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Title: Metabolome of human gut microbiome is predictive of host dysbiosis

Abstract

Background: Humans live in constant and vital symbiosis with a closely linked bacterial ecosystem called the microbiome, which influences many aspects of human health. When this microbial ecosystem becomes disrupted, the health of the human host can suffer; a condition called dysbiosis. The community compositions of human microbiomes also vary dramatically from individual to individual, and over time, making it difficult to uncover the underlying mechanisms linking the microbiome to human health. We propose that a microbiome’s interaction with its human host is not necessarily dependent upon the presence or absence of particular bacterial species, but instead is dependent on its community metabolome; an emergent property of the microbiome. Results: Using data from a previously published, longitudinal study of microbiome populations of the human gut, we extrapolated information about microbiome community enzyme profiles and metabolome models. Using machine learning techniques, we demonstrated that the aggregate predicted community enzyme function profiles and modeled metabolomes of a microbiome are more predictive of dysbiosis than either observed microbiome community composition or predicted enzyme function profiles. Conclusions: Specific enzyme functions and metabolites predictive of dysbiosis provide insights into the molecular mechanisms of microbiome–host interactions. The ability to use machine learning to predict dysbiosis frommore » microbiome community interaction data provides a potentially powerful tool for understanding the links between the human microbiome and human health, pointing to potential microbiome-based diagnostics and therapeutic interventions.« less

Authors:
 [1];  [2]
  1. Univ. of Illinois at Chicago, Chicago, IL (United States). Bioengineering Dept.; Argonne National Lab. (ANL), Argonne, IL (United States)
  2. Univ. of Illinois at Chicago, Chicago, IL (United States). Bioengineering Dept.
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1224066
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
GigaScience
Additional Journal Information:
Journal Volume: 4; Journal Issue: 1; Journal ID: ISSN 2047-217X
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; dysbiosis; gut microbiome; human microbiome; machine learning; metabolome modeling; metagenomics; microbial communities

Citation Formats

Larsen, Peter E., and Dai, Yang. Metabolome of human gut microbiome is predictive of host dysbiosis. United States: N. p., 2015. Web. doi:10.1186/s13742-015-0084-3.
Larsen, Peter E., & Dai, Yang. Metabolome of human gut microbiome is predictive of host dysbiosis. United States. doi:10.1186/s13742-015-0084-3.
Larsen, Peter E., and Dai, Yang. Mon . "Metabolome of human gut microbiome is predictive of host dysbiosis". United States. doi:10.1186/s13742-015-0084-3. https://www.osti.gov/servlets/purl/1224066.
@article{osti_1224066,
title = {Metabolome of human gut microbiome is predictive of host dysbiosis},
author = {Larsen, Peter E. and Dai, Yang},
abstractNote = {Background: Humans live in constant and vital symbiosis with a closely linked bacterial ecosystem called the microbiome, which influences many aspects of human health. When this microbial ecosystem becomes disrupted, the health of the human host can suffer; a condition called dysbiosis. The community compositions of human microbiomes also vary dramatically from individual to individual, and over time, making it difficult to uncover the underlying mechanisms linking the microbiome to human health. We propose that a microbiome’s interaction with its human host is not necessarily dependent upon the presence or absence of particular bacterial species, but instead is dependent on its community metabolome; an emergent property of the microbiome. Results: Using data from a previously published, longitudinal study of microbiome populations of the human gut, we extrapolated information about microbiome community enzyme profiles and metabolome models. Using machine learning techniques, we demonstrated that the aggregate predicted community enzyme function profiles and modeled metabolomes of a microbiome are more predictive of dysbiosis than either observed microbiome community composition or predicted enzyme function profiles. Conclusions: Specific enzyme functions and metabolites predictive of dysbiosis provide insights into the molecular mechanisms of microbiome–host interactions. The ability to use machine learning to predict dysbiosis from microbiome community interaction data provides a potentially powerful tool for understanding the links between the human microbiome and human health, pointing to potential microbiome-based diagnostics and therapeutic interventions.},
doi = {10.1186/s13742-015-0084-3},
journal = {GigaScience},
number = 1,
volume = 4,
place = {United States},
year = {2015},
month = {9}
}

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    Works referencing / citing this record:

    Supporting materials for "Metabolome of Human gut microbiome is predictive of host dysbiosis".
    dataset, January 2015

    • Larsen, Peter E.; Dai, Yang
    • GigaScience Database
    • DOI: 10.5524/100163

    Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein
    journal, January 2013

    • Russell, Wendy R.; Duncan, Sylvia H.; Scobbie, Lorraine
    • Molecular Nutrition & Food Research, Vol. 57, Issue 3
    • DOI: 10.1002/mnfr.201200594

    Role of the Gut in Modulating Lipoprotein Metabolism
    journal, June 2014

    • Hennessy, Alan A.; Ross, R. Paul; Fitzgerald, Gerald F.
    • Current Cardiology Reports, Vol. 16, Issue 8
    • DOI: 10.1007/s11886-014-0515-2

    Gut microbiota and obesity: Role in aetiology and potential therapeutic target
    journal, August 2014

    • Moran, Carthage P.; Shanahan, Fergus
    • Best Practice & Research Clinical Gastroenterology, Vol. 28, Issue 4
    • DOI: 10.1016/j.bpg.2014.07.005

    Signaling pathways bridging microbial-triggered inflammation and cancer
    journal, February 2013


    The Dynamics of the Human Infant Gut Microbiome in Development and in Progression toward Type 1 Diabetes
    journal, February 2015


    Gut brain axis: diet microbiota interactions and implications for modulation of anxiety and depression
    journal, April 2015


    The dynamic microbiome
    journal, February 2014


    Connexins in respiratory and gastrointestinal mucosal immunity
    journal, March 2014


    Beneficial modulation of the gut microbiota
    journal, March 2014


    An overview of fecal microbiota transplantation: techniques, indications, and outcomes
    journal, August 2013


    Bridging immunity and lipid metabolism by gut microbiota
    journal, August 2013

    • Greer, Renee L.; Morgun, Andrey; Shulzhenko, Natalia
    • Journal of Allergy and Clinical Immunology, Vol. 132, Issue 2
    • DOI: 10.1016/j.jaci.2013.06.025

    The gut microbiota and inflammatory noncommunicable diseases: Associations and potentials for gut microbiota therapies
    journal, January 2015

    • West, Christina E.; Renz, Harald; Jenmalm, Maria C.
    • Journal of Allergy and Clinical Immunology, Vol. 135, Issue 1
    • DOI: 10.1016/j.jaci.2014.11.012

    Functional genomic and metagenomic approaches to understanding gut microbiota–animal mutualism
    journal, April 2015


    Biological significance of dietary polyamines
    journal, January 2007


    The “psychomicrobiotic”: Targeting microbiota in major psychiatric disorders: A systematic review
    journal, February 2015


    The involvement of gut microbiota in inflammatory bowel disease pathogenesis: Potential for therapy
    journal, May 2015


    The Ins and Outs of siderophore mediated iron uptake by extra-intestinal pathogenic Escherichia coli
    journal, November 2011


    Satellite remote sensing data can be used to model marine microbial metabolite turnover
    journal, July 2014

    • Larsen, Peter E.; Scott, Nicole; Post, Anton F.
    • The ISME Journal, Vol. 9, Issue 1
    • DOI: 10.1038/ismej.2014.107

    Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission
    journal, February 2014

    • Rooks, Michelle G.; Veiga, Patrick; Wardwell-Scott, Leslie H.
    • The ISME Journal, Vol. 8, Issue 7
    • DOI: 10.1038/ismej.2014.3

    Genomic variation landscape of the human gut microbiome
    journal, December 2012

    • Schloissnig, Siegfried; Arumugam, Manimozhiyan; Sunagawa, Shinichi
    • Nature, Vol. 493, Issue 7430
    • DOI: 10.1038/nature11711

    Diet rapidly and reproducibly alters the human gut microbiome
    journal, December 2013

    • David, Lawrence A.; Maurice, Corinne F.; Carmody, Rachel N.
    • Nature, Vol. 505, Issue 7484
    • DOI: 10.1038/nature12820

    Dynamics and associations of microbial community types across the human body
    journal, April 2014


    Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
    journal, August 2013

    • Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory
    • Nature Biotechnology, Vol. 31, Issue 9
    • DOI: 10.1038/nbt.2676

    Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection
    journal, January 2014

    • Theriot, Casey M.; Koenigsknecht, Mark J.; Carlson, Paul E.
    • Nature Communications, Vol. 5, Issue 1
    • DOI: 10.1038/ncomms4114

    Current understanding of the human microbiome
    journal, April 2018

    • Gilbert, Jack A.; Blaser, Martin J.; Caporaso, J. Gregory
    • Nature Medicine, Vol. 24, Issue 4
    • DOI: 10.1038/nm.4517

    Predicting bacterial community assemblages using an artificial neural network approach
    journal, April 2012

    • Larsen, Peter E.; Field, Dawn; Gilbert, Jack A.
    • Nature Methods, Vol. 9, Issue 6
    • DOI: 10.1038/nmeth.1975

    Antibiotics in early life and obesity
    journal, December 2014


    A role for the gut microbiota in IBS
    journal, April 2014


    Maternal influences on fetal microbial colonization and immune development
    journal, October 2014

    • Romano-Keeler, Joann; Weitkamp, Jörn-Hendrik
    • Pediatric Research, Vol. 77, Issue 1-2
    • DOI: 10.1038/pr.2014.163

    Of the bugs that shape us: maternal obesity, the gut microbiome, and long-term disease risk
    journal, October 2014

    • Gohir, Wajiha; Ratcliffe, Elyanne M.; Sloboda, Deborah M.
    • Pediatric Research, Vol. 77, Issue 1-2
    • DOI: 10.1038/pr.2014.169

    Gut microbiota: a source of novel tools to reduce the risk of human disease?
    journal, October 2014

    • Collado, Maria Carmen; Rautava, Samuli; Isolauri, Erika
    • Pediatric Research, Vol. 77, Issue 1-2
    • DOI: 10.1038/pr.2014.173

    The human gut microbiota: a dynamic interplay with the host from birth to senescence settled during childhood
    journal, April 2014

    • Putignani, Lorenza; Del Chierico, Federica; Petrucca, Andrea
    • Pediatric Research, Vol. 76, Issue 1
    • DOI: 10.1038/pr.2014.49

    Manipulation of the Microbiota for Treatment of IBS and IBD—Challenges and Controversies
    journal, May 2014


    The Microbiome in Inflammatory Bowel Disease: Current Status and the Future Ahead
    journal, May 2014


    The Intestinal Metabolome: An Intersection Between Microbiota and Host
    journal, May 2014


    Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
    journal, November 2003


    Review article: evidence for the role of gut microbiota in irritable bowel syndrome and its potential influence on therapeutic targets
    journal, March 2014

    • DuPont, H. L.
    • Alimentary Pharmacology & Therapeutics, Vol. 39, Issue 10
    • DOI: 10.1111/apt.12728

    Metagenomics of human microbiome: beyond 16s rDNA
    journal, July 2012


    Role of the gut microbiota in human nutrition and metabolism: Role of the gut microbiota
    journal, November 2013

    • Ramakrishna, Balakrishnan S.
    • Journal of Gastroenterology and Hepatology, Vol. 28
    • DOI: 10.1111/jgh.12294

    Longitudinal analysis of microbial interaction between humans and the indoor environment
    journal, August 2014


    Dysbiosis in inflammatory bowel disease
    journal, January 2004


    Does the microbiota play a role in the pathogenesis of autoimmune diseases?
    journal, November 2014


    Vitamin D, immune regulation, the microbiota, and inflammatory bowel disease
    journal, March 2014

    • Cantorna, Margherita T.; McDaniel, Kaitlin; Bora, Stephanie
    • Experimental Biology and Medicine, Vol. 239, Issue 11
    • DOI: 10.1177/1535370214523890

    Predicted Relative Metabolomic Turnover (PRMT): determining metabolic turnover from a coastal marine metagenomic dataset
    journal, June 2011

    • Larsen, Peter E.; Collart, Frank R.; Field, Dawn
    • Microbial Informatics and Experimentation, Vol. 1, Issue 1
    • DOI: 10.1186/2042-5783-1-4

    Host lifestyle affects human microbiota on daily timescales
    journal, January 2014

    • David, Lawrence A.; Materna, Arne C.; Friedman, Jonathan
    • Genome Biology, Vol. 15, Issue 7
    • DOI: 10.1186/gb-2014-15-7-r89

    Impact of prematurity and nutrition on the developing gut microbiome and preterm infant growth
    journal, December 2017


    Predicting Ecological Roles in the Rhizosphere Using Metabolome and Transportome Modeling
    journal, September 2015


    Metabolic Effects of Bile Acids in the Gut in Health and Disease
    journal, July 2014


    Folate Production by Probiotic Bacteria
    journal, January 2011

    • Rossi, Maddalena; Amaretti, Alberto; Raimondi, Stefano
    • Nutrients, Vol. 3, Issue 1
    • DOI: 10.3390/nu3010118

    Fecal microbiota transplantation broadening its application beyond intestinal disorders
    journal, January 2015


    Application of metagenomics in the human gut microbiome
    journal, January 2015

    • Wang, Wei-Lin; Xu, Shao-Yan; Ren, Zhi-Gang
    • World Journal of Gastroenterology, Vol. 21, Issue 3
    • DOI: 10.3748/wjg.v21.i3.803

    Current Status and Prospects of Intestinal Microbiome Studies
    journal, January 2014


    AMON: annotation of metabolite origins via networks to integrate microbiome and metabolome data
    journal, November 2019


    Current understanding of the human microbiome
    journal, April 2018

    • Gilbert, Jack A.; Blaser, Martin J.; Caporaso, J. Gregory
    • Nature Medicine, Vol. 24, Issue 4
    • DOI: 10.1038/nm.4517

    Association of oral microbiome with type 2 diabetes risk
    journal, February 2017

    • Long, J.; Cai, Q.; Steinwandel, M.
    • Journal of Periodontal Research, Vol. 52, Issue 3
    • DOI: 10.1111/jre.12432

    AMON: annotation of metabolite origins via networks to integrate microbiome and metabolome data
    journal, November 2019


    Impact of prematurity and nutrition on the developing gut microbiome and preterm infant growth
    journal, December 2017