Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome

Snijders, Antoine M.; Langley, Sasha A.; Kim, Young-Mo; Brislawn, Colin J.; Noecker, Cecilia; Zink, Erika M.; Fansler, Sarah J.; Casey, Cameron P.; Miller, Darla R.; Huang, Yurong; Karpen, Gary H.; Celniker, Susan E.; Brown, James B.; Borenstein, Elhanan; Jansson, Janet K.; Metz, Thomas O.; Mao, Jian-Hua

doi:10.1038/nmicrobiol.2016.221

Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome

Journal Article · Mon Nov 28 04:00:00 EST 2016 · Nature Microbiology

DOI:https://doi.org/10.1038/nmicrobiol.2016.221· OSTI ID:1393596

Snijders, Antoine M.; Langley, Sasha A.; ; Brislawn, Colin J.; Noecker, Cecilia; Zink, Erika M.; Fansler, Sarah J.; Casey, Cameron P.; Miller, Darla R.; Huang, Yurong; ; Celniker, Susan E.; Brown, James B.; Borenstein, Elhanan; Jansson, Janet K.; Metz, Thomas O.; Mao, Jian-Hua

Although the gut microbiome plays important roles in host physiology, health and disease1, we lack understanding of the complex interplay between host genetics and early life environment on the microbial and metabolic composition of the gut.We used the genetically diverse Collaborative Cross mouse system2 to discover that early life history impacts themicrobiome composition, whereas dietary changes have only a moderate effect. By contrast, the gut metabolome was shaped mostly by diet, with specific non-dietary metabolites explained by microbial metabolism. Quantitative trait analysis identified mouse genetic trait loci (QTL) that impact the abundances of specific microbes. Human orthologues of genes in the mouse QTL are implicated in gastrointestinal cancer. Additionally, genes located in mouse QTL for Lactobacillales abundance are implicated in arthritis, rheumatic disease and diabetes. Furthermore, Lactobacillales abundance was predictive of higher host T-helper cell counts, suggesting an important link between Lactobacillales and host adaptive immunity.

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

DOE Contract Number:: AC02-05CH11231

OSTI ID:: 1393596

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Vol. 2; ISSN 2058-5276

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

References (44)

Importance of Sulfur-Containing Metabolites in Discriminating Fecal Extracts between Normal and Type-2 Diabetic Mice Walker, Alesia; Lucio, Marianna; Pfitzner, Barbara Journal of Proteome Research, Vol. 13, Issue 10 https://doi.org/10.1021/pr500046b	journal	September 2014
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
A genome-wide approach accounting for body mass index identifies genetic variants influencing fasting glycemic traits and insulin resistance Manning, Alisa K.; Hivert, Marie-France; Scott, Robert A. Nature Genetics, Vol. 44, Issue 6 https://doi.org/10.1038/ng.2274	journal	May 2012
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) Sumner, Lloyd W.; Amberg, Alexander; Barrett, Dave Metabolomics, Vol. 3, Issue 3 https://doi.org/10.1007/s11306-007-0082-2	journal	September 2007
Circos: An information aesthetic for comparative genomics Krzywinski, M.; Schein, J.; Birol, I. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.092759.109	journal	June 2009
Genome-wide trans-ancestry meta-analysis provides insight into the genetic architecture of type 2 diabetes susceptibility Mahajan, Anubha; Go, Min Jin; Zhang, Weihua Nature Genetics, Vol. 46, Issue 3 https://doi.org/10.1038/ng.2897	journal	February 2014
The Mouse Genome Database (MGD): facilitating mouse as a model for human biology and disease Eppig, Janan T.; Blake, Judith A.; Bult, Carol J. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku967	journal	October 2014
PROX1 Gene Variant is Associated with Fasting Glucose Change After Antihypertensive Treatment Gong, Yan; McDonough, Caitrin W.; Beitelshees, Amber L. Pharmacotherapy: The Journal of Human Pharmacology and Drug Therapy, Vol. 34, Issue 2 https://doi.org/10.1002/phar.1355	journal	October 2013
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors Benson, A. K.; Kelly, S. A.; Legge, R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 44 https://doi.org/10.1073/pnas.1007028107	journal	October 2010
The Collaborative Cross, developing a resource for mammalian systems genetics: A status report of the Wellcome Trust cohort Iraqi, Fuad A.; Churchill, Gary; Mott, Richard Mammalian Genome, Vol. 19, Issue 6 https://doi.org/10.1007/s00335-008-9113-1	journal	June 2008
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities Lozupone, C.; Knight, R. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8228-8235.2005	journal	December 2005
Identification of genetic factors that modify motor performance and body weight using Collaborative Cross mice Mao, Jian-Hua; Langley, Sasha A.; Huang, Yurong Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep16247	journal	November 2015
UCHIME improves sensitivity and speed of chimera detection Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C. Bioinformatics, Vol. 27, Issue 16 https://doi.org/10.1093/bioinformatics/btr381	journal	June 2011
Gut microbiota and probiotics: Focus on diabetes mellitus Bordalo Tonucci, Livia; Dos Santos, Karina Maria Olbrich; De Luces Fortes Ferreira, Celia Lucia Critical Reviews in Food Science and Nutrition, Vol. 57, Issue 11 https://doi.org/10.1080/10408398.2014.934438	journal	April 2015
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization Mohamadzadeh, M.; Olson, S.; Kalina, W. V. Proceedings of the National Academy of Sciences, Vol. 102, Issue 8 https://doi.org/10.1073/pnas.0500098102	journal	February 2005
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Metabolic Model-Based Integration of Microbiome Taxonomic and Metabolomic Profiles Elucidates Mechanistic Links between Ecological and Metabolic Variation Noecker, Cecilia; Eng, Alexander; Srinivasan, Sujatha mSystems, Vol. 1, Issue 1 https://doi.org/10.1128/mSystems.00013-15	journal	December 2015
The Genome Architecture of the Collaborative Cross Mouse Genetic Reference Population Consortium, Collaborative Cross Genetics, Vol. 190, Issue 2, p. 389-401 https://doi.org/10.1534/genetics.111.132639	journal	January 2012
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea McDonald, Daniel; Price, Morgan N.; Goodrich, Julia The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.139	journal	December 2011
Human Genetics Shape the Gut Microbiome Goodrich, Julia K.; Waters, Jillian L.; Poole, Angela C. Cell, Vol. 159, Issue 4 https://doi.org/10.1016/j.cell.2014.09.053	journal	November 2014
Genome-Wide Association Study of a Heart Failure Related Metabolomic Profile Among African Americans in the Atherosclerosis Risk in Communities (ARIC) Study Yu, Bing; Zheng, Yan; Alexander, Danny Genetic Epidemiology, Vol. 37, Issue 8 https://doi.org/10.1002/gepi.21752	journal	August 2013
Improved Bacterial 16S rRNA Gene (V4 and V4-5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys Walters, William; Hyde, Embriette R.; Berg-Lyons, Donna mSystems, Vol. 1, Issue 1 https://doi.org/10.1128/mSystems.00009-15	journal	December 2015
Murine Gut Microbiota Is Defined by Host Genetics and Modulates Variation of Metabolic Traits McKnite, Autumn M.; Perez-Munoz, Maria Elisa; Lu, Lu PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0039191	journal	June 2012
The Collaborative Cross at Oak Ridge National Laboratory: developing a powerful resource for systems genetics Chesler, Elissa J.; Miller, Darla R.; Branstetter, Lisa R. Mammalian Genome, Vol. 19, Issue 6 https://doi.org/10.1007/s00335-008-9135-8	journal	June 2008
MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian Analytical Chemistry, Vol. 81, Issue 9 https://doi.org/10.1021/ac802689c	journal	May 2009
Status and access to the Collaborative Cross population Welsh, Catherine E.; Miller, Darla R.; Manly, Kenneth F. Mammalian Genome, Vol. 23, Issue 9-10 https://doi.org/10.1007/s00335-012-9410-6	journal	July 2012
MUSiCC: a marker genes based framework for metagenomic normalization and accurate profiling of gene abundances in the microbiome Manor, Ohad; Borenstein, Elhanan Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0610-8	journal	March 2015
FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry Kind, Tobias; Wohlgemuth, Gert; Lee, Do Yup Analytical Chemistry, Vol. 81, Issue 24 https://doi.org/10.1021/ac9019522	journal	December 2009
Salmonella modulates metabolism during growth under conditions that induce expression of virulence genes Kim, Young-Mo; Schmidt, Brian J.; Kidwai, Afshan S. Molecular BioSystems, Vol. 9, Issue 6 https://doi.org/10.1039/c3mb25598k	journal	January 2013
MHC variation sculpts individualized microbial communities that control susceptibility to enteric infection Kubinak, Jason L.; Stephens, W. Zac; Soto, Ray Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9642	journal	October 2015
ggbio: an R package for extending the grammar of graphics for genomic data Yin, Tengfei; Cook, Dianne; Lawrence, Michael Genome Biology, Vol. 13, Issue 8 https://doi.org/10.1186/gb-2012-13-8-r77	journal	January 2012
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Establishment of “The Gene Mine”: a resource for rapid identification of complex trait genes Morahan, Grant; Balmer, Lois; Monley, Donald Mammalian Genome, Vol. 19, Issue 6 https://doi.org/10.1007/s00335-008-9134-9	journal	June 2008
Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve Bravo, J. A.; Forsythe, P.; Chew, M. V. Proceedings of the National Academy of Sciences, Vol. 108, Issue 38 https://doi.org/10.1073/pnas.1102999108	journal	August 2011
Combined linkage and association analyses identify a novel locus for obesity near PROX1 in Asians : Novel Locus for Obesity Near Kim, Hyun-Jin; Yoo, Yun Joo; Ju, Young Seok Obesity, Vol. 21, Issue 11 https://doi.org/10.1002/oby.20153	journal	July 2013
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
Host genetic architecture and the landscape of microbiome composition: humans weigh in Benson, Andrew K. Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0775-1	journal	September 2015
The Impact of the Gut Microbiota on Human Health: An Integrative View Clemente, Jose C.; Ursell, Luke K.; Parfrey, Laura Wegener Cell, Vol. 148, Issue 6 https://doi.org/10.1016/j.cell.2012.01.035	journal	March 2012
Use of Probiotics in HIV-infected Children: A Randomized Double-blind Controlled Study Trois, L.; Cardoso, E. M.; Miura, E. Journal of Tropical Pediatrics, Vol. 54, Issue 1 https://doi.org/10.1093/tropej/fmm066	journal	November 2007
Creating reference gene annotation for the mouse C57BL6/J genome assembly Mudge, Jonathan M.; Harrow, Jennifer Mammalian Genome, Vol. 26, Issue 9-10 https://doi.org/10.1007/s00335-015-9583-x	journal	July 2015
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory Nature Biotechnology, Vol. 31, Issue 9 https://doi.org/10.1038/nbt.2676	journal	August 2013

Similar Records

Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome

Journal Article · Sun Nov 27 23:00:00 EST 2016 · Nature Microbiology · OSTI ID:1342294

Impact of Dietary Resistant Starch on the Human Gut Microbiome, Metaproteome, and Metabolome

Journal Article · Tue Nov 07 19:00:00 EST 2017 · mBio · OSTI ID:1786916

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome

Citation Formats

References (44)

Similar Records

Related Subjects