Homologous Recombination Drives Both Sequence Diversity and Gene Content Variation in Neisseria meningitidis

Kong, Ying‐Yee; Jennifer, H.; Warren, Keisha; Tsang, Raymond S. W.; Low, Donald E.; Alexander, David C.; Hao, Weilong

doi:10.1093/gbe/evt116

Cited by 39 publications

(54 citation statements)

References 78 publications

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“…Although the urethritis clusters caused by the US_NmUC isolates represent a clonal expansion event with no variation by conventional genotyping (MLST, fine-typing antigens), continued genomic alteration and evolution were evident within the genomes. For example, multiple genomic regions of the Columbus CNM26 isolate showed SNP differences in short nucleotide segments of a few hundred base pairs (mosaic nucleotide sequence variation) (16) from the corresponding regions of CNM10, which was isolated ∼1 1/2 mo earlier, indicating that homologous recombination is continuing to contribute to the evolution of this clade. Phylogenetic comparison of the US_NmUC isolates to lineage 11 isolates presented by Lucidarme et al (12) and additional urogenital isolates identified in the PubMLST database using the Genome Comparator tool (17) clearly showed that the clade forms a distinct branch within the lineage 11.2 (Fig.…”

Section: Resultsmentioning

confidence: 99%

Emergence of a new Neisseria meningitidis clonal complex 11 lineage 11.2 clade as an effective urogenital pathogen

Tzeng

Bazan

Turner

et al. 2017

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

124

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Neisseria meningitidis (Nm) clonal complex 11 (cc11) lineage is a hypervirulent pathogen responsible for outbreaks of invasive meningococcal disease, including among men who have sex with men, and is increasingly associated with urogenital infections. Recently, clusters of Nm urethritis have emerged primarily among heterosexual males in the United States. We determined that nonencapsulated meningococcal isolates from an ongoing Nm urethritis outbreak among epidemiologically unrelated men in Columbus, Ohio, are linked to increased Nm urethritis cases in multiple US cities, including Atlanta and Indianapolis, and that they form a unique clade (the US Nm urethritis clade, US_NmUC). The isolates belonged to the cc11 lineage 11.2/ET-15 with fine type of PorA P1.5–1, 10–8; FetA F3-6; PorB 2–2 and express a unique FHbp allele. A common molecular fingerprint of US_NmUC isolates was an IS1301 element in the intergenic region separating the capsule ctr-css operons and adjacent deletion of cssA/B/C and a part of csc, encoding the serogroup C capsule polymerase. This resulted in the loss of encapsulation and intrinsic lipooligosaccharide sialylation that may promote adherence to mucosal surfaces. Furthermore, we detected an IS1301-mediated inversion of an ∼20-kb sequence near the cps locus. Surprisingly, these isolates had acquired by gene conversion the complete gonococcal denitrification norB-aniA gene cassette, and strains grow well anaerobically. The cc11 US_NmUC isolates causing urethritis clusters in the United States may have adapted to a urogenital environment by loss of capsule and gene conversion of the Neisseria gonorrheae norB-aniA cassette promoting anaerobic growth.

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Section: Resultsmentioning

confidence: 99%

Emergence of a new Neisseria meningitidis clonal complex 11 lineage 11.2 clade as an effective urogenital pathogen

Tzeng

Bazan

Turner

et al. 2017

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

124

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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%

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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“…MLSA studies can also be constructed on information derived from wholegenome sequence data, such as those based on ribosomal protein subunit genes (rMLST) ( Jolley et al, 2012;Read et al, 2013) that allow strains to be assigned to taxonomic ranks from strains to domains; such studies allow the roles that adaptive and virulence genes play in speciation to be explored (Didelot et al, 2012;Hernandez-Lopez et al, 2013;Kong et al, 2013;Paul et al, 2013).…”

Section: Mlsa Based On Whole Genome Sequencesmentioning

confidence: 99%

“…MLSA is widely used to type the genetic structure of bacterial populations (Kong et al, 2013;Yahara et al, 2012). Doroghazi and Buckley (2010) used MLSA to quantify intra-and inter-species homologous recombination among streptomycetes and found high levels of gene exchange compared to many other bacterial groups (Vos & Didelot, 2009).…”

Section: Mlsa Based On Whole Genome Sequencesmentioning

confidence: 99%