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

Title: Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium

Abstract

Multi-species microbial communities play a critical role in human health, industry, and waste remediation. Recently, the evolution of synthetic consortia in the laboratory has enabled adaptation to be addressed in the context of interacting species. Using an engineered bacterial consortium,we repeatedly evolved cooperative genotypes and examined both the predictability of evolution and the phenotypes that determinecommunity dynamics. Eight Salmonella enterica serovar Typhimurium strains evolved methionine excretion sufficient to support growth of an Escherichia coli methionine auxotroph, from whom they required excreted growth substrates. Non-synonymousmutations in metA, encoding homoserine trans-succinylase (HTS), were detected in each evolved S. enterica methionine cooperator and were shown to be necessary for cooperative consortia growth. Molecular modeling was used to predict that most of the non-synonymous mutations slightly increase the binding affinity for HTS homodimer formation. Despite this genetic parallelism and trend of increasing protein binding stability, these metA alleles gave rise to a wide range of phenotypic diversity in termsof individual versus group benefit. The cooperators with the highest methionine excretion permitted nearly two-fold faster consortia growth and supported the highest fraction of E. coli, yet also had the slowest individual growth rates compared to less cooperative strains. Thus, although the genetic basis of adaptationmore » was quite similar across independent origins of cooperative phenotypes, quantitative measurements of metabolite production were required to predict either the individual-level growth consequences or how these propagate to community-level behavior.« less

Authors:
; ; ; ; ;
Publication Date:
Research Org.:
Harvard Univ., Cambridge, MA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1337793
Alternate Identifier(s):
OSTI ID: 1436492
Grant/Contract Number:  
SC0006731
Resource Type:
Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Name: PLoS ONE Journal Volume: 11 Journal Issue: 9; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science (PLoS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Douglas, Sarah M., Chubiz, Lon M., Harcombe, William R., Ytreberg, F. Marty, Marx, Christopher J., and Brown, ed., Sam Paul. Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0161837.
Douglas, Sarah M., Chubiz, Lon M., Harcombe, William R., Ytreberg, F. Marty, Marx, Christopher J., & Brown, ed., Sam Paul. Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium. United States. doi:10.1371/journal.pone.0161837.
Douglas, Sarah M., Chubiz, Lon M., Harcombe, William R., Ytreberg, F. Marty, Marx, Christopher J., and Brown, ed., Sam Paul. Mon . "Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium". United States. doi:10.1371/journal.pone.0161837.
@article{osti_1337793,
title = {Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium},
author = {Douglas, Sarah M. and Chubiz, Lon M. and Harcombe, William R. and Ytreberg, F. Marty and Marx, Christopher J. and Brown, ed., Sam Paul},
abstractNote = {Multi-species microbial communities play a critical role in human health, industry, and waste remediation. Recently, the evolution of synthetic consortia in the laboratory has enabled adaptation to be addressed in the context of interacting species. Using an engineered bacterial consortium,we repeatedly evolved cooperative genotypes and examined both the predictability of evolution and the phenotypes that determinecommunity dynamics. Eight Salmonella enterica serovar Typhimurium strains evolved methionine excretion sufficient to support growth of an Escherichia coli methionine auxotroph, from whom they required excreted growth substrates. Non-synonymousmutations in metA, encoding homoserine trans-succinylase (HTS), were detected in each evolved S. enterica methionine cooperator and were shown to be necessary for cooperative consortia growth. Molecular modeling was used to predict that most of the non-synonymous mutations slightly increase the binding affinity for HTS homodimer formation. Despite this genetic parallelism and trend of increasing protein binding stability, these metA alleles gave rise to a wide range of phenotypic diversity in termsof individual versus group benefit. The cooperators with the highest methionine excretion permitted nearly two-fold faster consortia growth and supported the highest fraction of E. coli, yet also had the slowest individual growth rates compared to less cooperative strains. Thus, although the genetic basis of adaptation was quite similar across independent origins of cooperative phenotypes, quantitative measurements of metabolite production were required to predict either the individual-level growth consequences or how these propagate to community-level behavior.},
doi = {10.1371/journal.pone.0161837},
journal = {PLoS ONE},
number = 9,
volume = 11,
place = {United States},
year = {2016},
month = {9}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1371/journal.pone.0161837

Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Fitness Effects of Fixed Beneficial Mutations in Microbial Populations
journal, June 2002


Regulation of the Methionine Feedback-Sensitive Enzyme in Mutants of Salmonella typhimurium
journal, January 1972


Parallel Evolutionary Dynamics of Adaptive Diversification in Escherichia coli
journal, February 2013


Short-Term Signatures of Evolutionary Change in the Salmonella enterica Serovar Typhimurium 14028 Genome
journal, November 2009

  • Jarvik, T.; Smillie, C.; Groisman, E. A.
  • Journal of Bacteriology, Vol. 192, Issue 2
  • DOI: 10.1128/JB.01233-09

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

Adaptive radiation in a heterogeneous environment
journal, July 1998

  • Rainey, Paul B.; Travisano, Michael
  • Nature, Vol. 394, Issue 6688
  • DOI: 10.1038/27900

Species interactions differ in their genetic robustness
journal, April 2015


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


Social evolution theory for microorganisms
journal, August 2006

  • West, Stuart A.; Griffin, Ashleigh S.; Gardner, Andy
  • Nature Reviews Microbiology, Vol. 4, Issue 8
  • DOI: 10.1038/nrmicro1461

Microbe–microbe interactions in mixed culture food fermentations
journal, April 2013


The SWISS-MODEL Repository and associated resources
journal, January 2009

  • Kiefer, F.; Arnold, K.; Kunzli, M.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn750

Integrated Perspective for Effective Bioremediation
journal, December 2011

  • Paliwal, Vasundhara; Puranik, Sampada; Purohit, Hemant J.
  • Applied Biochemistry and Biotechnology, Vol. 166, Issue 4
  • DOI: 10.1007/s12010-011-9479-5

Importance of positioning for microbial evolution
journal, April 2014

  • Kim, W.; Racimo, F.; Schluter, J.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 16
  • DOI: 10.1073/pnas.1323632111

The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling
journal, November 2005


Predicting Changes in the Stability of Proteins and Protein Complexes: A Study of More Than 1000 Mutations
journal, July 2002


Vaginal Microbiome: Rethinking Health and Disease
journal, October 2012


The Distribution of Fitness Effects of Beneficial Mutations in Pseudomonas aeruginosa
journal, March 2009


Control of methionine biosynthesis in Escherichia coli by proteolysis
journal, September 2000


The Molecular Diversity of Adaptive Convergence
journal, January 2012

  • Tenaillon, O.; Rodriguez-Verdugo, A.; Gaut, R. L.
  • Science, Vol. 335, Issue 6067, p. 457-461
  • DOI: 10.1126/science.1212986

Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli
journal, January 2003

  • Cooper, T. F.; Rozen, D. E.; Lenski, R. E.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 3
  • DOI: 10.1073/pnas.0334340100

Genome evolution and adaptation in a long-term experiment with Escherichia coli
journal, October 2009

  • Barrick, Jeffrey E.; Yu, Dong Su; Yoon, Sung Ho
  • Nature, Vol. 461, Issue 7268
  • DOI: 10.1038/nature08480

Effects of Deregulation of Methionine Biosynthesis on Methionine Excretion in Escherichia coli
journal, June 2005


Second-Order Selection for Evolvability in a Large Escherichia coli Population
journal, March 2011


Prediction of water and metal binding sites and their affinities by using the Fold-X force field
journal, July 2005

  • Schymkowitz, J. W. H.; Rousseau, F.; Martins, I. C.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 29
  • DOI: 10.1073/pnas.0501980102

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


Ex Uno Plures: Clonal Reinforcement Drives Evolution of a Simple Microbial Community
journal, June 2014


Eco-evolutionary feedbacks drive species interactions
journal, December 2013

  • Andrade-Domínguez, Andrés; Salazar, Emmanuel; del Carmen Vargas-Lagunas, María
  • The ISME Journal, Vol. 8, Issue 5
  • DOI: 10.1038/ismej.2013.208

Regulation of methionine biosynthesis in the enterobacteriaceae
journal, January 1991

  • Old, Iain G.; Phillips, Simon E. V.; Stockley, Peter G.
  • Progress in Biophysics and Molecular Biology, Vol. 56, Issue 3
  • DOI: 10.1016/0079-6107(91)90012-H

Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes
journal, November 2011

  • Lieberman, Tami D.; Michel, Jean-Baptiste; Aingaran, Mythili
  • Nature Genetics, Vol. 43, Issue 12
  • DOI: 10.1038/ng.997

Red Queen: from populations to taxa and communities
journal, July 2011

  • Liow, Lee Hsiang; Van Valen, Leigh; Stenseth, Nils Chr.
  • Trends in Ecology & Evolution, Vol. 26, Issue 7
  • DOI: 10.1016/j.tree.2011.03.016

Can You Sequence Ecology? Metagenomics of Adaptive Diversification
journal, February 2013


S-adenosylmethionine synthetase in methionine regulatory mutants of Salmonella typhimurium
journal, January 1973

  • Hobson, Ann C.; Smith, D. A.
  • MGG Molecular & General Genetics, Vol. 126, Issue 1
  • DOI: 10.1007/BF00333477

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

Impact of the K24N mutation on the transactivation domain of p53 and its binding to murine double-minute clone 2: Effects of a Mutation on p53-MDM2 Binding
journal, July 2013

  • Zhan, Yingqian Ada; Wu, Hongwei; Powell, Anne T.
  • Proteins: Structure, Function, and Bioinformatics, Vol. 81, Issue 10
  • DOI: 10.1002/prot.24310

Tests of parallel molecular evolution in a long-term experiment with Escherichia coli
journal, June 2006

  • Woods, R.; Schneider, D.; Winkworth, C. L.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 24
  • DOI: 10.1073/pnas.0602917103

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

  • Momeni, Babak; Brileya, Kristen A.; Fields, Matthew W.
  • eLife, Vol. 2
  • DOI: 10.7554/eLife.00230

Construction of targeted single copy lac fusions using λ Red and FLP-mediated site-specific recombination in bacteria
journal, May 2002


Improved Thermostability and Acetic Acid Tolerance of Escherichia coli via Directed Evolution of Homoserine o-Succinyltransferase
journal, October 2008

  • Mordukhova, E. A.; Lee, H. -S.; Pan, J. -G.
  • Applied and Environmental Microbiology, Vol. 74, Issue 24
  • DOI: 10.1128/AEM.00654-08

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

  • Hillesland, K. L.; Stahl, D. A.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 5
  • DOI: 10.1073/pnas.0908456107

Optimization of Gene Expression through Divergent Mutational Paths
journal, February 2012


13C-based metabolic flux analysis
journal, May 2009

  • Zamboni, Nicola; Fendt, Sarah-Maria; Rühl, Martin
  • Nature Protocols, Vol. 4, Issue 6
  • DOI: 10.1038/nprot.2009.58

Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in Escherichia coli
journal, March 2014


Computational estimation of rainbow trout estrogen receptor binding affinities for environmental estrogens
journal, February 2011

  • Shyu, Conrad; Cavileer, Timothy D.; Nagler, James J.
  • Toxicology and Applied Pharmacology, Vol. 250, Issue 3
  • DOI: 10.1016/j.taap.2010.11.005