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Title: Evolution of bidirectional costly mutualism from byproduct consumption

Abstract

Mutualisms are essential for life, yet it is unclear how they arise. A two-stage process has been proposed for the evolution of mutualisms that involve exchanges of two costly resources. First, costly provisioning by one species may be selected for if that species gains a benefit from costless byproducts generated by a second species, and cooperators get disproportionate access to byproducts. Selection could then drive the second species to provide costly resources in return. Previously, a synthetic consortium evolved the first stage of this scenario: Salmonella enterica evolved costly production of methionine in exchange for costless carbon byproducts generated by an auxotrophic Escherichia coli. Growth on agar plates localized the benefits of cooperation around methionine-secreting S. enterica. Here, we report that further evolution of these partners on plates led to hypercooperative E. coli that secrete the sugar galactose. Sugar secretion arose repeatedly across replicate communities and is costly to E. coli producers, but enhances the growth of S. enterica. The tradeoff between individual costs and group benefits led to maintenance of both cooperative and efficient E. coli genotypes in this spatially structured environment. This study provides an experimental example of de novo, bidirectional costly mutualism evolving from byproduct consumption. Themore » results validate the plausibility of costly cooperation emerging from initially costless exchange, a scenario widely used to explain the origin of the mutualistic species interactions that are central to life on Earth.« less

Authors:
ORCiD logo; ; ; ;
Publication Date:
Research Org.:
Harvard Univ., Cambridge, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Institutes of Health (NIH)
OSTI Identifier:
1478449
Alternate Identifier(s):
OSTI ID: 1610892
Grant/Contract Number:  
SC0006731; 1R01-GM121498
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 115 Journal Issue: 47; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; science & technology - other topics; mutualism; cross-feeding; genome-scale metabolic modeling

Citation Formats

Harcombe, William R., Chacón, Jeremy M., Adamowicz, Elizabeth M., Chubiz, Lon M., and Marx, Christopher J. Evolution of bidirectional costly mutualism from byproduct consumption. United States: N. p., 2018. Web. doi:10.1073/pnas.1810949115.
Harcombe, William R., Chacón, Jeremy M., Adamowicz, Elizabeth M., Chubiz, Lon M., & Marx, Christopher J. Evolution of bidirectional costly mutualism from byproduct consumption. United States. https://doi.org/10.1073/pnas.1810949115
Harcombe, William R., Chacón, Jeremy M., Adamowicz, Elizabeth M., Chubiz, Lon M., and Marx, Christopher J. Mon . "Evolution of bidirectional costly mutualism from byproduct consumption". United States. https://doi.org/10.1073/pnas.1810949115.
@article{osti_1478449,
title = {Evolution of bidirectional costly mutualism from byproduct consumption},
author = {Harcombe, William R. and Chacón, Jeremy M. and Adamowicz, Elizabeth M. and Chubiz, Lon M. and Marx, Christopher J.},
abstractNote = {Mutualisms are essential for life, yet it is unclear how they arise. A two-stage process has been proposed for the evolution of mutualisms that involve exchanges of two costly resources. First, costly provisioning by one species may be selected for if that species gains a benefit from costless byproducts generated by a second species, and cooperators get disproportionate access to byproducts. Selection could then drive the second species to provide costly resources in return. Previously, a synthetic consortium evolved the first stage of this scenario: Salmonella enterica evolved costly production of methionine in exchange for costless carbon byproducts generated by an auxotrophic Escherichia coli. Growth on agar plates localized the benefits of cooperation around methionine-secreting S. enterica. Here, we report that further evolution of these partners on plates led to hypercooperative E. coli that secrete the sugar galactose. Sugar secretion arose repeatedly across replicate communities and is costly to E. coli producers, but enhances the growth of S. enterica. The tradeoff between individual costs and group benefits led to maintenance of both cooperative and efficient E. coli genotypes in this spatially structured environment. This study provides an experimental example of de novo, bidirectional costly mutualism evolving from byproduct consumption. The results validate the plausibility of costly cooperation emerging from initially costless exchange, a scenario widely used to explain the origin of the mutualistic species interactions that are central to life on Earth.},
doi = {10.1073/pnas.1810949115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 47,
volume = 115,
place = {United States},
year = {Mon Oct 22 00:00:00 EDT 2018},
month = {Mon Oct 22 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1810949115

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Cited by: 65 works
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Works referenced in this record:

Identification of Mutations in Laboratory-Evolved Microbes from Next-Generation Sequencing Data Using breseq
book, January 2014


The Evolution of Reciprocal Altruism
journal, March 1971

  • Trivers, Robert L.
  • The Quarterly Review of Biology, Vol. 46, Issue 1
  • DOI: 10.1086/406755

A comprehensive genome‐scale reconstruction of Escherichia coli metabolism—2011
journal, January 2011

  • Orth, Jeffrey D.; Conrad, Tom M.; Na, Jessica
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.65

Resource competition and social conflict in experimental populations of yeast
journal, May 2006


Clarity: An Open-Source Manager for Laboratory Automation
journal, April 2013

  • Delaney, Nigel F.; Rojas Echenique, José I.; Marx, Christopher J.
  • Journal of Laboratory Automation, Vol. 18, Issue 2
  • DOI: 10.1177/2211068212460237

Can altruism evolve in purely viscous populations?
journal, July 1992

  • Wilson, D. S.; Pollock, G. B.; Dugatkin, L. A.
  • Evolutionary Ecology, Vol. 6, Issue 4
  • DOI: 10.1007/BF02270969

Species interactions differ in their genetic robustness
journal, April 2015


Constraint-based analysis of metabolic capacity of Salmonella typhimurium during host-pathogen interaction
journal, January 2009

  • Raghunathan, Anu; Reed, Jennifer; Shin, Sookil
  • BMC Systems Biology, Vol. 3, Issue 1
  • DOI: 10.1186/1752-0509-3-38

Preparation of Genomic DNA from Bacteria
journal, October 2001


Adding biotic complexity alters the metabolic benefits of mutualism: SELECTION FOR MUTUALISM IN A COMMUNITY CONTEXT
journal, June 2016

  • Harcombe, William R.; Betts, Alex; Shapiro, Jason W.
  • Evolution, Vol. 70, Issue 8
  • DOI: 10.1111/evo.12973

The Evolution of Cooperation
journal, June 2004

  • Sachs, Joel L.; Mueller, Ulrich G.; Wilcox, Thomas P.
  • The Quarterly Review of Biology, Vol. 79, Issue 2
  • DOI: 10.1086/383541

The Growth and Form of Bacterial Colonies
journal, October 1979


Competitive resource allocation to metabolic pathways contributes to overflow metabolisms and emergent properties in cross-feeding microbial consortia
journal, February 2018

  • Carlson, Ross P.; Beck, Ashley E.; Phalak, Poonam
  • Biochemical Society Transactions, Vol. 46, Issue 2
  • DOI: 10.1042/BST20170242

Metabolic Resource Allocation in Individual Microbes Determines Ecosystem Interactions and Spatial Dynamics
journal, May 2014


Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium
journal, September 2016


The spatial and metabolic basis of colony size variation
journal, January 2018

  • Chacón, Jeremy M.; Möbius, Wolfram; Harcombe, William R.
  • The ISME Journal, Vol. 12, Issue 3
  • DOI: 10.1038/s41396-017-0038-0

A general model for the evolution of mutualisms
journal, July 2006


Development of an Optimized Medium, Strain and High-Throughput Culturing Methods for Methylobacterium extorquens
journal, April 2013


Population Dynamics Constrain the Cooperative Evolution of Cross-Feeding
journal, January 2009


Cooperation and Competition in the Evolution of ATP-Producing Pathways
journal, April 2001


Pseudo-reciprocity: Investing in mutualism
journal, October 1986


Evolution of Cross‐Feeding in Microbial Populations
journal, June 2004

  • Pfeiffer, Thomas; Bonhoeffer, Sebastian
  • The American Naturalist, Vol. 163, Issue 6
  • DOI: 10.1086/383593

Identification of the potentiating mutations and synergistic epistasis that enabled the evolution of inter-species cooperation
journal, May 2017