) and one novel bacterial species (Methylobacterium ajmalii). In addition, four bins exhibited fungal genomes; this is the first-time fungal genomes were assembled from ISS metagenomes. Phylogenetic analyses of five bacterial species showed ISS-specific evolution. The genes pertaining to cell membranes, such as transmembrane transport, cell wall organization, and regulation of cell shape, were enriched. Variations in the antimicrobial-resistant (AMR) and virulence genes of the selected 20 MAGs were characterized to predict the ecology and evolution of biosafety level (BSL) 2 microorganisms in space. Since microbial virulence increases in microgravity, AMR gene sequences of MAGs were compared with genomes of respective ISS isolates and corresponding type strains. Among these 20 MAGs characterized, AMR genes were more prevalent in the Enterobacter bugandensis MAG, which has been predominantly isolated from clinical samples. MAGs were further used to analyze if genes involved in AMR and biofilm formation of viable microbes in ISS have variation due to generational evolution in microgravity and radiation pressure. CONCLUSIONS: Comparative analyses of MAGs and whole-genome sequences of related ISS isolates and their type strains were characterized to understand the variation related to the microbial evolution under microgravity. The Pantoea/Kalamiella strains have the maximum single-nucleotide polymorphisms found within the ISS strains examined. This may suggest that Pantoea/Kalamiella strains are much more subjective to microgravity changes. The reconstructed genomes will enable researchers to study the evolution of genomes under microgravity and low-dose irradiation compared to the evolution of microbes here on Earth. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01545-7. BioMed Central 2023-06-01 /pmc/articles/PMC10233975/ /pubmed/37264385 http://dx.doi.org/10.1186/s40168-023-01545-7 Text en © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Singh, Nitin K.
Wood, Jason M.
Patane, Jose
Moura, Livia Maria Silva
Lombardino, Jonathan
Setubal, João Carlos
Venkateswaran, Kasthuri
Characterization of metagenome-assembled genomes from the International Space Station
title Characterization of metagenome-assembled genomes from the International Space Station
title_full Characterization of metagenome-assembled genomes from the International Space Station
title_fullStr Characterization of metagenome-assembled genomes from the International Space Station
title_full_unstemmed Characterization of metagenome-assembled genomes from the International Space Station
title_short Characterization of metagenome-assembled genomes from the International Space Station
title_sort characterization of metagenome-assembled genomes from the international space station
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10233975/
https://www.ncbi.nlm.nih.gov/pubmed/37264385
http://dx.doi.org/10.1186/s40168-023-01545-7
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