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

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 repea...

Full description

Saved in:
Bibliographic Details
Main Authors: Sarah M Douglas, Lon M Chubiz, William R Harcombe, F Marty Ytreberg, Christopher J Marx
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0161837&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850232547922935808
author Sarah M Douglas
Lon M Chubiz
William R Harcombe
F Marty Ytreberg
Christopher J Marx
author_facet Sarah M Douglas
Lon M Chubiz
William R Harcombe
F Marty Ytreberg
Christopher J Marx
author_sort Sarah M Douglas
collection DOAJ
description 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 determine community 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-synonymous mutations 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 terms of 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.
format Article
id doaj-art-ffc628268d0e40189a22efd83b2c8527
institution OA Journals
issn 1932-6203
language English
publishDate 2016-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-ffc628268d0e40189a22efd83b2c85272025-08-20T02:03:08ZengPublic Library of Science (PLoS)PLoS ONE1932-62032016-01-01119e016183710.1371/journal.pone.0161837Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium.Sarah M DouglasLon M ChubizWilliam R HarcombeF Marty YtrebergChristopher J MarxMulti-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 determine community 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-synonymous mutations 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 terms of 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.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0161837&type=printable
spellingShingle Sarah M Douglas
Lon M Chubiz
William R Harcombe
F Marty Ytreberg
Christopher J Marx
Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium.
PLoS ONE
title Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium.
title_full Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium.
title_fullStr Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium.
title_full_unstemmed Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium.
title_short Parallel Mutations Result in a Wide Range of Cooperation and Community Consequences in a Two-Species Bacterial Consortium.
title_sort parallel mutations result in a wide range of cooperation and community consequences in a two species bacterial consortium
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0161837&type=printable
work_keys_str_mv AT sarahmdouglas parallelmutationsresultinawiderangeofcooperationandcommunityconsequencesinatwospeciesbacterialconsortium
AT lonmchubiz parallelmutationsresultinawiderangeofcooperationandcommunityconsequencesinatwospeciesbacterialconsortium
AT williamrharcombe parallelmutationsresultinawiderangeofcooperationandcommunityconsequencesinatwospeciesbacterialconsortium
AT fmartyytreberg parallelmutationsresultinawiderangeofcooperationandcommunityconsequencesinatwospeciesbacterialconsortium
AT christopherjmarx parallelmutationsresultinawiderangeofcooperationandcommunityconsequencesinatwospeciesbacterialconsortium