Evolution and regulation of microbial secondary metabolism

  1. Guillem Santamaria
  2. Chen Liao
  3. Chloe Lindberg
  4. Yanyan Chen
  5. Zhe Wang
  6. Kyu Rhee
  7. Francisco Rodrigues Pinto
  8. Jinyuan Yan  Is a corresponding author
  9. Joao B Xavier  Is a corresponding author
  1. University of Lisboa, Portugal
  2. Memorial Sloan Kettering Cancer Center, United States
  3. Weill Cornell Medical College, United States
  4. Memorial Sloan-Kettering Cancer Center, United States

Abstract

Microbes have disproportionate impacts on the macroscopic world. This is in part due to their ability to grow to large populations that collectively secrete massive amounts of secondary metabolites and alter their environment. Yet, the conditions favoring secondary metabolism despite the potential costs for primary metabolism remain unclear. Here we investigated the biosurfactants that the bacterium Pseudomonas aeruginosa makes and secretes to decrease the surface tension of surrounding liquid. Using a combination of genomics, metabolomics, transcriptomics, and mathematical modeling we show that the ability to make surfactants from glycerol varies inconsistently across the phylogenetic tree; instead, lineages that lost this ability are also worse at reducing the oxidative stress of primary metabolism on glycerol. Experiments with different carbon sources support a link with oxidative stress that explains the inconsistent distribution across the P. aeruginosa phylogeny and suggests a general principle: P. aeruginosa lineages produce surfactants if they can reduce the oxidative stress produced by primary metabolism and have excess resources, beyond their primary needs, to afford secondary metabolism. These results add a new layer to the regulation of a secondary metabolite unessential for primary metabolism but important to change physical properties of the environments surrounding bacterial populations.

Data availability

Sequencing data have been deposited in SRA, in the bioproject accession number PRJNA253624. Each individual sample has a file accession number listed in supporting table 7 provided. The additional dataset is provided through Dryad.

The following data sets were generated

Article and author information

Author details

  1. Guillem Santamaria

    3BioISI - Biosystems and Integrative Sciences Institute, University of Lisboa, Lisboa, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  2. Chen Liao

    Program for Computational and Systems Biology, Memorial Sloan Kettering Cancer Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8474-1196
  3. Chloe Lindberg

    Program for Computational and Systems Biology, Memorial Sloan Kettering Cancer Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Yanyan Chen

    Program for Computational and Systems Biology, Memorial Sloan Kettering Cancer Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Zhe Wang

    Department of Medicine, Weill Cornell Medical College, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Kyu Rhee

    Department of Medicine, Weill Cornell Medical College, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Francisco Rodrigues Pinto

    3BioISI - Biosystems and Integrative Sciences Institute, University of Lisboa, Lisboa, Portugal
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4217-0054
  8. Jinyuan Yan

    Computational & Systems Biology, Memorial Sloan-Kettering Cancer Center, New York, United States
    For correspondence
    yanj2@mskcc.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2046-5625
  9. Joao B Xavier

    Program for Computational and Systems Biology, Memorial Sloan Kettering Cancer Center, New York, United States
    For correspondence
    xavierj@mskcc.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3592-1689

Funding

National Institutes of Health (U01 AI124275)

  • Joao B Xavier

National Institutes of Health (R01 AI137269)

  • Joao B Xavier

FCT/Portugal (UIDB/04046/2020)

  • Francisco Rodrigues Pinto

FCT/Portugal (UIDP/04046/2020)

  • Francisco Rodrigues Pinto

European Research Council (734790)

  • Francisco Rodrigues Pinto

FCT/Portugal (SFRH/BD/142899/2018)

  • Guillem Santamaria

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

Reviewing Editor

  1. Sara Mitri, University of Lausanne, Switzerland

Publication history

  1. Received: December 4, 2021
  2. Accepted: November 18, 2022
  3. Accepted Manuscript published: November 21, 2022 (version 1)

Copyright

© 2022, Santamaria 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. Guillem Santamaria
  2. Chen Liao
  3. Chloe Lindberg
  4. Yanyan Chen
  5. Zhe Wang
  6. Kyu Rhee
  7. Francisco Rodrigues Pinto
  8. Jinyuan Yan
  9. Joao B Xavier
(2022)
Evolution and regulation of microbial secondary metabolism
eLife 11:e76119.
https://doi.org/10.7554/eLife.76119

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