Mobile elements drive recombination hotspots in the core genome of Staphylococcus aureus

Everitt, Richard G.; Didelot, Xavier; Batty, Elizabeth M.; Miller, Ruth R.; Knox, Kyle; Young, Bernadette C.; Bowden, Rory; Auton, Adam; Votintseva, Antonina A.; Larner-Svensson, Hanna; Charlesworth, Jane; Golubchik, Tanya; Ip, Camilla L. C.; Godwin, Heather; Fung, Rowena; Peto, Tim E. A.; Walker, A. Sarah; Crook, Derrick W.; Wilson, Daniel J.

doi:10.1038/ncomms4956

Cited by 133 publications

(147 citation statements)

References 70 publications

(113 reference statements)

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“…As might be expected, the power and accuracy of these algorithms are maximized when a donor sequence is included (imparting the source of homology between unrelated lineages) and when the recombinant sequence introduces many polymorphic nucleotides (43,46). Therefore, homoplasiescharacters that are inferred to be shared by, but not present in, the common ancestor of lineages-represent robust signals of recombination and provide a very fine (i.e., per nucleotide site) resolution of recombination maps, as have been performed recently for sequenced strains of Staphylococcus aureus (47). Homoplasic sites allow detection of internal recombination events (i.e., recombinant polymorphic sites that are included in the dataset) but ignore polymorphic sites that were introduced by external, unsampled sources.…”

Section: How To Best Assess the Impact Of Recombination On E Coli Evmentioning

confidence: 99%

“…There are many classes of accessory genes, such as mobile elements (e.g., prophages, transposons), which are known to be associated with elevated rates of recombination. In both E. coli and S. aureus, it was recently shown that core genes in the vicinity of accessory genes or mobile elements experience higher recombination rates (44,47). Chromosome loci with the highest homologous recombination rates (recombination hotspots) have also been associated with nonmobilizable genomic islands in E. coli (e.g., the fim locus).…”

Section: Beyond the Core Genomementioning

confidence: 99%

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Impermanence of bacterial clones

Bobay

Traverse

Ochman

2015

Proc. Natl. Acad. Sci. U.S.A.

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Bacteria reproduce asexually and pass on a single genome copied from the parent, a reproductive mode that assures the clonal descent of progeny; however, a truly clonal bacterial species is extremely rare. The signal of clonality can be interrupted by gene uptake and exchange, initiating homologous recombination that results in the unique sequence of one clone being incorporated into another. Because recombination occurs sporadically and on local scales, these events are often difficult to recognize, even when considering large samples of completely sequenced genomes. Moreover, several processes can produce the appearance of clonality in populations that undergo frequent recombination. The rates and consequences of recombination have been studied in Escherichia coli for over 40 y, and, during this time, there have been several shifting views of its clonal status, population structure, and rates of gene exchange. We reexamine the studies and retrace the evolution of the methods that have assessed the extent of DNA flux, largely focusing on its impact on the E. coli genome.clonality | homologous exchange | recombination | genome evolution | E. coli R eproduction by binary fission virtually guarantees the clonality of a bacterial lineage. Apart from mutations and other rare events that might modify chromosome integrity during replication, the primary sequence of DNA in all daughter and descendent cells remains identical, generation after generation after generation. Unlike animals, in which parthenogenetic forms are ecologically constrained and relatively short-lived over evolutionary timescales (1-3), asexually reproducing bacteria have persisted since the origin of cellular life and represent the most diverse and widespread organisms on the planet. Naturally, the vast diversity present in bacteria could have arisen solely by asexual means-there has certainly been sufficient time and large enough population sizes to allow for enormous numbers of mutations (and combinations of mutations) to be experienced. Moreover, it seems as though some of the most extraordinary innovations in the history of life have occurred without intervention of the sexual process (4). Bacteria as Clonal OrganismsDespite their obligatory asexual mode of reproduction, the clonality of bacterial lineages can be disrupted by sex, or at least by what we refer to as sex. In bacteria, sex is the inheritance of genetic material from any source aside from their one parent cell and can occur by any of several processes. Foreign DNA can be introduced by cell-to-cell contact, transmitted to the cell by an infectious agent, or acquired directly from the environment; and, therefore, genes can be obtained from organisms representing any domain of life, and even from entities (i.e., viruses and phages) that are not classified to any domain of life. Moreover, events of sex in bacteria occur without known regularity and usually constitute a very small portion of the genome. In fact, sexually acquired DNA need not involve recombination at all but can persist...

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Section: How To Best Assess the Impact Of Recombination On E Coli Evmentioning

confidence: 99%

Section: Beyond the Core Genomementioning

confidence: 99%

Impermanence of bacterial clones

Bobay

Traverse

Ochman

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…To explore whether recombination was due to donors from the same lineage, we classed homoplasic SNPs as those confined to a certain lineage as opposed to those found in multiple lineages. The number of such positions were scaled by the synapomorphic SNPs in a 10-kb sliding window at 1-kb intervals across the genome, similar to the method previously described (Everitt et al 2014) …”

Section: Recombination Analysismentioning

confidence: 99%

Comprehensive global genome dynamics of Chlamydia trachomatis show ancient diversification followed by contemporary mixing and recent lineage expansion

et al. 2017

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Chlamydia trachomatis is the world's most prevalent bacterial sexually transmitted infection and leading infectious cause of blindness, yet it is one of the least understood human pathogens, in part due to the difficulties of in vitro culturing and the lack of available tools for genetic manipulation. Genome sequencing has reinvigorated this field, shedding light on the contemporary history of this pathogen. Here, we analyze 563 full genomes, 455 of which are novel, to show that the history of the species comprises two phases, and conclude that the currently circulating lineages are the result of evolution in different genomic ecotypes. Temporal analysis indicates these lineages have recently expanded in the space of thousands of years, rather than the millions of years as previously thought, a finding that dramatically changes our understanding of this pathogen's history. Finally, at a time when almost every pathogen is becoming increasingly resistant to antimicrobials, we show that there is no evidence of circulating genomic resistance in C. trachomatis.

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“…Our results provided no evidence for the mobilization of sequences flanking the element's integration site. Thus, the mechanism responsible for the strong signal of chromosomal recombination adjacent to the integration site of ICE6013 in S. aureus strain MRSA252 (20) requires further study. The frequencies of ICE6013 conjugation between some strains approached that of the well-studied conjugative plasmid pGO1 (47,48).…”

Section: Discussionmentioning

confidence: 99%

“…ICE6013 was noted to have relatively low integration site specificity, since the 3-bp target site that forms a direct repeat upon integration was variable in sequence and integration occurred at 11 different loci among 12 different strains of S. aureus (13). According to one analysis, the ICE6013 integration site in strain MRSA252 is adjacent to the strongest hot spot for recombination in the S. aureus chromosome (20). However, neither the integration site preference nor the conjugative transfer of ICE6013 or its flanking chromosomal sequences has been experimentally demonstrated.…”

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confidence: 99%

Transposase-Mediated Excision, Conjugative Transfer, and Diversity of ICE 6013 Elements in Staphylococcus aureus

et al. 2017

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ICE6013 represents one of two families of integrative conjugative elements (ICEs) identified in the pan-genome of the human and animal pathogen Staphylococcus aureus. Here we investigated the excision and conjugation functions of ICE6013 and further characterized the diversity of this element. ICE6013 excision was not significantly affected by growth, temperature, pH, or UV exposure and did not depend on recA. The IS30-like DDE transposase (Tpase; encoded by orf1 and orf2) of ICE6013 must be uninterrupted for excision to occur, whereas disrupting three of the other open reading frames (ORFs) on the element significantly affects the level of excision. We demonstrate that ICE6013 conjugatively transfers to different S. aureus backgrounds at frequencies approaching that of the conjugative plasmid pGO1. We found that excision is required for conjugation, that not all S. aureus backgrounds are successful recipients, and that transconjugants acquire the ability to transfer ICE6013. Sequencing of chromosomal integration sites in serially passaged transconjugants revealed a significant integration site preference for a 15-bp AT-rich palindromic consensus sequence, which surrounds the 3-bp target site that is duplicated upon integration. A sequence analysis of ICE6013 from different host strains of S. aureus and from eight other species of staphylococci identified seven divergent subfamilies of ICE6013 that include sequences previously classified as a transposon, a plasmid, and various ICEs. In summary, these results indicate that the IS30-like Tpase functions as the ICE6013 recombinase and that ICE6013 represents a diverse family of mobile genetic elements that mediate conjugation in staphylococci.IMPORTANCE Integrative conjugative elements (ICEs) encode the abilities to integrate into and excise from bacterial chromosomes and plasmids and mediate conjugation between bacteria. As agents of horizontal gene transfer, ICEs may affect bacterial evolution. ICE6013 represents one of two known families of ICEs in the pathogen Staphylococcus aureus, but its core functions of excision and conjugation are not well studied. Here, we show that ICE6013 depends on its IS30-like DDE transposase for excision, which is unique among ICEs, and we demonstrate the conjugative transfer and integration site preference of ICE6013. A sequence analysis revealed that ICE6013 has diverged into seven subfamilies that are dispersed among staphylococci.

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Mobile elements drive recombination hotspots in the core genome of Staphylococcus aureus

Cited by 133 publications

References 70 publications

Impermanence of bacterial clones

Impermanence of bacterial clones

Comprehensive global genome dynamics of Chlamydia trachomatis show ancient diversification followed by contemporary mixing and recent lineage expansion

Transposase-Mediated Excision, Conjugative Transfer, and Diversity of ICE 6013 Elements in Staphylococcus aureus

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