Inference of Homologous Recombination in Bacteria Using Whole-Genome Sequences

Didelot, Xavier; Lawson, Daniel J.; Darling, Aaron E.; Falush, Daniel

doi:10.1534/genetics.110.120121

Cited by 163 publications

(200 citation statements)

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“…Whole-genome approaches to detecting historical recombination are becoming increasingly practical as DNA sequencing costs decrease, and these reveal patterns of past recombination events that are not observable by MLST genotyping (67)(68)(69). However, these population-based approaches come with several caveats: a high historical recombination frequency may be due to horizontal gene transfer processes other than natural competence, and a competent species might show a low frequency due to scarcity of DNA from other strains, infrequent induction of competence, low recombination rates, or sampling of many nontransformable strains.…”

Section: The Phylogenetic Distribution Of Natural Competencementioning

confidence: 99%

“…Once they have arisen at specific positions, uptake sequences are stable; many USSs are in homologous positions in H. influenzae and its relative Pasteurella multocida despite the hundreds of millions of years since their divergence (101). Comparison of DUS locations in three closely related species of Neisseria also found strong conservation (100); more divergent genomes are now available for analysis (68).…”

Section: The Mechanism and Diversity Of Dna Uptake Specificitymentioning

confidence: 99%

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Natural Competence and the Evolution of DNA Uptake Specificity

2014

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Many bacteria are naturally competent, able to actively transport environmental DNA fragments across their cell envelope and into their cytoplasm. Because incoming DNA fragments can recombine with and replace homologous segments of the chromosome, competence provides cells with a potent mechanism of horizontal gene transfer as well as access to the nutrients in extracellular DNA. This review starts with an introductory overview of competence and continues with a detailed consideration of the DNA uptake specificity of competent proteobacteria in the Pasteurellaceae and Neisseriaceae. Species in these distantly related families exhibit strong preferences for genomic DNA from close relatives, a self-specificity arising from the combined effects of biases in the uptake machinery and genomic overrepresentation of the sequences this machinery prefers. Other competent species tested lack obvious uptake bias or uptake sequences, suggesting that strong convergent evolutionary forces have acted on these two families. Recent results show that uptake sequences have multiple "dialects," with clades within each family preferring distinct sequence variants and having corresponding variants enriched in their genomes. Although the genomic consensus uptake sequences are 12 and 29 to 34 bp, uptake assays have found that only central cores of 3 to 4 bp, conserved across dialects, are crucial for uptake. The other bases, which differ between dialects, make weaker individual contributions but have important cooperative interactions. Together, these results make predictions about the mechanism of DNA uptake across the outer membrane, supporting a model for the evolutionary accumulation and stability of uptake sequences and suggesting that uptake biases may be more widespread than currently thought. N aturally competent bacteria actively pull DNA fragments from their environment into their cells. These fragments provide nucleotides, but high similarity with the chromosome also allows them to change the cell's genotype by homologous recombination, a process called natural transformation ( Fig. 1; reviewed in references 1, 2, 3, 4, and 5). Most competent bacteria that have been tested can take up DNA from any source, but species in two distantly related families of Gram-negative bacteria, the Pasteurellaceae and the Neisseriaceae, show strong preferences for DNAs containing short sequences that are highly overrepresented in their own genomes, leading to preferential uptake of conspecific DNA (6). This self-specificity both raises questions about and provides a tool for investigating the evolution of competence and the mechanism of DNA uptake.We begin with a general overview of competence, emphasizing the evolutionary issues. We then describe the two components that together create self-specificity, sequence biases in the DNA uptake machinery and overrepresentation of uptake sequences in the genomes, highlighting recent work on the mechanism and evolution of uptake biases in the two families and an evolutionary model that accounts for upt...

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Section: The Phylogenetic Distribution Of Natural Competencementioning

confidence: 99%

Section: The Mechanism and Diversity Of Dna Uptake Specificitymentioning

confidence: 99%

Natural Competence and the Evolution of DNA Uptake Specificity

2014

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“…Standard phylogenetic methods can be used to build a core genome-wide phylogeny, and the average impact of recombination can be measured by assessing linkage disequilibrium among SNPs. Specific recombination events and breakpoints can then be identified using methods, such as BratNextGen (Marttinen et al 2012), ClonalFrame/ClonalOrigin (Didelot et al 2010), and STARRInIGHTS (Shapiro et al 2012). These analyses will reveal the number of major genotypic units (well-supported monophyletic groups), and whether these units are supported genome-wide (consistent with mostly clonal evolution) or in "islands" or "continents" of the genome.…”

Section: Microbial Speciationmentioning

confidence: 99%

Microbial Speciation

Shapiro

Polz

2015

Cold Spring Harb Perspect Biol

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“…Using a coalescent model with gene-conversion, computationally intensive methods have been developed that allow estimation of recombination rates on a whole-genome scale (Didelot et al 2010;Ansari and Didelot 2014). Other methods detect recombination events based on regional differences of single nucleotide polymorphism (SNP) density (Croucher et al 2015) or inferred phylogeny (Marttinen et al 2012), and are often used to establish a clonal phylogeny for a sample based on the vertically inherited regions.…”

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confidence: 99%

Correlated Mutations and Homologous Recombination Within Bacterial Populations

Lin

Kussell

2017

Genetics

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Inferring the rate of homologous recombination within a bacterial population remains a key challenge in quantifying the basic parameters of bacterial evolution. Due to the high sequence similarity within a clonal population, and unique aspects of bacterial DNA transfer processes, detecting recombination events based on phylogenetic reconstruction is often difficult, and estimating recombination rates using coalescent model-based methods is computationally expensive, and often infeasible for large sequencing data sets. Here, we present an efficient solution by introducing a set of mutational correlation functions computed using pairwise sequence comparison, which characterize various facets of bacterial recombination. We provide analytical expressions for these functions, which precisely recapitulate simulation results of neutral and adapting populations under different coalescent models. We used these to fit correlation functions measured at synonymous substitutions using whole-genome data on Escherichia coli and Streptococcus pneumoniae populations. We calculated and corrected for the effect of sample selection bias, i.e., the uneven sampling of individuals from natural microbial populations that exists in most datasets. Our method is fast and efficient, and does not employ phylogenetic inference or other computationally intensive numerics. By simply fitting analytical forms to measurements from sequence data, we show that recombination rates can be inferred, and the relative ages of different samples can be estimated. Our approach, which is based on population genetic modeling, is broadly applicable to a wide variety of data, and its computational efficiency makes it particularly attractive for use in the analysis of large sequencing datasets.KEYWORDS bacteria; homologous recombination; population diversity; sample selection bias; sample ages; adapting populations; Bolthausen-Sznitman coalescent B ACTERIA can receive DNA fragments from their environment by different mechanisms, and integrate them into their genome in a set of processes collectively known as horizontal gene transfer (HGT) (Thomas and Nielsen 2005). While the importance of HGT in bacterial evolution is increasingly appreciated (Koonin and Wolf 2008;Shapiro et al. 2012;Oren et al. 2014;Ravenhall et al. 2015;Rosen et al. 2015), quantifying its impact across bacterial genomes, and in diverse environmental samples, remains a key challenge (Maynard Smith 1991;Soucy et al. 2015). In particular, a prevalent form of HGT involves homologous recombination of fragments that bear a high degree of sequence similarity to the recipient genome (Andam and Gogarten 2011;Williams et al. 2012). Such transfer events are particularly difficult to detect, since they leave no obvious marks, and are indistinguishable based on nucleotide composition, yet they are likely to represent the majority of HGT events in bacteria (Fraser et al. 2007).Three major mechanisms of HGT-transformation, conjugation, and transduction-mediate the passage of external DNA into bacte...

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Inference of Homologous Recombination in Bacteria Using Whole-Genome Sequences

Cited by 163 publications

References 65 publications

Natural Competence and the Evolution of DNA Uptake Specificity

Natural Competence and the Evolution of DNA Uptake Specificity

Microbial Speciation

Correlated Mutations and Homologous Recombination Within Bacterial Populations

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