Transposon insertion sequencing reveals novel hypermutator genes in Acinetobacter baumannii

ABSTRACT Mutation rates in bacteria are an important determinant of adaptation to new environments and success in different niches. In some bacterial pathogens, “hypermutator” variants—most often associated with mutations in components of the DNA mismatch repair system—are associated with increased...

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Main Authors: Francesca L. Short, Ram Maharjan, Liping Li, Nusrat Afrin, Natasha Delgado, Christine J. Boinett, Julian Parkhill, Amy K. Cain, Ian T. Paulsen
Format: Article
Language:English
Published: American Society for Microbiology 2025-08-01
Series:mBio
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Online Access:https://journals.asm.org/doi/10.1128/mbio.00966-25
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author Francesca L. Short
Ram Maharjan
Liping Li
Nusrat Afrin
Natasha Delgado
Christine J. Boinett
Julian Parkhill
Amy K. Cain
Ian T. Paulsen
author_facet Francesca L. Short
Ram Maharjan
Liping Li
Nusrat Afrin
Natasha Delgado
Christine J. Boinett
Julian Parkhill
Amy K. Cain
Ian T. Paulsen
author_sort Francesca L. Short
collection DOAJ
description ABSTRACT Mutation rates in bacteria are an important determinant of adaptation to new environments and success in different niches. In some bacterial pathogens, “hypermutator” variants—most often associated with mutations in components of the DNA mismatch repair system—are associated with increased antibiotic resistance and poorer patient outcomes. We report the serendipitous finding of novel hypermutator genes in Acinetobacter baumannii through genome-scale mutant fitness screening. Exposure of a transposon insertion mutant library of A. baumannii to extended weak antibiotic selection resulted in selection for mutations that directly increased fitness as expected, but also revealed genes where transposon insertion indirectly increased fitness due to elevated general mutation rates. Three novel hypermutator genes were confirmed in A. baumannii: nusB, encoding a transcription antiterminator; ABUW_0208, encoding a hypothetical protein; and ABUW_2121, which encodes a sulfite transporter. We find selection for hypermutator variants in transposon insertion sequencing (TIS) data sets from diverse bacteria under various antibiotic treatments. Our results expand the range of biological functions linked to hypermutator phenotypes in bacteria and provide a workflow for the identification of putative hypermutators by TIS.IMPORTANCEAll organisms have the capacity for evolution through mutation. Bacteria with high mutation rates have a survival advantage in some stressful environments because they generate beneficial mutations more frequently. “Hypermutators” are bacterial strains that carry gene inactivations that increase general mutation rates. These variants are important in chronic infections, as their increased genetic diversity allows higher drug resistance and prolonged survival in the host. Only a few different hypermutator genes are known, and there is no high-throughput method for their identification. We have made the serendipitous finding that hypermutator genes can be identified by genome-wide mutant fitness screening under specific selection conditions. We have identified novel hypermutator alleles in the notorious hospital pathogen Acinetobacter baumannii and show that hypermutator variants can be detected in screens of a wide range of pathogens.
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spelling doaj-art-53f7a253759949d2b2cf19c5ccdae5302025-08-20T04:00:49ZengAmerican Society for MicrobiologymBio2150-75112025-08-0116810.1128/mbio.00966-25Transposon insertion sequencing reveals novel hypermutator genes in Acinetobacter baumanniiFrancesca L. Short0Ram Maharjan1Liping Li2Nusrat Afrin3Natasha Delgado4Christine J. Boinett5Julian Parkhill6Amy K. Cain7Ian T. Paulsen8Department of Microbiology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria, AustraliaARC Centre of Excellence in Synthetic Biology, School of Natural Sciences, Macquarie University, Sydney, New South Wales, AustraliaARC Centre of Excellence in Synthetic Biology, School of Natural Sciences, Macquarie University, Sydney, New South Wales, AustraliaARC Centre of Excellence in Synthetic Biology, School of Natural Sciences, Macquarie University, Sydney, New South Wales, AustraliaARC Centre of Excellence in Synthetic Biology, School of Natural Sciences, Macquarie University, Sydney, New South Wales, AustraliaWellcome Sanger Institute, Hinxton, United KingdomWellcome Sanger Institute, Hinxton, United KingdomARC Centre of Excellence in Synthetic Biology, School of Natural Sciences, Macquarie University, Sydney, New South Wales, AustraliaARC Centre of Excellence in Synthetic Biology, School of Natural Sciences, Macquarie University, Sydney, New South Wales, AustraliaABSTRACT Mutation rates in bacteria are an important determinant of adaptation to new environments and success in different niches. In some bacterial pathogens, “hypermutator” variants—most often associated with mutations in components of the DNA mismatch repair system—are associated with increased antibiotic resistance and poorer patient outcomes. We report the serendipitous finding of novel hypermutator genes in Acinetobacter baumannii through genome-scale mutant fitness screening. Exposure of a transposon insertion mutant library of A. baumannii to extended weak antibiotic selection resulted in selection for mutations that directly increased fitness as expected, but also revealed genes where transposon insertion indirectly increased fitness due to elevated general mutation rates. Three novel hypermutator genes were confirmed in A. baumannii: nusB, encoding a transcription antiterminator; ABUW_0208, encoding a hypothetical protein; and ABUW_2121, which encodes a sulfite transporter. We find selection for hypermutator variants in transposon insertion sequencing (TIS) data sets from diverse bacteria under various antibiotic treatments. Our results expand the range of biological functions linked to hypermutator phenotypes in bacteria and provide a workflow for the identification of putative hypermutators by TIS.IMPORTANCEAll organisms have the capacity for evolution through mutation. Bacteria with high mutation rates have a survival advantage in some stressful environments because they generate beneficial mutations more frequently. “Hypermutators” are bacterial strains that carry gene inactivations that increase general mutation rates. These variants are important in chronic infections, as their increased genetic diversity allows higher drug resistance and prolonged survival in the host. Only a few different hypermutator genes are known, and there is no high-throughput method for their identification. We have made the serendipitous finding that hypermutator genes can be identified by genome-wide mutant fitness screening under specific selection conditions. We have identified novel hypermutator alleles in the notorious hospital pathogen Acinetobacter baumannii and show that hypermutator variants can be detected in screens of a wide range of pathogens.https://journals.asm.org/doi/10.1128/mbio.00966-25hypermutatortn-seqtradismutation rateAcinetobacter
spellingShingle Francesca L. Short
Ram Maharjan
Liping Li
Nusrat Afrin
Natasha Delgado
Christine J. Boinett
Julian Parkhill
Amy K. Cain
Ian T. Paulsen
Transposon insertion sequencing reveals novel hypermutator genes in Acinetobacter baumannii
mBio
hypermutator
tn-seq
tradis
mutation rate
Acinetobacter
title Transposon insertion sequencing reveals novel hypermutator genes in Acinetobacter baumannii
title_full Transposon insertion sequencing reveals novel hypermutator genes in Acinetobacter baumannii
title_fullStr Transposon insertion sequencing reveals novel hypermutator genes in Acinetobacter baumannii
title_full_unstemmed Transposon insertion sequencing reveals novel hypermutator genes in Acinetobacter baumannii
title_short Transposon insertion sequencing reveals novel hypermutator genes in Acinetobacter baumannii
title_sort transposon insertion sequencing reveals novel hypermutator genes in acinetobacter baumannii
topic hypermutator
tn-seq
tradis
mutation rate
Acinetobacter
url https://journals.asm.org/doi/10.1128/mbio.00966-25
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