Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural Transformation

Horizontal gene transfer (HGT) can have profound effects on bacterial evolution by allowing individuals to rapidly acquire adaptive traits that shape their strategies for competition. One strategy for intermicrobial antagonism often used by Proteobacteria is the genetically encoded contact-dependent...

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Main Authors: Jacob Thomas, Samit S. Watve, William C. Ratcliff, Brian K. Hammer, Bonnie Bassler
Format: Article
Language:English
Published: American Society for Microbiology 2017-07-01
Series:mBio
Online Access:http://mbio.asm.org/cgi/content/full/8/4/e00654-17
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spelling doaj-d85554e60764476faede017a6ad37b442021-07-02T08:29:30ZengAmerican Society for MicrobiologymBio2150-75112017-07-0184e00654-1710.1128/mBio.00654-17Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural TransformationJacob ThomasSamit S. WatveWilliam C. RatcliffBrian K. HammerBonnie BasslerHorizontal gene transfer (HGT) can have profound effects on bacterial evolution by allowing individuals to rapidly acquire adaptive traits that shape their strategies for competition. One strategy for intermicrobial antagonism often used by Proteobacteria is the genetically encoded contact-dependent type VI secretion system (T6SS), a weapon used to kill heteroclonal neighbors by direct injection of toxic effectors. Here, we experimentally demonstrate that Vibrio cholerae can acquire new T6SS effector genes via horizontal transfer and utilize them to kill neighboring cells. Replacement of one or more parental alleles with novel effectors allows the recombinant strain to dramatically outcompete its parent. Using spatially explicit modeling, we examine how this process could affect the ecology and evolution of surface-attached microbial populations. HGT of T6SS effector-immunity pairs is risky: transformation brings a cell into conflict with its former clone mates but can be adaptive when superior T6SS alleles are acquired. More generally, we find that these costs and benefits are not symmetric and that high rates of HGT can act as a hedge against competitors with unpredictable T6SS efficacy. We conclude that antagonism and horizontal transfer drive successive rounds of weapon optimization and selective sweeps, dynamically shaping the composition of microbial communities.http://mbio.asm.org/cgi/content/full/8/4/e00654-17
collection DOAJ
language English
format Article
sources DOAJ
author Jacob Thomas
Samit S. Watve
William C. Ratcliff
Brian K. Hammer
Bonnie Bassler
spellingShingle Jacob Thomas
Samit S. Watve
William C. Ratcliff
Brian K. Hammer
Bonnie Bassler
Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural Transformation
mBio
author_facet Jacob Thomas
Samit S. Watve
William C. Ratcliff
Brian K. Hammer
Bonnie Bassler
author_sort Jacob Thomas
title Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural Transformation
title_short Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural Transformation
title_full Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural Transformation
title_fullStr Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural Transformation
title_full_unstemmed Horizontal Gene Transfer of Functional Type VI Killing Genes by Natural Transformation
title_sort horizontal gene transfer of functional type vi killing genes by natural transformation
publisher American Society for Microbiology
series mBio
issn 2150-7511
publishDate 2017-07-01
description Horizontal gene transfer (HGT) can have profound effects on bacterial evolution by allowing individuals to rapidly acquire adaptive traits that shape their strategies for competition. One strategy for intermicrobial antagonism often used by Proteobacteria is the genetically encoded contact-dependent type VI secretion system (T6SS), a weapon used to kill heteroclonal neighbors by direct injection of toxic effectors. Here, we experimentally demonstrate that Vibrio cholerae can acquire new T6SS effector genes via horizontal transfer and utilize them to kill neighboring cells. Replacement of one or more parental alleles with novel effectors allows the recombinant strain to dramatically outcompete its parent. Using spatially explicit modeling, we examine how this process could affect the ecology and evolution of surface-attached microbial populations. HGT of T6SS effector-immunity pairs is risky: transformation brings a cell into conflict with its former clone mates but can be adaptive when superior T6SS alleles are acquired. More generally, we find that these costs and benefits are not symmetric and that high rates of HGT can act as a hedge against competitors with unpredictable T6SS efficacy. We conclude that antagonism and horizontal transfer drive successive rounds of weapon optimization and selective sweeps, dynamically shaping the composition of microbial communities.
url http://mbio.asm.org/cgi/content/full/8/4/e00654-17
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