Evolution and regulation of microbial secondary metabolism
- University of Lisboa, Portugal
- Memorial Sloan Kettering Cancer Center, United States
- Weill Cornell Medical College, United States
- 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.
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RNAseq filesNCBI Bioproject, PRJNA253624.
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Evolution and regulation of microbial secondary metabolismDryad Digital Repository, doi:10.5061/dryad.7sqv9s4tg.
Article and author information
Author details
Francisco Rodrigues Pinto
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
- Sara Mitri, University of Lausanne, Switzerland
Version history
- Preprint posted: September 3, 2020 (view preprint)
- Received: December 4, 2021
- Accepted: November 18, 2022
- Accepted Manuscript published: November 21, 2022 (version 1)
- Version of Record published: November 29, 2022 (version 2)
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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Evolution and regulation of microbial secondary metabolism
eLife 11:e76119.
https://doi.org/10.7554/eLife.76119
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