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Title: Identification of the potentiating mutations and synergistic epistasis that enabled the evolution of inter-species cooperation

Abstract

Microbes often engage in cooperation through releasing biosynthetic compounds required by other species to grow. Given that production of costly biosynthetic metabolites is generally subjected to multiple layers of negative feedback, single mutations may frequently be insufficient to generate cooperative phenotypes. Synergistic epistatic interactions between multiple coordinated changes may thus often underlie the evolution of cooperation through overproduction of metabolites. To test the importance of synergistic mutations in cooperation we used an engineered bacterial consortium of an Escherichia coli methionine auxotroph and Salmonella enterica. S. enterica relies on carbon by-products from E. coli if lactose is the only carbon source. Directly selecting wild-type S. enterica in an environment that favored cooperation through secretion of methionine only once led to a methionine producer, and this producer both took a long time to emerge and was not very effective at cooperating. On the other hand, when an initial selection for resistance of S. enterica to a toxic methionine analog, ethionine, was used, subsequent selection for cooperation with E. coli was rapid, and the resulting double mutants were much more effective at cooperation. We found that potentiating mutations in metJ increase expression of metA, which encodes the first step of methionine biosynthesis. Thismore » increase in expression is required for the previously identified actualizing mutations in metA to generate cooperation. This work highlights that where biosynthesis of metabolites involves multiple layers of regulation, significant secretion of those metabolites may require multiple mutations, thereby constraining the evolution of cooperation.« less

Authors:
 [1];  [2];  [3];  [4]
  1. Harvard Univ., Cambridge, MA (United States). Dept. of Molecular and Cellular Biology; Harvard Univ., Cambridge, MA (United States). Dept. of Orgasmic and Evolutionary Biology
  2. Harvard Univ., Cambridge, MA (United States). Dept. of Orgasmic and Evolutionary Biology; Univ. of Missouri, St. Louis, MO (United States). Dept. of Biology
  3. Harvard Univ., Cambridge, MA (United States). Dept. of Orgasmic and Evolutionary Biology; Univ. of Minnesota, St. Paul, MN (United States). Dept. of Ecology, Evolution, and Behavior
  4. Harvard Univ., Cambridge, MA (United States). Dept. of Orgasmic and Evolutionary Biology; Univ. of Idaho, Moscow, ID (United States). Dept. of Biological Sciences; Univ. of Idaho, Moscow, ID (United States). Inst. for Bioinformatics and Evolutionary Studies; Univ. of Idaho, Moscow, ID (United States). Center for Modeling Complex Ineractions
Publication Date:
Research Org.:
Harvard Univ., Cambridge, MA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1356458
Alternate Identifier(s):
OSTI ID: 1393571
Grant/Contract Number:  
SC0006731
Resource Type:
Journal Article: Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 12; Journal Issue: 5; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Douglas, Sarah M., Chubiz, Lon M., Harcombe, William R., and Marx, Christopher J. Identification of the potentiating mutations and synergistic epistasis that enabled the evolution of inter-species cooperation. United States: N. p., 2017. Web. doi:10.1371/journal.pone.0174345.
Douglas, Sarah M., Chubiz, Lon M., Harcombe, William R., & Marx, Christopher J. Identification of the potentiating mutations and synergistic epistasis that enabled the evolution of inter-species cooperation. United States. doi:10.1371/journal.pone.0174345.
Douglas, Sarah M., Chubiz, Lon M., Harcombe, William R., and Marx, Christopher J. Thu . "Identification of the potentiating mutations and synergistic epistasis that enabled the evolution of inter-species cooperation". United States. doi:10.1371/journal.pone.0174345.
@article{osti_1356458,
title = {Identification of the potentiating mutations and synergistic epistasis that enabled the evolution of inter-species cooperation},
author = {Douglas, Sarah M. and Chubiz, Lon M. and Harcombe, William R. and Marx, Christopher J.},
abstractNote = {Microbes often engage in cooperation through releasing biosynthetic compounds required by other species to grow. Given that production of costly biosynthetic metabolites is generally subjected to multiple layers of negative feedback, single mutations may frequently be insufficient to generate cooperative phenotypes. Synergistic epistatic interactions between multiple coordinated changes may thus often underlie the evolution of cooperation through overproduction of metabolites. To test the importance of synergistic mutations in cooperation we used an engineered bacterial consortium of an Escherichia coli methionine auxotroph and Salmonella enterica. S. enterica relies on carbon by-products from E. coli if lactose is the only carbon source. Directly selecting wild-type S. enterica in an environment that favored cooperation through secretion of methionine only once led to a methionine producer, and this producer both took a long time to emerge and was not very effective at cooperating. On the other hand, when an initial selection for resistance of S. enterica to a toxic methionine analog, ethionine, was used, subsequent selection for cooperation with E. coli was rapid, and the resulting double mutants were much more effective at cooperation. We found that potentiating mutations in metJ increase expression of metA, which encodes the first step of methionine biosynthesis. This increase in expression is required for the previously identified actualizing mutations in metA to generate cooperation. This work highlights that where biosynthesis of metabolites involves multiple layers of regulation, significant secretion of those metabolites may require multiple mutations, thereby constraining the evolution of cooperation.},
doi = {10.1371/journal.pone.0174345},
journal = {PLoS ONE},
number = 5,
volume = 12,
place = {United States},
year = {Thu May 11 00:00:00 EDT 2017},
month = {Thu May 11 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1371/journal.pone.0174345

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Works referenced in this record:

One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products
journal, May 2000

  • Datsenko, K. A.; Wanner, B. L.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645
  • DOI: 10.1073/pnas.120163297