Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes
Roy Kishony and colleagues sequenced the genomes of 112 Burkholderia dolosa isolates recovered from 14 individuals with cystic fibrosis as part of a retrospective study from a hospital epidemic monitored over the course of 16 years. They tracked recurrent mutations occurring in the bacterial isolate...
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| Published in | Nature genetics Vol. 43; no. 12; pp. 1275 - 1280 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.12.2011
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1061-4036 1546-1718 1546-1718 |
| DOI | 10.1038/ng.997 |
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| Abstract | Roy Kishony and colleagues sequenced the genomes of 112
Burkholderia dolosa
isolates recovered from 14 individuals with cystic fibrosis as part of a retrospective study from a hospital epidemic monitored over the course of 16 years. They tracked recurrent mutations occurring in the bacterial isolates and found that 17 genes showed evidence of parallel adaptive evolution.
Bacterial pathogens evolve during the infection of their human host
1
,
2
,
3
,
4
,
5
,
6
,
7
,
8
, but separating adaptive and neutral mutations remains challenging
9
,
10
,
11
. Here we identify bacterial genes under adaptive evolution by tracking recurrent patterns of mutations in the same pathogenic strain during the infection of multiple individuals. We conducted a retrospective study of a
Burkholderia dolosa
outbreak among subjects with cystic fibrosis, sequencing the genomes of 112 isolates collected from 14 individuals over 16 years. We find that 17 bacterial genes acquired nonsynonymous mutations in multiple individuals, which indicates parallel adaptive evolution. Mutations in these genes affect important pathogenic phenotypes, including antibiotic resistance and bacterial membrane composition and implicate oxygen-dependent regulation as paramount in lung infections. Several genes have not previously been implicated in pathogenesis and may represent new therapeutic targets. The identification of parallel molecular evolution as a pathogen spreads among multiple individuals points to the key selection forces it experiences within human hosts. |
|---|---|
| AbstractList | Bacterial pathogens evolve during the infection of their human hosts
1
-
8
, but separating adaptive and neutral mutations remains challenging
9
-
11
. Here, we identify bacterial genes under adaptive evolution by tracking recurrent patterns of mutations in the same pathogenic strain during the infection of multiple patients. We conducted a retrospective study of a
Burkholderia dolosa
outbreak among people with cystic fibrosis, sequencing the genomes of 112 isolates collected from 14 individuals over 16 years. We find that 17 bacterial genes acquired non-synonymous mutations in multiple individuals, which indicates parallel adaptive evolution. Mutations in these genes illuminate the genetic basis of important pathogenic phenotypes, including antibiotic resistance and bacterial membrane composition, and implicate oxygen-dependent gene regulation as paramount in lung infections. Several genes have not been previously implicated in pathogenesis, suggesting new therapeutic targets. The identification of parallel molecular evolution suggests key selection forces acting on pathogens within humans and can help predict and prepare for their future evolutionary course. Bacterial pathogens evolve during the infection of their human host, but separating adaptive and neutral mutations remains challenging. Here we identify bacterial genes under adaptive evolution by tracking recurrent patterns of mutations in the same pathogenic strain during the infection of multiple individuals. We conducted a retrospective study of a Burkholderia dolosa outbreak among subjects with cystic fibrosis, sequencing the genomes of 112 isolates collected from 14 individuals over 16 years. We find that 17 bacterial genes acquired nonsynonymous mutations in multiple individuals, which indicates parallel adaptive evolution. Mutations in these genes affect important pathogenic phenotypes, including antibiotic resistance and bacterial membrane composition and implicate oxygen-dependent regulation as paramount in lung infections. Several genes have not previously been implicated in pathogenesis and may represent new therapeutic targets. The identification of parallel molecular evolution as a pathogen spreads among multiple individuals points to the key selection forces it experiences within human hosts. [PUBLICATION ABSTRACT] Bacterial pathogens evolve during the infection of their human host(1-8), but separating adaptive and neutral mutations remains challenging(9-11). Here we identify bacterial genes under adaptive evolution by tracking recurrent patterns of mutations in the same pathogenic strain during the infection of multiple individuals. We conducted a retrospective study of a Burkholderia dolosa outbreak among subjects with cystic fibrosis, sequencing the genomes of 112 isolates collected from 14 individuals over 16 years. We find that 17 bacterial genes acquired nonsynonymous mutations in multiple individuals, which indicates parallel adaptive evolution. Mutations in these genes affect important pathogenic phenotypes, including antibiotic resistance and bacterial membrane composition and implicate oxygen-dependent regulation as paramount in lung infections. Several genes have not previously been implicated in pathogenesis and may represent new therapeutic targets. The identification of parallel molecular evolution as a pathogen spreads among multiple individuals points to the key selection forces it experiences within human hosts.Bacterial pathogens evolve during the infection of their human host(1-8), but separating adaptive and neutral mutations remains challenging(9-11). Here we identify bacterial genes under adaptive evolution by tracking recurrent patterns of mutations in the same pathogenic strain during the infection of multiple individuals. We conducted a retrospective study of a Burkholderia dolosa outbreak among subjects with cystic fibrosis, sequencing the genomes of 112 isolates collected from 14 individuals over 16 years. We find that 17 bacterial genes acquired nonsynonymous mutations in multiple individuals, which indicates parallel adaptive evolution. Mutations in these genes affect important pathogenic phenotypes, including antibiotic resistance and bacterial membrane composition and implicate oxygen-dependent regulation as paramount in lung infections. Several genes have not previously been implicated in pathogenesis and may represent new therapeutic targets. The identification of parallel molecular evolution as a pathogen spreads among multiple individuals points to the key selection forces it experiences within human hosts. Roy Kishony and colleagues sequenced the genomes of 112 Burkholderia dolosa isolates recovered from 14 individuals with cystic fibrosis as part of a retrospective study from a hospital epidemic monitored over the course of 16 years. They tracked recurrent mutations occurring in the bacterial isolates and found that 17 genes showed evidence of parallel adaptive evolution. Bacterial pathogens evolve during the infection of their human host 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , but separating adaptive and neutral mutations remains challenging 9 , 10 , 11 . Here we identify bacterial genes under adaptive evolution by tracking recurrent patterns of mutations in the same pathogenic strain during the infection of multiple individuals. We conducted a retrospective study of a Burkholderia dolosa outbreak among subjects with cystic fibrosis, sequencing the genomes of 112 isolates collected from 14 individuals over 16 years. We find that 17 bacterial genes acquired nonsynonymous mutations in multiple individuals, which indicates parallel adaptive evolution. Mutations in these genes affect important pathogenic phenotypes, including antibiotic resistance and bacterial membrane composition and implicate oxygen-dependent regulation as paramount in lung infections. Several genes have not previously been implicated in pathogenesis and may represent new therapeutic targets. The identification of parallel molecular evolution as a pathogen spreads among multiple individuals points to the key selection forces it experiences within human hosts. Bacterial pathogens evolve during the infection of their human host, but separating adaptive and neutral mutations remains challenging. Here we identify bacterial genes under adaptive evolution by tracking recurrent patterns of mutations in the same pathogenic strain during the infection of multiple individuals. We conducted a retrospective study of a Burkholderia dolosa outbreak among subjects with cystic fibrosis, sequencing the genomes of 112 isolates collected from 14 individuals over 16 years. We find that 17 bacterial genes acquired nonsynonymous mutations in multiple individuals, which indicates parallel adaptive evolution. Mutations in these genes affect important pathogenic phenotypes, including antibiotic resistance and bacterial membrane composition and implicate oxygen-dependent regulation as paramount in lung infections. Several genes have not previously been implicated in pathogenesis and may represent new therapeutic targets. The identification of parallel molecular evolution as a pathogen spreads among multiple individuals points to the key selection forces it experiences within human hosts. Bacterial pathogens evolve during the infection of their human host(1-8), but separating adaptive and neutral mutations remains challenging(9-11). Here we identify bacterial genes under adaptive evolution by tracking recurrent patterns of mutations in the same pathogenic strain during the infection of multiple individuals. We conducted a retrospective study of a Burkholderia dolosa outbreak among subjects with cystic fibrosis, sequencing the genomes of 112 isolates collected from 14 individuals over 16 years. We find that 17 bacterial genes acquired nonsynonymous mutations in multiple individuals, which indicates parallel adaptive evolution. Mutations in these genes affect important pathogenic phenotypes, including antibiotic resistance and bacterial membrane composition and implicate oxygen-dependent regulation as paramount in lung infections. Several genes have not previously been implicated in pathogenesis and may represent new therapeutic targets. The identification of parallel molecular evolution as a pathogen spreads among multiple individuals points to the key selection forces it experiences within human hosts. |
| Audience | Academic |
| Author | Goldberg, Joanna B Potter-Bynoe, Gail Kishony, Roy Lieberman, Tami D Skurnik, David Aingaran, Mythili Priebe, Gregory P Roux, Damien McAdam, Alexander J Leiby, Nicholas Michel, Jean-Baptiste Davis, Michael R LiPuma, John J |
| AuthorAffiliation | 8 Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA 4 Infection Prevention & Control, Children's Hospital Boston, Boston, MA, USA 3 Department of Medicine, Division of Infectious Diseases, Children's Hospital Boston, Boston, MA, USA 9 Department of Laboratory Medicine, Children's Hospital Boston, Boston, MA, USA 5 Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, Boston, MA, USA 2 Program for Evolutionary Dynamics, Harvard University, Cambridge, MA, USA 7 Department of Pediatrics, University of Michigan Medical School, Ann Arbor, MI, USA 11 School of Engineering and Applied Sciences, Harvard University, Cambridge, MA, USA 10 Department of Anesthesia, Division of Critical Care Medicine, Children's Hospital Boston, Boston MA, USA 1 Department of Systems Biology, Harvard Medical School, Boston, MA, USA 6 Department of Microbiology, University of Virginia Health System, Charlottesville, VA, USA |
| AuthorAffiliation_xml | – name: 5 Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, Boston, MA, USA – name: 7 Department of Pediatrics, University of Michigan Medical School, Ann Arbor, MI, USA – name: 8 Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA – name: 11 School of Engineering and Applied Sciences, Harvard University, Cambridge, MA, USA – name: 10 Department of Anesthesia, Division of Critical Care Medicine, Children's Hospital Boston, Boston MA, USA – name: 6 Department of Microbiology, University of Virginia Health System, Charlottesville, VA, USA – name: 4 Infection Prevention & Control, Children's Hospital Boston, Boston, MA, USA – name: 9 Department of Laboratory Medicine, Children's Hospital Boston, Boston, MA, USA – name: 1 Department of Systems Biology, Harvard Medical School, Boston, MA, USA – name: 2 Program for Evolutionary Dynamics, Harvard University, Cambridge, MA, USA – name: 3 Department of Medicine, Division of Infectious Diseases, Children's Hospital Boston, Boston, MA, USA |
| Author_xml | – sequence: 1 givenname: Tami D surname: Lieberman fullname: Lieberman, Tami D organization: Department of Systems Biology, Harvard Medical School – sequence: 2 givenname: Jean-Baptiste surname: Michel fullname: Michel, Jean-Baptiste organization: Department of Systems Biology, Harvard Medical School, Program for Evolutionary Dynamics, Harvard University – sequence: 3 givenname: Mythili surname: Aingaran fullname: Aingaran, Mythili organization: Department of Medicine, Division of Infectious Diseases, Children's Hospital Boston – sequence: 4 givenname: Gail surname: Potter-Bynoe fullname: Potter-Bynoe, Gail organization: Infection Prevention & Control, Children's Hospital Boston – sequence: 5 givenname: Damien surname: Roux fullname: Roux, Damien organization: Department of Medicine, Channing Laboratory, Brigham and Women's Hospital – sequence: 6 givenname: Michael R surname: Davis fullname: Davis, Michael R organization: Department of Microbiology, University of Virginia Health System – sequence: 7 givenname: David surname: Skurnik fullname: Skurnik, David organization: Department of Medicine, Channing Laboratory, Brigham and Women's Hospital – sequence: 8 givenname: Nicholas surname: Leiby fullname: Leiby, Nicholas organization: Department of Systems Biology, Harvard Medical School – sequence: 9 givenname: John J surname: LiPuma fullname: LiPuma, John J organization: Department of Pediatrics, University of Michigan Medical School, Department of Epidemiology, University of Michigan School of Public Health – sequence: 10 givenname: Joanna B surname: Goldberg fullname: Goldberg, Joanna B organization: Department of Microbiology, University of Virginia Health System – sequence: 11 givenname: Alexander J surname: McAdam fullname: McAdam, Alexander J email: alexander.mcadam@childrens.harvard.edu organization: Department of Laboratory Medicine, Children's Hospital Boston – sequence: 12 givenname: Gregory P surname: Priebe fullname: Priebe, Gregory P email: gregory_priebe@childrens.harvard.edu organization: Department of Medicine, Division of Infectious Diseases, Children's Hospital Boston, Department of Medicine, Channing Laboratory, Brigham and Women's Hospital, Department of Anesthesia, Division of Critical Care Medicine, Children's Hospital Boston – sequence: 13 givenname: Roy surname: Kishony fullname: Kishony, Roy email: roy_kishony@hms.harvard.edu organization: Department of Systems Biology, Harvard Medical School, School of Engineering and Applied Sciences, Harvard University |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25285522$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/22081229$$D View this record in MEDLINE/PubMed |
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| CODEN | NGENEC |
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| Snippet | Roy Kishony and colleagues sequenced the genomes of 112
Burkholderia dolosa
isolates recovered from 14 individuals with cystic fibrosis as part of a... Bacterial pathogens evolve during the infection of their human host(1-8), but separating adaptive and neutral mutations remains challenging(9-11). Here we... Bacterial pathogens evolve during the infection of their human host (1-8), but separating adaptive and neutral mutations remains challenging (9-11). Here we... Bacterial pathogens evolve during the infection of their human host, but separating adaptive and neutral mutations remains challenging. Here we identify... Bacterial pathogens evolve during the infection of their human hosts 1 - 8 , but separating adaptive and neutral mutations remains challenging 9 - 11 . Here,... |
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| SubjectTerms | 631/208/2489/144 631/208/514/1948 631/326/41/2531 Adaptation, Biological Agriculture Animal Genetics and Genomics Anti-Bacterial Agents - pharmacology Antibiotic resistance Antibiotics Bacteremia - microbiology Bacteria Bacterial genetics Bacterial infections Biological and medical sciences Biomedical and Life Sciences Biomedicine Burkholderia Burkholderia - drug effects Burkholderia - genetics Burkholderia - pathogenicity Burkholderia Infections - epidemiology Burkholderia Infections - microbiology Cancer Research Ciprofloxacin - pharmacology Cloning Cystic fibrosis Drug Resistance, Bacterial Epidemics Evolution Evolution & development Evolution, Molecular Evolutionary biology Fundamental and applied biological sciences. Psychology Gene Function Genes, Bacterial Genetic aspects Genetic diversity Genetics of eukaryotes. Biological and molecular evolution Genome, Bacterial Genomes Hospitals Host-Pathogen Interactions Human Genetics Human subjects Humans letter Likelihood Functions Lipopolysaccharides - genetics Lung Diseases - microbiology Microbial mutation Mutation Pathogenesis Pathogens Phylogeny Polymorphism, Single Nucleotide Retrospective Studies Selection, Genetic Virulence Factors - genetics |
| Title | Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes |
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