Space-type radiation induces multimodal responses in the mouse gut microbiome and metabolome
Abstract Background Space travel is associated with continuous low dose rate exposure to high linear energy transfer (LET) radiation. Pathophysiological manifestations after low dose radiation exposure are strongly influenced by non-cytocidal radiation effects, including changes in the microbiome an...
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doaj-cb615717b6f34ad6ac2b1fa76bbb750f2020-11-25T02:31:02ZengBMCMicrobiome2049-26182017-08-015111810.1186/s40168-017-0325-zSpace-type radiation induces multimodal responses in the mouse gut microbiome and metabolomeDavid Casero0Kirandeep Gill1Vijayalakshmi Sridharan2Igor Koturbash3Gregory Nelson4Martin Hauer-Jensen5Marjan Boerma6Jonathan Braun7Amrita K. Cheema8Department of Pathology and Laboratory Medicine, David Geffen School of Medicine, University of California, Los AngelesDepartment of Oncology, Georgetown University Medical CenterDivision of Radiation Health, University of Arkansas for Medical SciencesDepartment of Environmental and Occupational Health, University of Arkansas for Medical SciencesDepartment of Radiation Medicine, Loma Linda UniversityDivision of Radiation Health, University of Arkansas for Medical SciencesDivision of Radiation Health, University of Arkansas for Medical SciencesDepartment of Pathology and Laboratory Medicine, David Geffen School of Medicine, University of California, Los AngelesDepartment of Oncology, Georgetown University Medical CenterAbstract Background Space travel is associated with continuous low dose rate exposure to high linear energy transfer (LET) radiation. Pathophysiological manifestations after low dose radiation exposure are strongly influenced by non-cytocidal radiation effects, including changes in the microbiome and host gene expression. Although the importance of the gut microbiome in the maintenance of human health is well established, little is known about the role of radiation in altering the microbiome during deep-space travel. Results Using a mouse model for exposure to high LET radiation, we observed substantial changes in the composition and functional potential of the gut microbiome. These were accompanied by changes in the abundance of multiple metabolites, which were related to the enzymatic activity of the predicted metagenome by means of metabolic network modeling. There was a complex dynamic in microbial and metabolic composition at different radiation doses, suggestive of transient, dose-dependent interactions between microbial ecology and signals from the host’s cellular damage repair processes. The observed radiation-induced changes in microbiota diversity and composition were analyzed at the functional level. A constitutive change in activity was found for several pathways dominated by microbiome-specific enzymatic reactions like carbohydrate digestion and absorption and lipopolysaccharide biosynthesis, while the activity in other radiation-responsive pathways like phosphatidylinositol signaling could be linked to dose-dependent changes in the abundance of specific taxa. Conclusions The implication of microbiome-mediated pathophysiology after low dose ionizing radiation may be an unappreciated biologic hazard of space travel and deserves experimental validation. This study provides a conceptual and analytical basis of further investigations to increase our understanding of the chronic effects of space radiation on human health, and points to potential new targets for intervention in adverse radiation effects.http://link.springer.com/article/10.1186/s40168-017-0325-zIonizing radiationSpace travelMicrobiome16S rRNA amplicon sequencingUntargeted metabolomicsMetabolic network modeling |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
David Casero Kirandeep Gill Vijayalakshmi Sridharan Igor Koturbash Gregory Nelson Martin Hauer-Jensen Marjan Boerma Jonathan Braun Amrita K. Cheema |
spellingShingle |
David Casero Kirandeep Gill Vijayalakshmi Sridharan Igor Koturbash Gregory Nelson Martin Hauer-Jensen Marjan Boerma Jonathan Braun Amrita K. Cheema Space-type radiation induces multimodal responses in the mouse gut microbiome and metabolome Microbiome Ionizing radiation Space travel Microbiome 16S rRNA amplicon sequencing Untargeted metabolomics Metabolic network modeling |
author_facet |
David Casero Kirandeep Gill Vijayalakshmi Sridharan Igor Koturbash Gregory Nelson Martin Hauer-Jensen Marjan Boerma Jonathan Braun Amrita K. Cheema |
author_sort |
David Casero |
title |
Space-type radiation induces multimodal responses in the mouse gut microbiome and metabolome |
title_short |
Space-type radiation induces multimodal responses in the mouse gut microbiome and metabolome |
title_full |
Space-type radiation induces multimodal responses in the mouse gut microbiome and metabolome |
title_fullStr |
Space-type radiation induces multimodal responses in the mouse gut microbiome and metabolome |
title_full_unstemmed |
Space-type radiation induces multimodal responses in the mouse gut microbiome and metabolome |
title_sort |
space-type radiation induces multimodal responses in the mouse gut microbiome and metabolome |
publisher |
BMC |
series |
Microbiome |
issn |
2049-2618 |
publishDate |
2017-08-01 |
description |
Abstract Background Space travel is associated with continuous low dose rate exposure to high linear energy transfer (LET) radiation. Pathophysiological manifestations after low dose radiation exposure are strongly influenced by non-cytocidal radiation effects, including changes in the microbiome and host gene expression. Although the importance of the gut microbiome in the maintenance of human health is well established, little is known about the role of radiation in altering the microbiome during deep-space travel. Results Using a mouse model for exposure to high LET radiation, we observed substantial changes in the composition and functional potential of the gut microbiome. These were accompanied by changes in the abundance of multiple metabolites, which were related to the enzymatic activity of the predicted metagenome by means of metabolic network modeling. There was a complex dynamic in microbial and metabolic composition at different radiation doses, suggestive of transient, dose-dependent interactions between microbial ecology and signals from the host’s cellular damage repair processes. The observed radiation-induced changes in microbiota diversity and composition were analyzed at the functional level. A constitutive change in activity was found for several pathways dominated by microbiome-specific enzymatic reactions like carbohydrate digestion and absorption and lipopolysaccharide biosynthesis, while the activity in other radiation-responsive pathways like phosphatidylinositol signaling could be linked to dose-dependent changes in the abundance of specific taxa. Conclusions The implication of microbiome-mediated pathophysiology after low dose ionizing radiation may be an unappreciated biologic hazard of space travel and deserves experimental validation. This study provides a conceptual and analytical basis of further investigations to increase our understanding of the chronic effects of space radiation on human health, and points to potential new targets for intervention in adverse radiation effects. |
topic |
Ionizing radiation Space travel Microbiome 16S rRNA amplicon sequencing Untargeted metabolomics Metabolic network modeling |
url |
http://link.springer.com/article/10.1186/s40168-017-0325-z |
work_keys_str_mv |
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