Experimental Evolution of Metabolic Dependency in Bacteria

Bacteria frequently lose biosynthetic genes, thus making them dependent on an environmental uptake of the corresponding metabolite. Despite the ubiquity of this ‘genome streamlining’, it is generally unclear whether the concomitant loss of biosynthetic functions is favored by natural selection or ra...

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Main Authors: D’Souza, Glen, Kost, Christian
Format: Online
Language:English
Published: Public Library of Science 2016
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5096674/
id pubmed-5096674
recordtype oai_dc
spelling pubmed-50966742016-11-18 Experimental Evolution of Metabolic Dependency in Bacteria D’Souza, Glen Kost, Christian Research Article Bacteria frequently lose biosynthetic genes, thus making them dependent on an environmental uptake of the corresponding metabolite. Despite the ubiquity of this ‘genome streamlining’, it is generally unclear whether the concomitant loss of biosynthetic functions is favored by natural selection or rather caused by random genetic drift. Here we demonstrate experimentally that a loss of metabolic functions is strongly selected for when the corresponding metabolites can be derived from the environment. Serially propagating replicate populations of the bacterium Escherichia coli in amino acid-containing environments revealed that auxotrophic genotypes rapidly evolved in less than 2,000 generations in almost all replicate populations. Moreover, auxotrophs also evolved in environments lacking amino acids–yet to a much lesser extent. Loss of these biosynthetic functions was due to mutations in both structural and regulatory genes. In competition experiments performed in the presence of amino acids, auxotrophic mutants gained a significant fitness advantage over the evolutionary ancestor, suggesting their emergence was selectively favored. Interestingly, auxotrophic mutants derived amino acids not only via an environmental uptake, but also by cross-feeding from coexisting strains. Our results show that adaptive fitness benefits can favor biosynthetic loss-of-function mutants and drive the establishment of intricate metabolic interactions within microbial communities. Public Library of Science 2016-11-04 /pmc/articles/PMC5096674/ /pubmed/27814362 http://dx.doi.org/10.1371/journal.pgen.1006364 Text en © 2016 D’Souza, Kost 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 D’Souza, Glen
Kost, Christian
spellingShingle D’Souza, Glen
Kost, Christian
Experimental Evolution of Metabolic Dependency in Bacteria
author_facet D’Souza, Glen
Kost, Christian
author_sort D’Souza, Glen
title Experimental Evolution of Metabolic Dependency in Bacteria
title_short Experimental Evolution of Metabolic Dependency in Bacteria
title_full Experimental Evolution of Metabolic Dependency in Bacteria
title_fullStr Experimental Evolution of Metabolic Dependency in Bacteria
title_full_unstemmed Experimental Evolution of Metabolic Dependency in Bacteria
title_sort experimental evolution of metabolic dependency in bacteria
description Bacteria frequently lose biosynthetic genes, thus making them dependent on an environmental uptake of the corresponding metabolite. Despite the ubiquity of this ‘genome streamlining’, it is generally unclear whether the concomitant loss of biosynthetic functions is favored by natural selection or rather caused by random genetic drift. Here we demonstrate experimentally that a loss of metabolic functions is strongly selected for when the corresponding metabolites can be derived from the environment. Serially propagating replicate populations of the bacterium Escherichia coli in amino acid-containing environments revealed that auxotrophic genotypes rapidly evolved in less than 2,000 generations in almost all replicate populations. Moreover, auxotrophs also evolved in environments lacking amino acids–yet to a much lesser extent. Loss of these biosynthetic functions was due to mutations in both structural and regulatory genes. In competition experiments performed in the presence of amino acids, auxotrophic mutants gained a significant fitness advantage over the evolutionary ancestor, suggesting their emergence was selectively favored. Interestingly, auxotrophic mutants derived amino acids not only via an environmental uptake, but also by cross-feeding from coexisting strains. Our results show that adaptive fitness benefits can favor biosynthetic loss-of-function mutants and drive the establishment of intricate metabolic interactions within microbial communities.
publisher Public Library of Science
publishDate 2016
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5096674/
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