Reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflight

Abstract Background Space environment imposes a range of challenges to mammalian physiology and the gut microbiota, and interactions between the two are thought to be important in mammalian health in space. While previous findings have demonstrated a change in the gut microbial community structure d...

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Main Authors: Peng Jiang, Stefan J. Green, George E. Chlipala, Fred W. Turek, Martha Hotz Vitaterna
Format: Article
Language:English
Published: BMC 2019-08-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-019-0724-4
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author Peng Jiang
Stefan J. Green
George E. Chlipala
Fred W. Turek
Martha Hotz Vitaterna
author_facet Peng Jiang
Stefan J. Green
George E. Chlipala
Fred W. Turek
Martha Hotz Vitaterna
author_sort Peng Jiang
collection DOAJ
description Abstract Background Space environment imposes a range of challenges to mammalian physiology and the gut microbiota, and interactions between the two are thought to be important in mammalian health in space. While previous findings have demonstrated a change in the gut microbial community structure during spaceflight, specific environmental factors that alter the gut microbiome and the functional relevance of the microbiome changes during spaceflight remain elusive. Methods We profiled the microbiome using 16S rRNA gene amplicon sequencing in fecal samples collected from mice after a 37-day spaceflight onboard the International Space Station. We developed an analytical tool, named STARMAPs (Similarity Test for Accordant and Reproducible Microbiome Abundance Patterns), to compare microbiome changes reported here to other relevant datasets. We also integrated the gut microbiome data with the publically available transcriptomic data in the liver of the same animals for a systems-level analysis. Results We report an elevated microbiome alpha diversity and an altered microbial community structure that were associated with spaceflight environment. Using STARMAPs, we found the observed microbiome changes shared similarity with data reported in mice flown in a previous space shuttle mission, suggesting reproducibility of the effects of spaceflight on the gut microbiome. However, such changes were not comparable with those induced by space-type radiation in Earth-based studies. We found spaceflight led to significantly altered taxon abundance in one order, one family, five genera, and six species of microbes. This was accompanied by a change in the inferred microbial gene abundance that suggests an altered capacity in energy metabolism. Finally, we identified host genes whose expression in the liver were concordantly altered with the inferred gut microbial gene content, particularly highlighting a relationship between host genes involved in protein metabolism and microbial genes involved in putrescine degradation. Conclusions These observations shed light on the specific environmental factors that contributed to a robust effect on the gut microbiome during spaceflight with important implications for mammalian metabolism. Our findings represent a key step toward a better understanding the role of the gut microbiome in mammalian health during spaceflight and provide a basis for future efforts to develop microbiota-based countermeasures that mitigate risks to crew health during long-term human space expeditions.
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spelling doaj.art-b619dc9664ff4898bc4c208989db34ca2022-12-21T19:17:23ZengBMCMicrobiome2049-26182019-08-017111810.1186/s40168-019-0724-4Reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflightPeng Jiang0Stefan J. Green1George E. Chlipala2Fred W. Turek3Martha Hotz Vitaterna4Center for Sleep and Circadian Biology, Department of Neurobiology, Northwestern UniversitySequencing Core, Research Resources Center, University of Illinois at ChicagoSequencing Core, Research Resources Center, University of Illinois at ChicagoCenter for Sleep and Circadian Biology, Department of Neurobiology, Northwestern UniversityCenter for Sleep and Circadian Biology, Department of Neurobiology, Northwestern UniversityAbstract Background Space environment imposes a range of challenges to mammalian physiology and the gut microbiota, and interactions between the two are thought to be important in mammalian health in space. While previous findings have demonstrated a change in the gut microbial community structure during spaceflight, specific environmental factors that alter the gut microbiome and the functional relevance of the microbiome changes during spaceflight remain elusive. Methods We profiled the microbiome using 16S rRNA gene amplicon sequencing in fecal samples collected from mice after a 37-day spaceflight onboard the International Space Station. We developed an analytical tool, named STARMAPs (Similarity Test for Accordant and Reproducible Microbiome Abundance Patterns), to compare microbiome changes reported here to other relevant datasets. We also integrated the gut microbiome data with the publically available transcriptomic data in the liver of the same animals for a systems-level analysis. Results We report an elevated microbiome alpha diversity and an altered microbial community structure that were associated with spaceflight environment. Using STARMAPs, we found the observed microbiome changes shared similarity with data reported in mice flown in a previous space shuttle mission, suggesting reproducibility of the effects of spaceflight on the gut microbiome. However, such changes were not comparable with those induced by space-type radiation in Earth-based studies. We found spaceflight led to significantly altered taxon abundance in one order, one family, five genera, and six species of microbes. This was accompanied by a change in the inferred microbial gene abundance that suggests an altered capacity in energy metabolism. Finally, we identified host genes whose expression in the liver were concordantly altered with the inferred gut microbial gene content, particularly highlighting a relationship between host genes involved in protein metabolism and microbial genes involved in putrescine degradation. Conclusions These observations shed light on the specific environmental factors that contributed to a robust effect on the gut microbiome during spaceflight with important implications for mammalian metabolism. Our findings represent a key step toward a better understanding the role of the gut microbiome in mammalian health during spaceflight and provide a basis for future efforts to develop microbiota-based countermeasures that mitigate risks to crew health during long-term human space expeditions.http://link.springer.com/article/10.1186/s40168-019-0724-4Space environmentMicrogravityCosmic radiation16S rRNA amplicon sequencingRNA-seq
spellingShingle Peng Jiang
Stefan J. Green
George E. Chlipala
Fred W. Turek
Martha Hotz Vitaterna
Reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflight
Microbiome
Space environment
Microgravity
Cosmic radiation
16S rRNA amplicon sequencing
RNA-seq
title Reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflight
title_full Reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflight
title_fullStr Reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflight
title_full_unstemmed Reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflight
title_short Reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflight
title_sort reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflight
topic Space environment
Microgravity
Cosmic radiation
16S rRNA amplicon sequencing
RNA-seq
url http://link.springer.com/article/10.1186/s40168-019-0724-4
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