The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa

Novel traits play a key role in evolution, but their origins remain poorly understood. Here we address this problem by using experimental evolution to study bacterial innovation in real time. We allowed 380 populations of Pseudomonas aeruginosa to adapt to 95 different carbon sources that challenged...

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Main Authors:	Toll-Riera, Macarena, San Millan, Alvaro, Wagner, Andreas, MacLean, R. Craig
Format:	Online
Language:	English
Published:	Public Library of Science 2016
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4858143/

id	pubmed-4858143
recordtype	oai_dc
spelling	pubmed-48581432016-05-13 The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa Toll-Riera, Macarena San Millan, Alvaro Wagner, Andreas MacLean, R. Craig Research Article Novel traits play a key role in evolution, but their origins remain poorly understood. Here we address this problem by using experimental evolution to study bacterial innovation in real time. We allowed 380 populations of Pseudomonas aeruginosa to adapt to 95 different carbon sources that challenged bacteria with either evolving novel metabolic traits or optimizing existing traits. Whole genome sequencing of more than 80 clones revealed profound differences in the genetic basis of innovation and optimization. Innovation was associated with the rapid acquisition of mutations in genes involved in transcription and metabolism. Mutations in pre-existing duplicate genes in the P. aeruginosa genome were common during innovation, but not optimization. These duplicate genes may have been acquired by P. aeruginosa due to either spontaneous gene amplification or horizontal gene transfer. High throughput phenotype assays revealed that novelty was associated with increased pleiotropic costs that are likely to constrain innovation. However, mutations in duplicate genes with close homologs in the P. aeruginosa genome were associated with low pleiotropic costs compared to mutations in duplicate genes with distant homologs in the P. aeruginosa genome, suggesting that functional redundancy between duplicates facilitates innovation by buffering pleiotropic costs. Public Library of Science 2016-05-05 /pmc/articles/PMC4858143/ /pubmed/27149698 http://dx.doi.org/10.1371/journal.pgen.1006005 Text en © 2016 Toll-Riera et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Toll-Riera, Macarena San Millan, Alvaro Wagner, Andreas MacLean, R. Craig
spellingShingle	Toll-Riera, Macarena San Millan, Alvaro Wagner, Andreas MacLean, R. Craig The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa
author_facet	Toll-Riera, Macarena San Millan, Alvaro Wagner, Andreas MacLean, R. Craig
author_sort	Toll-Riera, Macarena
title	The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa
title_short	The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa
title_full	The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa
title_fullStr	The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa
title_full_unstemmed	The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa
title_sort	genomic basis of evolutionary innovation in pseudomonas aeruginosa
description	Novel traits play a key role in evolution, but their origins remain poorly understood. Here we address this problem by using experimental evolution to study bacterial innovation in real time. We allowed 380 populations of Pseudomonas aeruginosa to adapt to 95 different carbon sources that challenged bacteria with either evolving novel metabolic traits or optimizing existing traits. Whole genome sequencing of more than 80 clones revealed profound differences in the genetic basis of innovation and optimization. Innovation was associated with the rapid acquisition of mutations in genes involved in transcription and metabolism. Mutations in pre-existing duplicate genes in the P. aeruginosa genome were common during innovation, but not optimization. These duplicate genes may have been acquired by P. aeruginosa due to either spontaneous gene amplification or horizontal gene transfer. High throughput phenotype assays revealed that novelty was associated with increased pleiotropic costs that are likely to constrain innovation. However, mutations in duplicate genes with close homologs in the P. aeruginosa genome were associated with low pleiotropic costs compared to mutations in duplicate genes with distant homologs in the P. aeruginosa genome, suggesting that functional redundancy between duplicates facilitates innovation by buffering pleiotropic costs.
publisher	Public Library of Science
publishDate	2016
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4858143/
_version_	1613576032987643904

The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa

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