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...
Main Authors: | , , , , |
---|---|
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 |
id |
doaj-d85554e60764476faede017a6ad37b44 |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT jacobthomas horizontalgenetransferoffunctionaltypevikillinggenesbynaturaltransformation AT samitswatve horizontalgenetransferoffunctionaltypevikillinggenesbynaturaltransformation AT williamcratcliff horizontalgenetransferoffunctionaltypevikillinggenesbynaturaltransformation AT briankhammer horizontalgenetransferoffunctionaltypevikillinggenesbynaturaltransformation AT bonniebassler horizontalgenetransferoffunctionaltypevikillinggenesbynaturaltransformation |
_version_ |
1721334672720396288 |