skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Evolution of bidirectional costly mutualism from byproduct consumption

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America

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.

Research Organization:
Harvard Univ., Cambridge, MA (United States)
Sponsoring Organization:
USDOE Office of Science (SC); National Institutes of Health (NIH)
Grant/Contract Number:
SC0006731; 1R01-GM121498
OSTI ID:
1478449
Alternate ID(s):
OSTI ID: 1610892
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 115 Journal Issue: 47; ISSN 0027-8424
Publisher:
National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 65 works
Citation information provided by
Web of Science

References (23)

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
A comprehensive genome‐scale reconstruction of Escherichia coli metabolism—2011 journal January 2011
Resource competition and social conflict in experimental populations of yeast journal May 2006
Clarity: An Open-Source Manager for Laboratory Automation journal April 2013
Can altruism evolve in purely viscous populations? journal July 1992
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
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
The Evolution of Cooperation journal June 2004
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
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
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
Identification of the potentiating mutations and synergistic epistasis that enabled the evolution of inter-species cooperation journal May 2017