#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#
preLekára.sk / Odborné časopisy / PLOS Genetics / 2013 - 1

Mutational Spectrum Drives the Rise of Mutator Bacteria

English version České info

Understanding how mutator strains emerge in bacterial populations is relevant both to evolutionary theory and to reduce the threat they pose in clinical settings. The rise of mutator alleles is understood as a result of their hitchhiking with linked beneficial mutations, although the factors that govern this process remain unclear. A prominent but underappreciated fact is that each mutator allele increases only a specific spectrum of mutational changes. This spectrum has been speculated to alter the distribution of fitness effects of beneficial mutations, potentially affecting hitchhiking. To study this possibility, we analyzed the fitness distribution of beneficial mutations generated from different mutator and wild-type Escherichia coli strains. Using antibiotic resistance as a model system, we show that mutational spectra can alter these distributions substantially, ultimately determining the competitive ability of each strain across environments. Computer simulation showed that the effect of mutational spectrum on hitchhiking dynamics follows a non-linear function, implying that even slight spectrum-dependent fitness differences are sufficient to alter mutator success frequency by several orders of magnitude. These results indicate an unanticipated central role for the mutational spectrum in the evolution of bacterial mutation rates. At a practical level, this study indicates that knowledge of the molecular details of resistance determinants is crucial for minimizing mutator evolution during antibiotic therapy.

Vyšlo v časopise: Mutational Spectrum Drives the Rise of Mutator Bacteria. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003167
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003167

Souhrn

Understanding how mutator strains emerge in bacterial populations is relevant both to evolutionary theory and to reduce the threat they pose in clinical settings. The rise of mutator alleles is understood as a result of their hitchhiking with linked beneficial mutations, although the factors that govern this process remain unclear. A prominent but underappreciated fact is that each mutator allele increases only a specific spectrum of mutational changes. This spectrum has been speculated to alter the distribution of fitness effects of beneficial mutations, potentially affecting hitchhiking. To study this possibility, we analyzed the fitness distribution of beneficial mutations generated from different mutator and wild-type Escherichia coli strains. Using antibiotic resistance as a model system, we show that mutational spectra can alter these distributions substantially, ultimately determining the competitive ability of each strain across environments. Computer simulation showed that the effect of mutational spectrum on hitchhiking dynamics follows a non-linear function, implying that even slight spectrum-dependent fitness differences are sufficient to alter mutator success frequency by several orders of magnitude. These results indicate an unanticipated central role for the mutational spectrum in the evolution of bacterial mutation rates. At a practical level, this study indicates that knowledge of the molecular details of resistance determinants is crucial for minimizing mutator evolution during antibiotic therapy.

Zdroje

1. BoeL, DanielsenM, KnudsenS, PetersenJB, MaymannJ, et al. (2000) The frequency of mutators in populations of Escherichia coli. Mutat Res 448 : 47–55.

2. FunchainP, YeungA, StewartJL, LinR, SlupskaMM, et al. (2000) The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154 : 959–970.

3. LeClercJE, LiB, PayneWL, CebulaTA (1996) High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274 : 1208–1211.

4. SniegowskiPD, GerrishPJ, LenskiRE (1997) Evolution of high mutation rates in experimental populations of E. coli. Nature 387 : 703–705.

5. MaoEF, LaneL, LeeJ, MillerJH (1997) Proliferation of mutators in a cell population. J Bacteriol 179 : 417–422.

6. OliverA, CantónR, CampoP, BaqueroF, BlázquezJ (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288 : 1251–1253.

7. RichardsonAR, YuZ, PopovicT, StojiljkovicI (2002) Mutator clones of Neisseria meningitidis in epidemic serogroup A disease. Proc Natl Acad Sci USA 99 : 6103–6107.

8. PalC, MaciaMD, OliverA, SchacharI, BucklingA (2007) Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 450 : 1079–1081.

9. LeighEG (1970) Natural selection and mutability. Am Nat 104 : 301–305.

10. TaddeiF, RadmanM, Maynard-SmithJ, ToupanceB, GouyonPH, et al. (1997) Role of mutator alleles in adaptive evolution. Nature 387 : 700–702.

11. TenaillonO, ToupanceB, Le NagardH, TaddeiF, GodelleB (1999) Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics 152 : 485–493.

12. Notley-McRobbL, SeetoS, FerenciT (2002) Enrichment and elimination of mutY mutators in Escherichia coli populations. Genetics 162 : 1055–1062.

13. ShaverAC, DombrowskiPG, SweeneyJY, TreisT, ZappalaRM, et al. (2002) Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. Genetics 162 : 557–566.

14. TenaillonO, Le NagardH, GodelleB, TaddeiF (2000) Mutators and sex in bacteria: Conflict between adaptive strategies. Proc Natl Acad Sci USA 97 : 10465–10470.

15. BlázquezJ (2003) Hypermutation as a factor contributing to the acquisition of antimicrobial resistance. Clin Infect Dis 37 : 1201–1209.

16. LabatF, PradillonO, GarryL, PeuchmaurM, FantinB, et al. (2005) Mutator phenotype confers advantage in Escherichia coli chronic urinary tract infection pathogenesis. FEMS Immunol. Med Microbiol 44 : 317–321.

17. OliverA, MenaA (2010) Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin Microbiol Infect 16 : 798–808.

18. TravisJMJ, TravisER (2002) Mutator dynamics in fluctuating environments. Proc Biol Sci 269 : 591–597.

19. TanakaMM, BergstromCT, LevinBR (2003) The evolution of mutator genes in bacterial populations: the roles of environmental change and timing. Genetics 164 : 843–854.

20. WylieCS, GhimCM, KesslerD, LevineH (2009) The fixation probability of rare mutators in finite asexual populations. Genetics 181 : 1595–1612.

21. AndreJ, GodelleB (2006) The evolution of mutation rate in finite asexual populations. Genetics 172 : 611–626.

22. MaharjanR, SeetoS, Notley-McRobbL, FerenciT (2006) Clonal adaptive radiation in a constant environment. Science 313 : 514–517.

23. TenaillonO, Rodríguez-VerdugoA, GautRL, McDonaldP, BennettAF, et al. (2012) The molecular diversity of adaptive convergence. Science 335 : 457–461.

24. DenamurE, MaticI (2006) Evolution of mutation rates in bacteria. Mol Microbiol 60 : 820–827.

25. MillerJH (1996) Spontaneous mutators in bacteria: insights into pathways of mutagenesis and repair. Annu Rev Microbiol 50 : 625–643.

26. MacLeanRC, HallAR, PerronGG, BucklingA (2010) The population genetics of antibiotic resistance: integrating molecular mechanisms and treatment contexts. Nat Rev Genet 11 : 405–414.

27. GaribyanL, HuangT, KimM, WolffE, NguyenA, et al. (2003) Use of the rpoB gene to determine the specificity of base substitution mutations on the Escherichia coli chromosome. DNA Repair 2 : 593–608.

28. TimmsAR, SteingrimsdottirH, LehmannAR, BridgesBA (1992) Mutant sequences in the rpsL gene of Escherichia coli B/r: mechanistic implications for spontaneous and ultraviolet light mutagenesis. Mol Gen Genet 232 : 89–96.

29. BjedovI, DasguptaCN, SladeD, Le BlastierS, SelvaM, et al. (2007) Involvement of Escherichia coli DNA polymerase IV in tolerance of cytotoxic alkylating DNA lesions in vivo. Genetics 176 : 1431–1440.

30. HallAR, IlesJC, MacLeanRC (2002) The fitness cost of rifampicin resistance in Pseudomonas aeruginosa depends on demand for RNA polymerase. Genetics 187 : 817–822.

31. ReynoldsMG (2000) Compensatory evolution in rifampin-resistant Escherichia coli. Genetics 156 : 1471–1481.

32. Kurland C, Hughes D, Ehrenberg M (1996) Limitations of translational accuracy. In: Neidhardt F.C III, et al., editors. Escherichia coli and Salmonella: Cellular and molecular biology. ASM Press; Washington, DC: 1996. pp. 979–1004.

33. Kimura M (1994) Population genetics, molecular evolution, and the neutral theory: selected papers (University of Chicago Press)

34. BohannanBJ, LenskiRE (2000) Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett 3 : 362–377.

35. AnderssonDI, HughesD (2010) Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Micro 8 : 260–271.

36. PrindleMJ, FoxEJ, LoebLA (2010) The mutator phenotype in cancer: molecular mechanisms and targeting strategies. Curr. Drug Targets 11 : 1296–1303.

37. LenskiRE, RoseMR, SimpsonSC, TadlerSC (1991) Long-term experimental evolution in Escherichia coli I. Adaptation and divergence during 2,000 generations. Am Nat 138 : 1315–1341.

38. R Development Core Team (2011) R: A language and environment for statistical computing, reference index version 2.13.0. (R Foundation for Statistical Computing, Vienna).

39. de VisserJA, ZeylCW, GerrishPJ, BlanchardJL, LenskiRE (1999) Diminishing returns from mutation supply rate in asexual populations. Science 283 : 404–406.

40. AhrensJH, DieterU (1982) Computer generation of Poisson deviates from modified normal distributions. ACM Trans Math Softw 8 : 163–179.

41. RozenDE, de VisserJAGM, GerrishPJ (2002) Fitness effects of fixed beneficial mutations in microbial populations. Curr Biol 12 : 1040–1045.

42. TrindadeS, PerfeitoL, GordoI (2010) Rate and effects of spontaneous mutations that affect fitness in mutator Escherichia coli. Philos Trans R Soc Lond B Biol Sci 365 : 1177–1186.

Štítky
Genetika Reprodukčná medicína
Článek A Model of High Sugar Diet-Induced Cardiomyopathy
Článek Comparative Genome Structure, Secondary Metabolite, and Effector Coding Capacity across Pathogens
Článek Emerging Function of Fat Mass and Obesity-Associated Protein (Fto)
Článek Positional Cloning Reveals Strain-Dependent Expression of to Alter Susceptibility to Bleomycin-Induced Pulmonary Fibrosis in Mice
Článek Genetics of Ribosomal Proteins: “Curiouser and Curiouser”
Článek Transposable Elements Re-Wire and Fine-Tune the Transcriptome
Článek Function and Regulation of , a Gene Implicated in Autism and Human Evolution
Článek MAML1 Enhances the Transcriptional Activity of Runx2 and Plays a Role in Bone Development
Článek Predicting Mendelian Disease-Causing Non-Synonymous Single Nucleotide Variants in Exome Sequencing Studies
Článek A Systematic Mapping Approach of 16q12.2/ and BMI in More Than 20,000 African Americans Narrows in on the Underlying Functional Variation: Results from the Population Architecture using Genomics and Epidemiology (PAGE) Study
Článek Transcription of the Major microRNA–Like Small RNAs Relies on RNA Polymerase III
Článek Histone H3K56 Acetylation, Rad52, and Non-DNA Repair Factors Control Double-Strand Break Repair Choice with the Sister Chromatid
Článek Genome-Wide Association Study Identifies a Novel Susceptibility Locus at 12q23.1 for Lung Squamous Cell Carcinoma in Han Chinese
Článek Genetic Disruption of the Copulatory Plug in Mice Leads to Severely Reduced Fertility
Článek The [] Prion Exists as a Dynamic Cloud of Variants
Článek Adult Onset Global Loss of the Gene Alters Body Composition and Metabolism in the Mouse
Článek Fis Protein Insulates the Gene from Uncontrolled Transcription
Článek The Meiotic Nuclear Lamina Regulates Chromosome Dynamics and Promotes Efficient Homologous Recombination in the Mouse
Článek Genome-Wide Haplotype Analysis of Expression Quantitative Trait Loci in Monocytes
Článek TATES: Efficient Multivariate Genotype-Phenotype Analysis for Genome-Wide Association Studies
Článek Structural Basis of a Histone H3 Lysine 4 Demethylase Required for Stem Elongation in Rice
Článek The Ecm11-Gmc2 Complex Promotes Synaptonemal Complex Formation through Assembly of Transverse Filaments in Budding Yeast
Článek MCM8 Is Required for a Pathway of Meiotic Double-Strand Break Repair Independent of DMC1 in
Článek Comparative Genomic Analysis of the Endosymbionts of Herbivorous Insects Reveals Eco-Environmental Adaptations: Biotechnology Applications
Článek Integration of Nodal and BMP Signals in the Heart Requires FoxH1 to Create Left–Right Differences in Cell Migration Rates That Direct Cardiac Asymmetry
Článek Pharmacodynamics, Population Dynamics, and the Evolution of Persistence in
Článek A Hybrid Likelihood Model for Sequence-Based Disease Association Studies
Článek Aberration in DNA Methylation in B-Cell Lymphomas Has a Complex Origin and Increases with Disease Severity
Článek Multiple Opposing Constraints Govern Chromosome Interactions during Meiosis
Článek Transcriptional Dynamics Elicited by a Short Pulse of Notch Activation Involves Feed-Forward Regulation by Genes
Článek Dynamic Large-Scale Chromosomal Rearrangements Fuel Rapid Adaptation in Yeast Populations
Článek Heterologous Gln/Asn-Rich Proteins Impede the Propagation of Yeast Prions by Altering Chaperone Availability
Článek Gene Copy-Number Polymorphism Caused by Retrotransposition in Humans
Článek An Incompatibility between a Mitochondrial tRNA and Its Nuclear-Encoded tRNA Synthetase Compromises Development and Fitness in
Článek Secondary Metabolism and Development Is Mediated by LlmF Control of VeA Subcellular Localization in
Článek Single-Stranded Annealing Induced by Re-Initiation of Replication Origins Provides a Novel and Efficient Mechanism for Generating Copy Number Expansion via Non-Allelic Homologous Recombination
Článek Tbx2 Controls Lung Growth by Direct Repression of the Cell Cycle Inhibitor Genes and
Článek Suv4-20h Histone Methyltransferases Promote Neuroectodermal Differentiation by Silencing the Pluripotency-Associated Oct-25 Gene
Článek A Conserved Helicase Processivity Factor Is Needed for Conjugation and Replication of an Integrative and Conjugative Element
Článek Telomerase-Null Survivor Screening Identifies Novel Telomere Recombination Regulators
Článek Genome-Wide Analysis Reveals Selection for Important Traits in Domestic Horse Breeds
Článek Coordinated Degradation of Replisome Components Ensures Genome Stability upon Replication Stress in the Absence of the Replication Fork Protection Complex
Článek Nkx6.1 Controls a Gene Regulatory Network Required for Establishing and Maintaining Pancreatic Beta Cell Identity
Článek HIF- and Non-HIF-Regulated Hypoxic Responses Require the Estrogen-Related Receptor in
Článek Delineating a Conserved Genetic Cassette Promoting Outgrowth of Body Appendages
Článek The Telomere Capping Complex CST Has an Unusual Stoichiometry, Makes Multipartite Interaction with G-Tails, and Unfolds Higher-Order G-Tail Structures
Článek Comprehensive Methylome Characterization of and at Single-Base Resolution
Článek Loci Associated with -Glycosylation of Human Immunoglobulin G Show Pleiotropy with Autoimmune Diseases and Haematological Cancers
Článek Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel Insights from a Network-Based SNP Discovery Protocol
Článek Centromere-Like Regions in the Budding Yeast Genome
Článek Sequencing of Loci from the Elephant Shark Reveals a Family of Genes in Vertebrate Genomes, Forged by Ancient Duplications and Divergences
Článek Mendelian and Non-Mendelian Regulation of Gene Expression in Maize
Článek Human Disease-Associated Genetic Variation Impacts Large Intergenic Non-Coding RNA Expression
Článek The Roles of Whole-Genome and Small-Scale Duplications in the Functional Specialization of Genes
Článek Sex-Specific Signaling in the Blood–Brain Barrier Is Required for Male Courtship in
Článek A Newly Uncovered Group of Distantly Related Lysine Methyltransferases Preferentially Interact with Molecular Chaperones to Regulate Their Activity
Článek Is Required for Leptin-Mediated Depolarization of POMC Neurons in the Hypothalamic Arcuate Nucleus in Mice
Článek Unlocking the Bottleneck in Forward Genetics Using Whole-Genome Sequencing and Identity by Descent to Isolate Causative Mutations
Článek The Role of Autophagy in Genome Stability through Suppression of Abnormal Mitosis under Starvation
Článek MTERF3 Regulates Mitochondrial Ribosome Biogenesis in Invertebrates and Mammals
Článek Downregulation and Altered Splicing by in a Mouse Model of Facioscapulohumeral Muscular Dystrophy (FSHD)
Článek NBR1-Mediated Selective Autophagy Targets Insoluble Ubiquitinated Protein Aggregates in Plant Stress Responses
Článek Retroactive Maintains Cuticle Integrity by Promoting the Trafficking of Knickkopf into the Procuticle of
Článek Phenome-Wide Association Study (PheWAS) for Detection of Pleiotropy within the Population Architecture using Genomics and Epidemiology (PAGE) Network
Článek Genetic and Functional Modularity of Activities in the Specification of Limb-Innervating Motor Neurons
Článek A Population Genetic Model for the Maintenance of R2 Retrotransposons in rRNA Gene Loci
Článek A Quartet of PIF bHLH Factors Provides a Transcriptionally Centered Signaling Hub That Regulates Seedling Morphogenesis through Differential Expression-Patterning of Shared Target Genes in
Článek A Genome-Wide Integrative Genomic Study Localizes Genetic Factors Influencing Antibodies against Epstein-Barr Virus Nuclear Antigen 1 (EBNA-1)
Článek Mutation of the Diamond-Blackfan Anemia Gene in Mouse Results in Morphological and Neuroanatomical Phenotypes
Článek Life, the Universe, and Everything: An Interview with David Haussler
Článek Alternative Oxidase Expression in the Mouse Enables Bypassing Cytochrome Oxidase Blockade and Limits Mitochondrial ROS Overproduction
Článek An Evolutionarily Conserved Synthetic Lethal Interaction Network Identifies FEN1 as a Broad-Spectrum Target for Anticancer Therapeutic Development
Článek The Flowering Repressor Underlies a Novel QTL Interacting with the Genetic Background
Článek Telomerase Is Required for Zebrafish Lifespan
Článek and Diversified Expression of the Gene Family Bolster the Floral Stem Cell Network
Článek Susceptibility Loci Associated with Specific and Shared Subtypes of Lymphoid Malignancies
Článek An Insertion in 5′ Flanking Region of Causes Blue Eggshell in the Chicken
Článek Increased Maternal Genome Dosage Bypasses the Requirement of the FIS Polycomb Repressive Complex 2 in Arabidopsis Seed Development
Článek WNK1/HSN2 Mutation in Human Peripheral Neuropathy Deregulates Expression and Posterior Lateral Line Development in Zebrafish ()
Článek Synergistic Interaction of Rnf8 and p53 in the Protection against Genomic Instability and Tumorigenesis
Článek Dot1-Dependent Histone H3K79 Methylation Promotes Activation of the Mek1 Meiotic Checkpoint Effector Kinase by Regulating the Hop1 Adaptor
Článek A Heterogeneous Mixture of F-Series Prostaglandins Promotes Sperm Guidance in the Reproductive Tract
Článek Starvation, Together with the SOS Response, Mediates High Biofilm-Specific Tolerance to the Fluoroquinolone Ofloxacin
Článek Directed Evolution of a Model Primordial Enzyme Provides Insights into the Development of the Genetic Code
Článek Genome-Wide Screens for Tinman Binding Sites Identify Cardiac Enhancers with Diverse Functional Architectures
Článok vyšiel v časopise

PLOS Genetics

2013 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

nový kurz
Autori: doc. MUDr. David Zemánek, Ph.D., MUDr. Anna Chaloupka, Ph.D.
Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#