Resilience of small intestinal beneficial bacteria to the toxicity of soybean oil fatty acids

  1. Sara C Di Rienzi
  2. Juliet Jacobson
  3. Elizabeth A Kennedy
  4. Mary E Bell
  5. Qiaojuan Shi
  6. Jillian L Waters
  7. Peter Lawrence
  8. J Thomas Brenna
  9. Robert A Britton
  10. Jens Walter
  11. Ruth Emily Ley  Is a corresponding author
  1. Max Planck Institute for Developmental Biology, Germany
  2. Cornell University, United States
  3. Baylor College of Medicine, United States
  4. University of Alberta, Canada

Abstract

Over the past century, soybean oil (SBO) consumption in the United States increased dramatically. The main SBO fatty acid, linoleic acid (18:2), inhibits in vitro the growth of lactobacilli, beneficial members of the small intestinal microbiota. Human-associated lactobacilli have declined in prevalence in Western microbiomes, but how dietary changes may have impacted their ecology is unclear. Here, we compared the in vitro and in vivo effects of 18:2 on Lactobacillus reuteri and L. johnsonii. Directed evolution in vitro in both species led to strong 18:2 resistance with mutations in genes for lipid biosynthesis, acid stress, and the cell membrane or wall. Small-intestinal Lactobacillus populations in mice were unaffected by chronic and acute 18:2 exposure, yet harbored both 18:2- sensitive and resistant strains. This work shows that extant small intestinal lactobacilli are protected from toxic dietary components via the gut environment as well as their own capacity to evolve resistance.

Article and author information

Author details

  1. Sara C Di Rienzi

    Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6188-663X
  2. Juliet Jacobson

    Department of Molecular Biology and Genetics, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
  3. Elizabeth A Kennedy

    Department of Molecular Biology and Genetics, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
  4. Mary E Bell

    Department of Molecular Biology and Genetics, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
  5. Qiaojuan Shi

    Department of Molecular Biology and Genetics, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
  6. Jillian L Waters

    Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    No competing interests declared.
  7. Peter Lawrence

    Division of Nutritional Sciences, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
  8. J Thomas Brenna

    Division of Nutritional Sciences, Cornell University, Ithaca, United States
    Competing interests
    No competing interests declared.
  9. Robert A Britton

    Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, United States
    Competing interests
    No competing interests declared.
  10. Jens Walter

    Department of Agriculture, Food, and Nutritional Science, University of Alberta, Edmonton, Canada
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1754-172X
  11. Ruth Emily Ley

    Department of Microbiome Science, Max Planck Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    ruth.ley@tuebingen.mpg.de
    Competing interests
    Ruth Emily Ley, Guest Reviewing Editor for eLife microbiome special issue.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9087-1672

Funding

NIH Office of the Director (DP2OD007444)

  • Ruth Emily Ley

Life Sciences Research Foundation (Eli & Edythe Broad Fellow)

  • Ruth Emily Ley

Max-Planck-Gesellschaft (Open-access funding)

  • Ruth Emily Ley

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Peter Turnbaugh, University of California, San Francisco, United States

Ethics

Animal experimentation: All animal experimental procedures were reviewed and approved by the Institutional Animal Care and Usage Committee of Cornell University protocol 2010-0065.

Version history

  1. Received: October 6, 2017
  2. Accepted: March 14, 2018
  3. Accepted Manuscript published: March 27, 2018 (version 1)
  4. Version of Record published: April 16, 2018 (version 2)

Copyright

© 2018, Di Rienzi et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Sara C Di Rienzi
  2. Juliet Jacobson
  3. Elizabeth A Kennedy
  4. Mary E Bell
  5. Qiaojuan Shi
  6. Jillian L Waters
  7. Peter Lawrence
  8. J Thomas Brenna
  9. Robert A Britton
  10. Jens Walter
  11. Ruth Emily Ley
(2018)
Resilience of small intestinal beneficial bacteria to the toxicity of soybean oil fatty acids
eLife 7:e32581.
https://doi.org/10.7554/eLife.32581

Share this article

https://doi.org/10.7554/eLife.32581

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  1. The microbiome protects beneficial gut bacteria from toxic substances in our diet.

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