Morphine and high-fat diet differentially alter the gut microbiota composition and metabolic function in lean versus obese mice

Blakeley-Ruiz, J. Alfredo; McClintock, Carlee S.; Shrestha, Him K.; Poudel, Suresh; Yang, Zamin K.; Giannone, Richard J.; Choo, James J.; Podar, Mircea; Baghdoyan, Helen A.; Lydic, Ralph; Hettich, Robert L.

doi:10.1038/s43705-022-00131-6

Title: Morphine and high-fat diet differentially alter the gut microbiota composition and metabolic function in lean versus obese mice

Journal Article · Fri Aug 05 00:00:00 UTC 2022 · ISME Communications

DOI: https://doi.org/10.1038/s43705-022-00131-6 · OSTI ID:1908093

Blakeley-Ruiz, J. Alfredo ^[1]; McClintock, Carlee S. ^[2];

^[1]; Poudel, Suresh ^[3]; Yang, Zamin K. ^[3];

^[3]; Choo, James J. ^[4];

^[3];

^[5];

^[3]

Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Pain Consultants of East Tennessee, PLLC, Knoxville, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Pain Consultants of East Tennessee, PLLC, Knoxville, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States)

There are known associations between opioids, obesity, and the gut microbiome, but the molecular connection/mediation of these relationships is not understood. To better clarify the interplay of physiological, genetic, and microbial factors, this study investigated the microbiome and host inflammatory responses to chronic opioid administration in genetically obese, diet-induced obese, and lean mice. Samples of feces, urine, colon tissue, and plasma were analyzed using targeted LC-MS/MS quantification of metabolites, immunoassays of inflammatory cytokine levels, genome-resolved metagenomics, and metaproteomics. Genetic obesity, diet-induced obesity, and morphine treatment in lean mice each showed increases in distinct inflammatory cytokines. Metagenomic assembly and binning uncovered over 400 novel gut bacterial genomes and species. Morphine administration impacted the microbiome’s composition and function, with the strongest effect observed in lean mice. This microbiome effect was less pronounced than either diet or genetically driven obesity. Based on inferred microbial physiology from the metaproteome datasets, a high-fat diet transitioned constituent microbes away from harvesting diet-derived nutrients and towards nutrients present in the host mucosal layer. Considered together, these results identified novel host-dependent phenotypes, differentiated the effects of genetic obesity versus diet induced obesity on gut microbiome composition and function, and showed that chronic morphine administration altered the gut microbiome.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1908093

Journal Information:: ISME Communications, Journal Name: ISME Communications Journal Issue: 1 Vol. 2; ISSN 2730-6151

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

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The Role of the Bacterial Flagellum in Adhesion and Virulence Haiko, Johanna; Westerlund-Wikström, Benita Biology, Vol. 2, Issue 4 https://doi.org/10.3390/biology2041242	journal	October 2013
Eosinophils in the gastrointestinal tract and their role in the pathogenesis of major colorectal disorders Loktionov, Alexandre World Journal of Gastroenterology, Vol. 25, Issue 27 https://doi.org/10.3748/wjg.v25.i27.3503	journal	July 2019
The impact of sequence database choice on metaproteomic results in gut microbiota studies Tanca, Alessandro; Palomba, Antonio; Fraumene, Cristina Figshare https://doi.org/10.6084/m9.figshare.c.3621314.v1	collection	January 2016
MetaPro-IQ: a universal metaproteomic approach to studying human and mouse gut microbiota Zhang, Xu; Ning, Zhibin; Mayne, Janice figshare https://doi.org/10.6084/m9.figshare.c.3640535.v1	collection	January 2016
Genome-resolved metaproteomic characterization of preterm infant gut microbiota development reveals species-specific metabolic shifts and variabilities during early life [Supplementary Data] Xiong, Weili; Brown, Christopher; Morowitz, Michael Figshare-Supplementary information for journal article at DOI: 10.1186/s40168-017-0290-6, 9 files https://doi.org/10.6084/m9.figshare.c.3823267	dataset	July 2017
Metaproteomics reveals persistent and phylum-redundant metabolic functional stability in adult human gut microbiomes of Crohn’s remission patients despite temporal variations in microbial taxa, genomes, and proteomes Blakeley-Ruiz, J.; Erickson, Alison; Cantarel, Brandi Figshare https://doi.org/10.6084/m9.figshare.c.4397387	collection	January 2019
The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research Sert, Nathalie Percie Du; Hurst, Viki; Ahluwalia, Amrita figshare https://doi.org/10.6084/m9.figshare.c.5058343.v1	collection	January 2020
Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies Kang, Dongwan D.; Li, Feng; Kirton, Edward PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7359	journal	January 2019

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