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Title: Adding biotic complexity alters the metabolic benefits of mutualism

Abstract

Mutualism is ubiquitous in nature and plays an integral role in most communities. To predict the eco-evolutionary dynamics of mutualism it is critical to extend classic pairwise analysis to include additional species. We investigated the effect of adding a third species to a pair-wise mutualism in a spatially structured environment. We tested the hypotheses that selection for costly excretions in a focal population i) decreases when an exploiter is added ii) increases when a third mutualist is added relative to the pair-wise scenario. We assayed the selection acting on Salmonella enterica when it exchanges methionine for carbon in an obligate mutualism with an auxotrophic Escherichia coli. A third bacterium, Methylobacterium extorquens, was then added and acted either as an exploiter of the carbon or third obligate mutualist depending on the nitrogen source. In the tri-partite mutualism M. extorquens provided nitrogen to the other species. Contrary to our expectations, adding an exploiter increased selection for methionine excretion in S. enterica. Conversely, selection for cooperation was lower in the tri-partite mutualism relative to the pair-wise system. Genome-scale metabolic models helped identify the mechanisms underlying these changes in selection. Our results highlight the utility of connecting metabolic mechanisms and eco-evolutionary dynamics.

Authors:
 [1];  [2];  [3];  [4]
  1. Harvard Univ., Cambridge, MA (United States); Univ. of Minnesota, Minneapolis, MN (United States)
  2. Harvard Univ., Cambridge, MA (United States); Univ. of Oxford (United Kingdom)
  3. Univ. of Minnesota, Minneapolis, MN (United States)
  4. Harvard Univ., Cambridge, MA (United States); Univ. of Idaho, Moscow, ID (United States)
Publication Date:
Research Org.:
Harvard Univ., Cambridge, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1467618
Alternate Identifier(s):
OSTI ID: 1401860
Grant/Contract Number:  
SC0006731
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Evolution
Additional Journal Information:
Journal Volume: 70; Journal Issue: 8; Journal ID: ISSN 0014-3820
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Harcombe, William R., Betts, Alex, Shapiro, Jason W., and Marx, Christopher J. Adding biotic complexity alters the metabolic benefits of mutualism. United States: N. p., 2016. Web. doi:10.1111/evo.12973.
Harcombe, William R., Betts, Alex, Shapiro, Jason W., & Marx, Christopher J. Adding biotic complexity alters the metabolic benefits of mutualism. United States. https://doi.org/10.1111/evo.12973
Harcombe, William R., Betts, Alex, Shapiro, Jason W., and Marx, Christopher J. Tue . "Adding biotic complexity alters the metabolic benefits of mutualism". United States. https://doi.org/10.1111/evo.12973. https://www.osti.gov/servlets/purl/1467618.
@article{osti_1467618,
title = {Adding biotic complexity alters the metabolic benefits of mutualism},
author = {Harcombe, William R. and Betts, Alex and Shapiro, Jason W. and Marx, Christopher J.},
abstractNote = {Mutualism is ubiquitous in nature and plays an integral role in most communities. To predict the eco-evolutionary dynamics of mutualism it is critical to extend classic pairwise analysis to include additional species. We investigated the effect of adding a third species to a pair-wise mutualism in a spatially structured environment. We tested the hypotheses that selection for costly excretions in a focal population i) decreases when an exploiter is added ii) increases when a third mutualist is added relative to the pair-wise scenario. We assayed the selection acting on Salmonella enterica when it exchanges methionine for carbon in an obligate mutualism with an auxotrophic Escherichia coli. A third bacterium, Methylobacterium extorquens, was then added and acted either as an exploiter of the carbon or third obligate mutualist depending on the nitrogen source. In the tri-partite mutualism M. extorquens provided nitrogen to the other species. Contrary to our expectations, adding an exploiter increased selection for methionine excretion in S. enterica. Conversely, selection for cooperation was lower in the tri-partite mutualism relative to the pair-wise system. Genome-scale metabolic models helped identify the mechanisms underlying these changes in selection. Our results highlight the utility of connecting metabolic mechanisms and eco-evolutionary dynamics.},
doi = {10.1111/evo.12973},
url = {https://www.osti.gov/biblio/1467618}, journal = {Evolution},
issn = {0014-3820},
number = 8,
volume = 70,
place = {United States},
year = {2016},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 10 works
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Figures / Tables:

Figure 1 Figure 1: Interactions in the 2 and 3-species systems. S. enterica is the focal strain and the selection for mutualism in each system is determined by tracking the relative frequency of methionine-excreting cooperators (solid red) to non-excreting genotypes (red outline). All S. enterica genotypes require acetate and ammonia. E. colimore » (blue) consumes lactose, excretes acetate and requires methionine and ammonia. M. extorquens (green) requires acetate. If ammonia is provided in the media then M. extorquens acts as an exploiter with S. enterica for acetate. In contrast, if methylamine is the only nitrogen source then M. extorquens acts as a mutualist providing the other two species with ammonia.« less

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Works referenced in this record:

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journal, February 2007


The Evolution of Reciprocal Altruism
journal, March 1971


Coevolution of symbiotic mutualists and parasites in a community context
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Clarity: An Open-Source Manager for Laboratory Automation
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Species Interactions Alter Evolutionary Responses to a Novel Environment
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Metabolic Resource Allocation in Individual Microbes Determines Ecosystem Interactions and Spatial Dynamics
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Resource competition and social conflict in experimental populations of yeast
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The Ability of Flux Balance Analysis to Predict Evolution of Central Metabolism Scales with the Initial Distance to the Optimum
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Coexistence of mutualists and non-mutualists in a dual-lattice model
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Evolutionary games and spatial chaos
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Strong inter-population cooperation leads to partner intermixing in microbial communities
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Population Dynamics Constrain the Cooperative Evolution of Cross-Feeding
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Eco‐Evolutionary Dynamics of Mutualists and Exploiters
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Social evolution in multispecies biofilms
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Cheating can stabilize cooperation in mutualisms
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Rapid evolution of stability and productivity at the origin of a microbial mutualism
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Metabolic dependencies drive species co-occurrence in diverse microbial communities
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Frequency Dependence and Cooperation: Theory and a Test with Bacteria
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Competition between species can stabilize public‐goods cooperation within a species
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Constraint-based analysis of metabolic capacity of Salmonella typhimurium during host-pathogen interaction
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Multiple mutualist effects: conflict and synergy in multispecies mutualisms
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The evolution of cooperation
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Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection
journal, February 2006


Conditional outcomes in mutualistic interactions
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Development of an Optimized Medium, Strain and High-Throughput Culturing Methods for Methylobacterium extorquens
journal, April 2013


Group Selection and Kin Selection
journal, March 1964


Data from: Adding biotic complexity alters the metabolic benefits of mutualism
dataset, January 2016


Development of a broad-host-range sacB-based vector for unmarked allelic exchange
journal, January 2008


The fundamental role of competition in the ecology and evolution of mutualisms: Competition and mutualism
journal, May 2012


Omic data from evolved E. coli are consistent with computed optimal growth from genome‐scale models
journal, January 2010


Synthetic cooperation in engineered yeast populations
journal, January 2007


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


Species interactions differ in their genetic robustness
journal, April 2015


A theory of group selection.
journal, January 1975


Evolution of mutualism through spatial effects
journal, February 2004


Interacting Guilds: Moving beyond the Pairwise Perspective on Mutualisms
journal, October 2003


Cooperation and competition in pathogenic bacteria
journal, August 2004


A genome-scale, constraint-based approach to systems biology of human metabolism
journal, January 2007


The Evolution of Cooperation
journal, June 2004


What is flux balance analysis?
journal, March 2010


Water Stress Strengthens Mutualism Among Ants, Trees, and Scale Insects
journal, November 2013


Kinship, reciprocity and synergism in the evolution of social behaviour
journal, November 1985


Frequency-Dependent Selection in Bacterial Populations [and Discussion]
journal, July 1988


How context dependent are species interactions?
journal, April 2014


Genetic drift opposes mutualism during spatial population expansion
journal, January 2014


Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria
journal, November 2013


    Works referencing / citing this record:

    Omic data from evolved E. coli are consistent with computed optimal growth from genome‐scale models
    journal, January 2010


    A theory of group selection.
    journal, January 1975


    Strong inter-population cooperation leads to partner intermixing in microbial communities
    journal, January 2013


    Development of a broad-host-range sacB-based vector for unmarked allelic exchange
    journal, January 2008


    Water Stress Strengthens Mutualism Among Ants, Trees, and Scale Insects
    journal, November 2013


    Frequency-Dependent Selection in Bacterial Populations [and Discussion]
    journal, July 1988


    Genetics of Mutualism: The Evolution of Altruism between Species
    journal, October 1994


    Competition between species can stabilize public‐goods cooperation within a species
    journal, January 2012


    Metabolic dependencies drive species co-occurrence in diverse microbial communities
    journal, May 2015


    Social evolution in multispecies biofilms
    journal, June 2011


    Evolution of bidirectional costly mutualism from byproduct consumption
    journal, October 2018


    How context dependent are species interactions?
    journal, April 2014


    Genetic drift opposes mutualism during spatial population expansion
    journal, January 2014


    Data from: Adding biotic complexity alters the metabolic benefits of mutualism
    dataset, January 2016


    The Evolution of Cooperation
    journal, June 2004


    Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria
    journal, November 2013


    Cooperation and competition in pathogenic bacteria
    journal, August 2004


    Kinship, reciprocity and synergism in the evolution of social behaviour
    journal, November 1985


    The Ability of Flux Balance Analysis to Predict Evolution of Central Metabolism Scales with the Initial Distance to the Optimum
    journal, June 2013


    Bioprinting microbial communities to examine interspecies interactions in time and space
    journal, August 2018


    What is flux balance analysis?
    journal, March 2010


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


    Simpson's Paradox in a Synthetic Microbial System
    journal, January 2009


    Multiple mutualist effects: conflict and synergy in multispecies mutualisms
    journal, April 2014


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


    The fundamental role of competition in the ecology and evolution of mutualisms: Competition and mutualism
    journal, May 2012


    Data from: Adding biotic complexity alters the metabolic benefits of mutualism
    dataset, January 2016


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


    Group Selection and Kin Selection
    journal, March 1964


    Environments that Induce Synthetic Microbial Ecosystems
    journal, November 2010


    Evolution of mutualism through spatial effects
    journal, February 2004


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


    Evolutionary games and spatial chaos
    journal, October 1992


    Species interactions differ in their genetic robustness
    journal, April 2015


    Rapid evolution of stability and productivity at the origin of a microbial mutualism
    journal, January 2010


    The Evolution of Reciprocal Altruism
    journal, March 1971


    Interacting Guilds: Moving beyond the Pairwise Perspective on Mutualisms
    journal, October 2003


    The Power of Metabolism for Predicting Microbial Community Dynamics
    journal, June 2019


    A genome-scale, constraint-based approach to systems biology of human metabolism
    journal, January 2007


    Conditional outcomes in mutualistic interactions
    journal, June 1994


    Synthetic cooperation in engineered yeast populations
    journal, January 2007


    Metabolic Flux Analysis in Plants: From Intelligent Design to Rational Engineering
    journal, June 2008


    Frequency Dependence and Cooperation: Theory and a Test with Bacteria
    journal, September 2007


    Cooperation and coexpression: How coexpression networks shift in response to multiple mutualists
    journal, April 2018


    Cheating can stabilize cooperation in mutualisms
    journal, May 2006


    Species Interactions Alter Evolutionary Responses to a Novel Environment
    journal, May 2012


    Coevolution of symbiotic mutualists and parasites in a community context
    journal, March 2007


    The evolution of interspecific mutualisms
    journal, July 1998


    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


    The evolution of cooperation
    journal, March 1981


    Coexistence of mutualists and non-mutualists in a dual-lattice model
    journal, September 2013


    Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization
    journal, February 2007


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


    Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection
    journal, February 2006


      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.