Genomic, functional, and metabolic enhancements in multidrug-resistant Enterobacter bugandensis facilitating its persistence and succession in the International Space Station
Abstract Background The International Space Station (ISS) stands as a testament to human achievement in space exploration. Despite its highly controlled environment, characterised by microgravity, increased CO $$_{2}$$ 2 levels, and elevated solar radiation, microorganisms occupy a unique niche. The...
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| Format: | Article |
| Language: | English |
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BMC
2024-03-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-024-01777-1 |
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| author | Pratyay Sengupta Shobhan Karthick Muthamilselvi Sivabalan Nitin Kumar Singh Karthik Raman Kasthuri Venkateswaran |
| author_facet | Pratyay Sengupta Shobhan Karthick Muthamilselvi Sivabalan Nitin Kumar Singh Karthik Raman Kasthuri Venkateswaran |
| author_sort | Pratyay Sengupta |
| collection | DOAJ |
| description | Abstract Background The International Space Station (ISS) stands as a testament to human achievement in space exploration. Despite its highly controlled environment, characterised by microgravity, increased CO $$_{2}$$ 2 levels, and elevated solar radiation, microorganisms occupy a unique niche. These microbial inhabitants play a significant role in influencing the health and well-being of astronauts on board. One microorganism of particular interest in our study is Enterobacter bugandensis, primarily found in clinical specimens including the human gastrointestinal tract, and also reported to possess pathogenic traits, leading to a plethora of infections. Results Distinct from their Earth counterparts, ISS E. bugandensis strains have exhibited resistance mechanisms that categorise them within the ESKAPE pathogen group, a collection of pathogens recognised for their formidable resistance to antimicrobial treatments. During the 2-year Microbial Tracking 1 mission, 13 strains of multidrug-resistant E. bugandensis were isolated from various locations within the ISS. We have carried out a comprehensive study to understand the genomic intricacies of ISS-derived E. bugandensis in comparison to terrestrial strains, with a keen focus on those associated with clinical infections. We unravel the evolutionary trajectories of pivotal genes, especially those contributing to functional adaptations and potential antimicrobial resistance. A hypothesis central to our study was that the singular nature of the stresses of the space environment, distinct from any on Earth, could be driving these genomic adaptations. Extending our investigation, we meticulously mapped the prevalence and distribution of E. bugandensis across the ISS over time. This temporal analysis provided insights into the persistence, succession, and potential patterns of colonisation of E. bugandensis in space. Furthermore, by leveraging advanced analytical techniques, including metabolic modelling, we delved into the coexisting microbial communities alongside E. bugandensis in the ISS across multiple missions and spatial locations. This exploration revealed intricate microbial interactions, offering a window into the microbial ecosystem dynamics within the ISS. Conclusions Our comprehensive analysis illuminated not only the ways these interactions sculpt microbial diversity but also the factors that might contribute to the potential dominance and succession of E. bugandensis within the ISS environment. The implications of these findings are twofold. Firstly, they shed light on microbial behaviour, adaptation, and evolution in extreme, isolated environments. Secondly, they underscore the need for robust preventive measures, ensuring the health and safety of astronauts by mitigating risks associated with potential pathogenic threats. Video Abstract |
| first_indexed | 2024-04-24T19:53:40Z |
| format | Article |
| id | doaj.art-4203b466a7c34ef380c18c7b8221e922 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-24T19:53:40Z |
| publishDate | 2024-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-4203b466a7c34ef380c18c7b8221e9222024-03-24T12:27:43ZengBMCMicrobiome2049-26182024-03-0112111710.1186/s40168-024-01777-1Genomic, functional, and metabolic enhancements in multidrug-resistant Enterobacter bugandensis facilitating its persistence and succession in the International Space StationPratyay Sengupta0Shobhan Karthick Muthamilselvi Sivabalan1Nitin Kumar Singh2Karthik Raman3Kasthuri Venkateswaran4Department of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology MadrasDepartment of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology MadrasNASA Jet Propulsion Laboratory, California Institute of TechnologyDepartment of Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology MadrasNASA Jet Propulsion Laboratory, California Institute of TechnologyAbstract Background The International Space Station (ISS) stands as a testament to human achievement in space exploration. Despite its highly controlled environment, characterised by microgravity, increased CO $$_{2}$$ 2 levels, and elevated solar radiation, microorganisms occupy a unique niche. These microbial inhabitants play a significant role in influencing the health and well-being of astronauts on board. One microorganism of particular interest in our study is Enterobacter bugandensis, primarily found in clinical specimens including the human gastrointestinal tract, and also reported to possess pathogenic traits, leading to a plethora of infections. Results Distinct from their Earth counterparts, ISS E. bugandensis strains have exhibited resistance mechanisms that categorise them within the ESKAPE pathogen group, a collection of pathogens recognised for their formidable resistance to antimicrobial treatments. During the 2-year Microbial Tracking 1 mission, 13 strains of multidrug-resistant E. bugandensis were isolated from various locations within the ISS. We have carried out a comprehensive study to understand the genomic intricacies of ISS-derived E. bugandensis in comparison to terrestrial strains, with a keen focus on those associated with clinical infections. We unravel the evolutionary trajectories of pivotal genes, especially those contributing to functional adaptations and potential antimicrobial resistance. A hypothesis central to our study was that the singular nature of the stresses of the space environment, distinct from any on Earth, could be driving these genomic adaptations. Extending our investigation, we meticulously mapped the prevalence and distribution of E. bugandensis across the ISS over time. This temporal analysis provided insights into the persistence, succession, and potential patterns of colonisation of E. bugandensis in space. Furthermore, by leveraging advanced analytical techniques, including metabolic modelling, we delved into the coexisting microbial communities alongside E. bugandensis in the ISS across multiple missions and spatial locations. This exploration revealed intricate microbial interactions, offering a window into the microbial ecosystem dynamics within the ISS. Conclusions Our comprehensive analysis illuminated not only the ways these interactions sculpt microbial diversity but also the factors that might contribute to the potential dominance and succession of E. bugandensis within the ISS environment. The implications of these findings are twofold. Firstly, they shed light on microbial behaviour, adaptation, and evolution in extreme, isolated environments. Secondly, they underscore the need for robust preventive measures, ensuring the health and safety of astronauts by mitigating risks associated with potential pathogenic threats. Video Abstracthttps://doi.org/10.1186/s40168-024-01777-1Pangenome analysisEnterobacter bugandensisMetabolic modellingISS metagenomics |
| spellingShingle | Pratyay Sengupta Shobhan Karthick Muthamilselvi Sivabalan Nitin Kumar Singh Karthik Raman Kasthuri Venkateswaran Genomic, functional, and metabolic enhancements in multidrug-resistant Enterobacter bugandensis facilitating its persistence and succession in the International Space Station Microbiome Pangenome analysis Enterobacter bugandensis Metabolic modelling ISS metagenomics |
| title | Genomic, functional, and metabolic enhancements in multidrug-resistant Enterobacter bugandensis facilitating its persistence and succession in the International Space Station |
| title_full | Genomic, functional, and metabolic enhancements in multidrug-resistant Enterobacter bugandensis facilitating its persistence and succession in the International Space Station |
| title_fullStr | Genomic, functional, and metabolic enhancements in multidrug-resistant Enterobacter bugandensis facilitating its persistence and succession in the International Space Station |
| title_full_unstemmed | Genomic, functional, and metabolic enhancements in multidrug-resistant Enterobacter bugandensis facilitating its persistence and succession in the International Space Station |
| title_short | Genomic, functional, and metabolic enhancements in multidrug-resistant Enterobacter bugandensis facilitating its persistence and succession in the International Space Station |
| title_sort | genomic functional and metabolic enhancements in multidrug resistant enterobacter bugandensis facilitating its persistence and succession in the international space station |
| topic | Pangenome analysis Enterobacter bugandensis Metabolic modelling ISS metagenomics |
| url | https://doi.org/10.1186/s40168-024-01777-1 |
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