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Title: Species interactions differ in their genetic robustness

Abstract

Conflict and cooperation between bacterial species drive the composition and function of microbial communities. Stability of these emergent properties will be influenced by the degree to which species' interactions are robust to genetic perturbations. We use genome-scale metabolic modeling to computationally analyze the impact of genetic changes when Escherichia coli and Salmonella enterica compete, or cooperate. We systematically knocked out in silico each reaction in the metabolic network of E. coli to construct all 2583 mutant stoichiometric models. Then, using a recently developed multi-scale computational framework, we simulated the growth of each mutant E. coli in the presence of S. enterica. The type of interaction between species was set by modulating the initial metabolites present in the environment. We found that the community was most robust to genetic perturbations when the organisms were cooperating. Species ratios were more stable in the cooperative community, and community biomass had equal variance in the two contexts. Additionally, the number of mutations that have a substantial effect is lower when the species cooperate than when they are competing. In contrast, when mutations were added to the S. enterica network the system was more robust when the bacteria were competing. These results highlight the utilitymore » of connecting metabolic mechanisms and studies of ecological stability. Cooperation and conflict alter the connection between genetic changes and properties that emerge at higher levels of biological organization.« less

Authors:
 [1];  [2];  [2];  [3]
  1. Univ. of Missouri - St. Louis, MO (United States). Dept. of Biology
  2. Boston Univ., MA (United States). Bioinformatics Program
  3. Univ. of Minnesota, St. Paul, MN (United States). Dept. of Ecology, Evolution, and Behavior and BioTechnology Inst.
Publication Date:
Research Org.:
Boston Univ., MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Institutes of Health (NIH)
OSTI Identifier:
1185123
Grant/Contract Number:  
SC0004962
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal Issue: C; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cooperation; competition; genetic robustness; E. coli; Salmonella; community stability; metabolic modeling

Citation Formats

Chubiz, Lon M., Granger, Brian R., Segre, Daniel, and Harcombe, William R. Species interactions differ in their genetic robustness. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.00271.
Chubiz, Lon M., Granger, Brian R., Segre, Daniel, & Harcombe, William R. Species interactions differ in their genetic robustness. United States. https://doi.org/10.3389/fmicb.2015.00271
Chubiz, Lon M., Granger, Brian R., Segre, Daniel, and Harcombe, William R. Tue . "Species interactions differ in their genetic robustness". United States. https://doi.org/10.3389/fmicb.2015.00271. https://www.osti.gov/servlets/purl/1185123.
@article{osti_1185123,
title = {Species interactions differ in their genetic robustness},
author = {Chubiz, Lon M. and Granger, Brian R. and Segre, Daniel and Harcombe, William R.},
abstractNote = {Conflict and cooperation between bacterial species drive the composition and function of microbial communities. Stability of these emergent properties will be influenced by the degree to which species' interactions are robust to genetic perturbations. We use genome-scale metabolic modeling to computationally analyze the impact of genetic changes when Escherichia coli and Salmonella enterica compete, or cooperate. We systematically knocked out in silico each reaction in the metabolic network of E. coli to construct all 2583 mutant stoichiometric models. Then, using a recently developed multi-scale computational framework, we simulated the growth of each mutant E. coli in the presence of S. enterica. The type of interaction between species was set by modulating the initial metabolites present in the environment. We found that the community was most robust to genetic perturbations when the organisms were cooperating. Species ratios were more stable in the cooperative community, and community biomass had equal variance in the two contexts. Additionally, the number of mutations that have a substantial effect is lower when the species cooperate than when they are competing. In contrast, when mutations were added to the S. enterica network the system was more robust when the bacteria were competing. These results highlight the utility of connecting metabolic mechanisms and studies of ecological stability. Cooperation and conflict alter the connection between genetic changes and properties that emerge at higher levels of biological organization.},
doi = {10.3389/fmicb.2015.00271},
journal = {Frontiers in Microbiology},
number = C,
volume = 6,
place = {United States},
year = {Tue Apr 14 00:00:00 EDT 2015},
month = {Tue Apr 14 00:00:00 EDT 2015}
}

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Works referenced in this record:

Stability criteria for complex ecosystems
journal, February 2012


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

  • Baba, Tomoya; Ara, Takeshi; Hasegawa, Miki
  • Molecular Systems Biology, Vol. 2, Article No. 2006.0008
  • DOI: 10.1038/msb4100050

O2 as the regulatory signal for FNR-dependent gene regulation in Escherichia coli.
journal, August 1996


Anaerobic activation of arcA transcription in Escherichia coli: roles of Fnr and ArcA
journal, March 1994


Meta-analysis methods for genome-wide association studies and beyond
journal, May 2013

  • Evangelou, Evangelos; Ioannidis, John P. A.
  • Nature Reviews Genetics, Vol. 14, Issue 6
  • DOI: 10.1038/nrg3472

The Causes and Consequences of Compensatory Dynamics in Ecological Communities
journal, December 2009


Novel Cooperation Experimentally Evolved Between Species
journal, February 2010


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


The Genotype–Phenotype Map of Yeast Complex Traits: Basic Parameters and the Role of Natural Selection
journal, April 2014

  • Ho, Wei-Chin; Zhang, Jianzhi
  • Molecular Biology and Evolution, Vol. 31, Issue 6
  • DOI: 10.1093/molbev/msu131

Defined spatial structure stabilizes a synthetic multispecies bacterial community
journal, November 2008

  • Kim, H. J.; Boedicker, J. Q.; Choi, J. W.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 47
  • DOI: 10.1073/pnas.0807935105

Environments that Induce Synthetic Microbial Ecosystems
journal, November 2010


Ecosystems biology of microbial metabolism
journal, August 2011


Biodiversity and ecosystem stability: a synthesis of underlying mechanisms
journal, January 2013

  • Loreau, Michel; de Mazancourt, Claire
  • Ecology Letters, Vol. 16
  • DOI: 10.1111/ele.12073

Will a Large Complex System be Stable?
journal, August 1972


The Genotypic View of Social Interactions in Microbial Communities
journal, November 2013


Diversity of Interaction Types and Ecological Community Stability
journal, July 2012


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

What is flux balance analysis?
journal, March 2010

  • Orth, Jeffrey D.; Thiele, Ines; Palsson, Bernhard Ø
  • Nature Biotechnology, Vol. 28, Issue 3
  • DOI: 10.1038/nbt.1614

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

Analysis of optimality in natural and perturbed metabolic networks
journal, November 2002

  • Segre, D.; Vitkup, D.; Church, G. M.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 23
  • DOI: 10.1073/pnas.232349399

Synthetic cooperation in engineered yeast populations
journal, January 2007

  • Shou, W.; Ram, S.; Vilar, J. M. G.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 6
  • DOI: 10.1073/pnas.0610575104

Variation and selection of polygenic characters
journal, January 1941


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


Ecosystems biology of microbial metabolism
journal, August 2011


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

Stability criteria for complex ecosystems
journal, February 2012


Meta-analysis methods for genome-wide association studies and beyond
journal, May 2013

  • Evangelou, Evangelos; Ioannidis, John P. A.
  • Nature Reviews Genetics, Vol. 14, Issue 6
  • DOI: 10.1038/nrg3472

Development of CRISPR-Cas13a-based antimicrobials capable of sequence-specific killing of target bacteria
journal, June 2020


Synthetic cooperation in engineered yeast populations
journal, January 2007

  • Shou, W.; Ram, S.; Vilar, J. M. G.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 6
  • DOI: 10.1073/pnas.0610575104

Defined spatial structure stabilizes a synthetic multispecies bacterial community
journal, November 2008

  • Kim, H. J.; Boedicker, J. Q.; Choi, J. W.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 47
  • DOI: 10.1073/pnas.0807935105

Analysis of optimality in natural and perturbed metabolic networks
journal, November 2002

  • Segre, D.; Vitkup, D.; Church, G. M.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 23
  • DOI: 10.1073/pnas.232349399

The Genotype–Phenotype Map of Yeast Complex Traits: Basic Parameters and the Role of Natural Selection
journal, April 2014

  • Ho, Wei-Chin; Zhang, Jianzhi
  • Molecular Biology and Evolution, Vol. 31, Issue 6
  • DOI: 10.1093/molbev/msu131

Biodiversity and ecosystem stability: a synthesis of underlying mechanisms
journal, January 2013

  • Loreau, Michel; de Mazancourt, Claire
  • Ecology Letters, Vol. 16
  • DOI: 10.1111/ele.12073

Anaerobic activation of arcA transcription in Escherichia coli: roles of Fnr and ArcA
journal, March 1994


Novel Cooperation Experimentally Evolved Between Species
journal, February 2010


Diversity of Interaction Types and Ecological Community Stability
journal, July 2012


Experimental and Computational Assessment of Conditionally Essential Genes in Escherichia coli
journal, September 2006

  • Joyce, A. R.; Reed, J. L.; White, A.
  • Journal of Bacteriology, Vol. 188, Issue 23
  • DOI: 10.1128/jb.00740-06

The Genotypic View of Social Interactions in Microbial Communities
journal, November 2013


Environments that Induce Synthetic Microbial Ecosystems
journal, November 2010


Works referencing / citing this record:

Selection of Potential Probiotic Lactobacillus with Inhibitory Activity Against Salmonella and Fecal Coliform Bacteria
journal, July 2017

  • Abhisingha, Mattika; Dumnil, Jureeporn; Pitaksutheepong, Chetsadaporn
  • Probiotics and Antimicrobial Proteins, Vol. 10, Issue 2
  • DOI: 10.1007/s12602-017-9304-8

Cross-feeding modulates antibiotic tolerance in bacterial communities
journal, July 2018

  • Adamowicz, Elizabeth M.; Flynn, Jeffrey; Hunter, Ryan C.
  • The ISME Journal, Vol. 12, Issue 11
  • DOI: 10.1038/s41396-018-0212-z

Lytic bacteriophage have diverse indirect effects in a synthetic cross-feeding community
journal, October 2019


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

  • Harcombe, William R.; Chacón, Jeremy M.; Adamowicz, Elizabeth M.
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 47
  • DOI: 10.1073/pnas.1810949115

Synthetic microbial ecology and the dynamic interplay between microbial genotypes
journal, August 2016

  • Dolinšek, Jan; Goldschmidt, Felix; Johnson, David R.
  • FEMS Microbiology Reviews, Vol. 40, Issue 6
  • DOI: 10.1093/femsre/fuw024

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


Spatiotemporal modeling of microbial metabolism
journal, March 2016


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


Evolution of bacterial trade in a two-species community
journal, November 2018

  • Farrell, Jennifer M.; Brown, Sam P.
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 47
  • DOI: 10.1073/pnas.1817344115

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


More than just a gut feeling: constraint-based genome-scale metabolic models for predicting functions of human intestinal microbes
journal, July 2017

  • van der Ark, Kees C. H.; van Heck, Ruben G. A.; Martins Dos Santos, Vitor A. P.
  • Microbiome, Vol. 5, Issue 1
  • DOI: 10.1186/s40168-017-0299-x

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