Light-Stress Influences the Composition of the Murine Gut Microbiome, Memory Function, and Plasma Metabolome
Abstract
The gut microbiome plays an important role in the mammalian host and when in proper balance helps protect health and prevent disease. Host environmental stress and its influence on the gut microbiome, health, and disease is an emerging area of research. Exposures to unnatural light cycles are becoming increasingly common due to travel and shift work. However, much remains unknown about how these changes influence the microbiome and host health. This information is needed to understand and predict the relationship between the microbiome and host response to altered sleep cycles. In the present study, we exposed three cohorts of mice to different light cycle regimens for 12 consecutive weeks; including continuous light, continuous dark, and a standard light dark regimen consisting of 12 h light followed by 12 h of dark. After exposure, motor and memory behavior, and the composition of the fecal microbiome and plasma metabolome were measured. Memory potential was significantly reduced in mice exposed to continuous light, whereas rotarod performance was minimally affected. The overall composition of the microbiome was relatively constant over time. However, Bacteroidales Rikenellaceae was relatively more abundant in mice exposed to continuous dark, while Bacteroidales S24-7 was relatively more abundant in mice exposedmore »
- Authors:
-
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Div.
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Div.
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Computing and Analytics Div.
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1574891
- Alternate Identifier(s):
- OSTI ID: 1581324
- Report Number(s):
- PNNL-SA-144001
Journal ID: ISSN 2296-889X
- Grant/Contract Number:
- AC05-76RL01830; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Molecular Biosciences
- Additional Journal Information:
- Journal Volume: 6; Journal ID: ISSN 2296-889X
- Publisher:
- Frontiers Media SA
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; light stress; sleep cycle; gut microbiome; plasma metabolome; behavior change; memory function
Citation Formats
Kim, Young -Mo, Snijders, Antoine M., Brislawn, Colin J., Stratton, Kelly G., Zink, Erika M., Fansler, Sarah J., Metz, Thomas O., Mao, Jian -Hua, and Jansson, Janet K. Light-Stress Influences the Composition of the Murine Gut Microbiome, Memory Function, and Plasma Metabolome. United States: N. p., 2019.
Web. doi:10.3389/fmolb.2019.00108.
Kim, Young -Mo, Snijders, Antoine M., Brislawn, Colin J., Stratton, Kelly G., Zink, Erika M., Fansler, Sarah J., Metz, Thomas O., Mao, Jian -Hua, & Jansson, Janet K. Light-Stress Influences the Composition of the Murine Gut Microbiome, Memory Function, and Plasma Metabolome. United States. https://doi.org/10.3389/fmolb.2019.00108
Kim, Young -Mo, Snijders, Antoine M., Brislawn, Colin J., Stratton, Kelly G., Zink, Erika M., Fansler, Sarah J., Metz, Thomas O., Mao, Jian -Hua, and Jansson, Janet K. Fri .
"Light-Stress Influences the Composition of the Murine Gut Microbiome, Memory Function, and Plasma Metabolome". United States. https://doi.org/10.3389/fmolb.2019.00108. https://www.osti.gov/servlets/purl/1574891.
@article{osti_1574891,
title = {Light-Stress Influences the Composition of the Murine Gut Microbiome, Memory Function, and Plasma Metabolome},
author = {Kim, Young -Mo and Snijders, Antoine M. and Brislawn, Colin J. and Stratton, Kelly G. and Zink, Erika M. and Fansler, Sarah J. and Metz, Thomas O. and Mao, Jian -Hua and Jansson, Janet K.},
abstractNote = {The gut microbiome plays an important role in the mammalian host and when in proper balance helps protect health and prevent disease. Host environmental stress and its influence on the gut microbiome, health, and disease is an emerging area of research. Exposures to unnatural light cycles are becoming increasingly common due to travel and shift work. However, much remains unknown about how these changes influence the microbiome and host health. This information is needed to understand and predict the relationship between the microbiome and host response to altered sleep cycles. In the present study, we exposed three cohorts of mice to different light cycle regimens for 12 consecutive weeks; including continuous light, continuous dark, and a standard light dark regimen consisting of 12 h light followed by 12 h of dark. After exposure, motor and memory behavior, and the composition of the fecal microbiome and plasma metabolome were measured. Memory potential was significantly reduced in mice exposed to continuous light, whereas rotarod performance was minimally affected. The overall composition of the microbiome was relatively constant over time. However, Bacteroidales Rikenellaceae was relatively more abundant in mice exposed to continuous dark, while Bacteroidales S24-7 was relatively more abundant in mice exposed to continuous light. The plasma metabolome after the continuous dark exposure differed from the other exposure conditions. Several plasma metabolites, including glycolic acid, tryptophan, pyruvate, and several unidentified metabolites, were correlated to continuous dark and light exposure conditions. Networking analyses showed that serotonin was positively correlated with three microbial families (Rikenellaceae, Ruminococcaceae, and Turicibacteraceae), while tryptophan was negatively correlated with abundance of Bacteroidales S24-7 based on light exposure. This study provides the foundation for future studies into the mechanisms underlying the role of the gut microbiome on the murine host during light-dark stress.},
doi = {10.3389/fmolb.2019.00108},
journal = {Frontiers in Molecular Biosciences},
number = ,
volume = 6,
place = {United States},
year = {Fri Oct 18 00:00:00 EDT 2019},
month = {Fri Oct 18 00:00:00 EDT 2019}
}
Web of Science
Works referenced in this record:
Rhythmicity of the intestinal microbiota is regulated by gender and the host circadian clock
journal, August 2015
- Liang, Xue; Bushman, Frederic D.; FitzGerald, Garret A.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 33
Succession of microbial consortia in the developing infant gut microbiome
journal, July 2010
- Koenig, J. E.; Spor, A.; Scalfone, N.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
Stress & the gut-brain axis: Regulation by the microbiome
journal, December 2017
- Foster, Jane A.; Rinaman, Linda; Cryan, John F.
- Neurobiology of Stress, Vol. 7
Metabolomic analysis of mouse prefrontal cortex reveals upregulated analytes during wakefulness compared to sleep
journal, July 2018
- Bourdon, Allen K.; Spano, Giovanna Maria; Marshall, William
- Scientific Reports, Vol. 8, Issue 1
The intestinal microbiota regulates body composition through NFIL3 and the circadian clock
journal, August 2017
- Wang, Yuhao; Kuang, Zheng; Yu, Xiaofei
- Science, Vol. 357, Issue 6354
Improved Bacterial 16S rRNA Gene (V4 and V4-5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys
journal, December 2015
- Walters, William; Hyde, Embriette R.; Berg-Lyons, Donna
- mSystems, Vol. 1, Issue 1
Diurnality, nocturnality, and the evolution of primate visual systems
journal, January 2008
- Ankel-Simons, F.; Rasmussen, D. T.
- American Journal of Physical Anthropology, Vol. 137, Issue S47
Circadian Integration of Metabolism and Energetics
journal, December 2010
- Bass, J.; Takahashi, J. S.
- Science, Vol. 330, Issue 6009
Coordination of circadian timing in mammals
journal, August 2002
- Reppert, Steven M.; Weaver, David R.
- Nature, Vol. 418, Issue 6901
Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome
journal, November 2016
- Snijders, Antoine M.; Langley, Sasha A.; Kim, Young-Mo
- Nature Microbiology, Vol. 2, Issue 2
Circadian disruption and human health: a bidirectional relationship
journal, December 2018
- Abbott, Sabra M.; Malkani, Roneil; Zee, Phyllis C.
- European Journal of Neuroscience
MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses
journal, May 2016
- Nakayasu, Ernesto S.; Nicora, Carrie D.; Sims, Amy C.
- mSystems, Vol. 1, Issue 3
The future of NMR-based metabolomics
journal, February 2017
- Markley, John L.; Brüschweiler, Rafael; Edison, Arthur S.
- Current Opinion in Biotechnology, Vol. 43
Diet and Feeding Pattern Affect the Diurnal Dynamics of the Gut Microbiome
journal, December 2014
- Zarrinpar, Amir; Chaix, Amandine; Yooseph, Shibu
- Cell Metabolism, Vol. 20, Issue 6
Lachnospiraceae shift in the microbial community of mice faecal sample effects on water immersion restraint stress
journal, April 2017
- Li, Shiyin; Wang, Zelin; Yang, Yun
- AMB Express, Vol. 7, Issue 1
Constant darkness is a circadian metabolic signal in mammals
journal, January 2006
- Zhang, Jianfa; Kaasik, Krista; Blackburn, Michael R.
- Nature, Vol. 439, Issue 7074
Potential Role for the Gut Microbiota in Modulating Host Circadian Rhythms and Metabolic Health
journal, January 2019
- Parkar, Shanthi; Kalsbeek, Andries; Cheeseman, James
- Microorganisms, Vol. 7, Issue 2
Transkingdom Control of Microbiota Diurnal Oscillations Promotes Metabolic Homeostasis
journal, October 2014
- Thaiss, Christoph A.; Zeevi, David; Levy, Maayan
- Cell, Vol. 159, Issue 3
Effects of light and dark phase testing on the investigation of behavioural paradigms in mice: Relevance for behavioural neuroscience
journal, March 2019
- Richetto, Juliet; Polesel, Marcello; Weber-Stadlbauer, Ulrike
- Pharmacology Biochemistry and Behavior, Vol. 178
An Official American Thoracic Society Statement: The Importance of Healthy Sleep. Recommendations and Future Priorities
journal, June 2015
- Mukherjee, Sutapa; Patel, Sanjay R.; Kales, Stefanos N.
- American Journal of Respiratory and Critical Care Medicine, Vol. 191, Issue 12
Circadian rhythm disturbances in depression
journal, October 2008
- Germain, Anne; Kupfer, David J.
- Human Psychopharmacology: Clinical and Experimental, Vol. 23, Issue 7
Effects of Psychological, Environmental and Physical Stressors on the Gut Microbiota
journal, September 2018
- Karl, J. Philip; Hatch, Adrienne M.; Arcidiacono, Steven M.
- Frontiers in Microbiology, Vol. 9
Improved quality control processing of peptide-centric LC-MS proteomics data
journal, August 2011
- Matzke, Melissa M.; Waters, Katrina M.; Metz, Thomas O.
- Bioinformatics, Vol. 27, Issue 20
Functional interactions between the gut microbiota and host metabolism
journal, September 2012
- Tremaroli, Valentina; Bäckhed, Fredrik
- Nature, Vol. 489, Issue 7415
Current understanding of the human microbiome
journal, April 2018
- Gilbert, Jack A.; Blaser, Martin J.; Caporaso, J. Gregory
- Nature Medicine, Vol. 24, Issue 4
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012
- Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
- The ISME Journal, Vol. 6, Issue 8
The microbiome: stress, health and disease
journal, November 2013
- Moloney, Rachel D.; Desbonnet, Lieve; Clarke, Gerard
- Mammalian Genome, Vol. 25, Issue 1-2
MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis
journal, May 2009
- Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian
- Analytical Chemistry, Vol. 81, Issue 9
Circadian Disruption Changes Gut Microbiome Taxa and Functional Gene Composition
journal, April 2018
- Deaver, Jessica A.; Eum, Sung Y.; Toborek, Michal
- Frontiers in Microbiology, Vol. 9
Central and Peripheral Circadian Clocks in Mammals
journal, July 2012
- Mohawk, Jennifer A.; Green, Carla B.; Takahashi, Joseph S.
- Annual Review of Neuroscience, Vol. 35, Issue 1
Stress as a Normal Cue in the Symbiotic Environment
journal, May 2016
- Schwartzman, Julia A.; Ruby, Edward G.
- Trends in Microbiology, Vol. 24, Issue 5
Human Genetics Shape the Gut Microbiome
journal, November 2014
- Goodrich, Julia K.; Waters, Jillian L.; Poole, Angela C.
- Cell, Vol. 159, Issue 4
The shift work and health research agenda: Considering changes in gut microbiota as a pathway linking shift work, sleep loss and circadian misalignment, and metabolic disease
journal, August 2017
- Reynolds, Amy C.; Paterson, Jessica L.; Ferguson, Sally A.
- Sleep Medicine Reviews, Vol. 34
The gut microbiota in human energy homeostasis and obesity
journal, September 2015
- Rosenbaum, Michael; Knight, Rob; Leibel, Rudolph L.
- Trends in Endocrinology & Metabolism, Vol. 26, Issue 9
Theabrownin from Pu-erh tea together with swinging exercise synergistically ameliorates obesity and insulin resistance in rats
journal, July 2019
- Wu, Enkai; Zhang, Tingting; Tan, Chao
- European Journal of Nutrition, Vol. 59, Issue 5
Improved quality control processing of peptide-centric LC-MS proteomics data
text, January 2011
- G., Pounds, Joel; C., Sims, Amy; O., Metz, Thomas
- The University of North Carolina at Chapel Hill University Libraries
Effects of light and dark phase testing on the investigation of behavioural paradigms in mice: Relevance for behavioural neuroscience
text, January 2019
- Richetto, Juliet; Polesel, Marcello; Weber-Stadlbauer, Ulrike
- Elsevier
MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses
text, January 2016
- Bobbie-Jo, Webb-Robertson,; D., Smith, Richard; S., Nakayasu, Ernesto
- The University of North Carolina at Chapel Hill University Libraries
Diurnality, nocturnality, and the evolution of primate visual systems
journal, January 2008
- Ankel-Simons, F.; Rasmussen, D. T.
- American Journal of Physical Anthropology, Vol. 137, Issue S47
Circadian rhythm disturbances in depression
journal, October 2008
- Germain, Anne; Kupfer, David J.
- Human Psychopharmacology: Clinical and Experimental, Vol. 23, Issue 7
Transkingdom Control of Microbiota Diurnal Oscillations Promotes Metabolic Homeostasis
journal, October 2014
- Thaiss, Christoph A.; Zeevi, David; Levy, Maayan
- Cell, Vol. 159, Issue 3
Human Genetics Shape the Gut Microbiome
journal, November 2014
- Goodrich, Julia K.; Waters, Jillian L.; Poole, Angela C.
- Cell, Vol. 159, Issue 4
Diet and Feeding Pattern Affect the Diurnal Dynamics of the Gut Microbiome
journal, December 2014
- Zarrinpar, Amir; Chaix, Amandine; Yooseph, Shibu
- Cell Metabolism, Vol. 20, Issue 6
The future of NMR-based metabolomics
journal, February 2017
- Markley, John L.; Brüschweiler, Rafael; Edison, Arthur S.
- Current Opinion in Biotechnology, Vol. 43
Stress as a Normal Cue in the Symbiotic Environment
journal, May 2016
- Schwartzman, Julia A.; Ruby, Edward G.
- Trends in Microbiology, Vol. 24, Issue 5
MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis
journal, May 2009
- Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian
- Analytical Chemistry, Vol. 81, Issue 9
Constant darkness is a circadian metabolic signal in mammals
journal, January 2006
- Zhang, Jianfa; Kaasik, Krista; Blackburn, Michael R.
- Nature, Vol. 439, Issue 7074
Functional interactions between the gut microbiota and host metabolism
journal, September 2012
- Tremaroli, Valentina; Bäckhed, Fredrik
- Nature, Vol. 489, Issue 7415
Current understanding of the human microbiome
journal, April 2018
- Gilbert, Jack A.; Blaser, Martin J.; Caporaso, J. Gregory
- Nature Medicine, Vol. 24, Issue 4
Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome
journal, November 2016
- Snijders, Antoine M.; Langley, Sasha A.; Kim, Young-Mo
- Nature Microbiology, Vol. 2, Issue 2
Metabolomic analysis of mouse prefrontal cortex reveals upregulated analytes during wakefulness compared to sleep
journal, July 2018
- Bourdon, Allen K.; Spano, Giovanna Maria; Marshall, William
- Scientific Reports, Vol. 8, Issue 1
Rhythmicity of the intestinal microbiota is regulated by gender and the host circadian clock
journal, August 2015
- Liang, Xue; Bushman, Frederic D.; FitzGerald, Garret A.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 33
Circadian disruption and human health: a bidirectional relationship
journal, December 2018
- Abbott, Sabra M.; Malkani, Roneil; Zee, Phyllis C.
- European Journal of Neuroscience
Circadian Integration of Metabolism and Energetics
journal, December 2010
- Bass, J.; Takahashi, J. S.
- Science, Vol. 330, Issue 6009
The intestinal microbiota regulates body composition through NFIL3 and the circadian clock
journal, August 2017
- Wang, Yuhao; Kuang, Zheng; Yu, Xiaofei
- Science, Vol. 357, Issue 6354
The Host Microbiome Regulates and Maintains Human Health: A Primer and Perspective for Non-Microbiologists
journal, March 2017
- Thomas, Sunil; Izard, Jacques; Walsh, Emily
- Cancer Research, Vol. 77, Issue 8
Improved quality control processing of peptide-centric LC-MS proteomics data
text, January 2011
- G., Pounds, Joel; C., Sims, Amy; O., Metz, Thomas
- The University of North Carolina at Chapel Hill University Libraries
Circadian Disruption Changes Gut Microbiome Taxa and Functional Gene Composition
journal, April 2018
- Deaver, Jessica A.; Eum, Sung Y.; Toborek, Michal
- Frontiers in Microbiology, Vol. 9
Effects of Psychological, Environmental and Physical Stressors on the Gut Microbiota
journal, September 2018
- Karl, J. Philip; Hatch, Adrienne M.; Arcidiacono, Steven M.
- Frontiers in Microbiology, Vol. 9
Potential Role for the Gut Microbiota in Modulating Host Circadian Rhythms and Metabolic Health
journal, January 2019
- Parkar, Shanthi; Kalsbeek, Andries; Cheeseman, James
- Microorganisms, Vol. 7, Issue 2
Works referencing / citing this record:
Endogenous circadian time genes expressions in the liver of mice under constant darkness
journal, March 2020
- Li, Huan; Zhang, Shiyao; Zhang, Wenxiang
- BMC Genomics, Vol. 21, Issue 1
Endogenous circadian time genes expressions in the liver of mice under constant darkness
journal, March 2020
- Li, Huan; Zhang, Shiyao; Zhang, Wenxiang
- BMC Genomics, Vol. 21, Issue 1