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

ABSTRACT: 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.

SUBMITTER: Hadfield J

PROVIDER: S-EPMC5495073 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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Comprehensive global genome dynamics of <i>Chlamydia trachomatis</i> show ancient diversification followed by contemporary mixing and recent lineage expansion.

Hadfield James J Harris Simon R SR Seth-Smith Helena M B HMB Parmar Surendra S Andersson Patiyan P Giffard Philip M PM Schachter Julius J Moncada Jeanne J Ellison Louise L Vaulet María Lucía Gallo MLG Fermepin Marcelo Rodríguez MR Radebe Frans F Mendoza Suyapa S Ouburg Sander S Morré Servaas A SA Sachse Konrad K Puolakkainen Mirja M Korhonen Suvi J SJ Sonnex Chris C Wiggins Rebecca R Jalal Hamid H Brunelli Tamara T Casprini Patrizia P Pitt Rachel R Ison Cathy C Savicheva Alevtina A Shipitsyna Elena E Hadad Ronza R Kari Laszlo L Burton Matthew J MJ Mabey David D Solomon Anthony W AW Lewis David D Marsh Peter P Unemo Magnus M Clarke Ian N IN Parkhill Julian J Thomson Nicholas R NR

Genome research 20170606 7

<i>Chlamydia trachomatis</i> 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 histo ...[more]

PMID: 28588068

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Project description:BACKGROUND: The evolution and origin of cave organisms is a recurring issue in evolutionary studies, but analyses are often hindered by the inaccessibility of caves, morphological convergence, and complex colonization processes. Here we investigated the evolutionary history of Nesticella cave spiders, which are mainly distributed in the Yunnan-Guizhou Plateau, China. With comprehensive sampling and phylogenetic and coalescent-based analyses, we investigated the tempo and mode of diversification and the origins of these troglobites. We also aimed to determine which factors have influenced the diversification of this little-known group. RESULTS: Coalescent-based species delimitation validated the 18 species recognized by morphological inspection and also suggested the existence of cryptic lineages. Divergence time estimates suggested that Nesticella cave spiders in the Yunnan-Guizhou Plateau constituted a monophyletic troglobite clade that originated in the middle Miocene (11.1-18.6 Ma). Although the Yunnan-Guizhou Plateau clade was composed exclusively of troglobite species, suggesting an ancient common subterranean ancestor, we favor multiple, independent cave colonizations during the Pleistocene over a single ancient cave colonization event to explain the origin of these cave faunas. The diversification of plateau Nesticella has been greatly influenced by the sequential uplift of the plateau and likely reflects multiple cave colonizations over time by epigean ancestors during Pleistocene glacial advances. CONCLUSIONS: We concluded that plateau cave Nesticella represent an ancient group of spiders, but with young troglobite lineages that invaded caves only recently. The absence of extant epigean relatives and nearly complete isolation among caves supported their relict status. Our work highlights the importance of comprehensive sampling for studies of subterranean diversity and the evolution of cave organisms. The existence of potentially cryptic species and the relict status of Nesticella highlight the need to conserve these cave spiders.

Project description:Introduction Chlamydia trachomatis (C. trachomatis) is a Gram-negative bacterium and a common human pathogen. The World Health Organization (WHO) estimates that over 130 million people are infected with C. trachomatis globally each year and with increasing incidence. C. trachomatis causes long-lasting and recurrent infections that over time induce severe tissue damage in the female genital tract that can lead to ectopic pregnancy and infertility. Thus, the human immune system fails to control and eradicate C. trachomatis during primary infection and fails to develop protective immunity against secondary infections. In vivo infection models, using complement knock out mice, suggest that the complement system is critically involved in both anti-chlamydial immunity and infection-induced pathology. To increase our understanding of complement-mediated immunity against C. trachomatis we analyzed global complement deposition on serum-incubated C. trachomatis by mass spectrometry. Methods Purified C. trachomatis was incubated in seronegative normal human serum (NHS) or heat-inactivated normal human serum (HI-NHS) for 30 min, thoroughly washed, and processed for mass spectrometry. All samples were lysed, reduced and alkylated and digested with trypsin. Some samples were chemically modified to acetylate free amino groups (N-terminal and lysine amino groups) before trypsin digestion. Peptides were analyzed on a UltimateTM 3500 RSLCnano coupled to a Q Exactive HF-X mass spectrometer. Raw data files were searched against the Uniprot human reference proteome using MaxQuant. Results We demonstrate that C. trachomatis elicits potent complement activation demonstrated by deposition of both early and late complement factors together with several complement regulators. We further demonstrate proteolytically processing of complement C3b to “inactive” C3 cleavage fragments. Conclusion We demonstrate the deposition of several novel complement-associated proteins and -cleavage fragments on the surface of C. trachomatis.

Project description:The genome sequences of Chlamydia trachomatis mouse pneumonitis (MoPn) strain Nigg (1 069 412 nt) and Chlamydia pneumoniae strain AR39 (1 229 853 nt) were determined using a random shotgun strategy. The MoPn genome exhibited a general conservation of gene order and content with the previously sequenced C.trachomatis serovar D. Differences between C.trachomatis strains were focused on an approximately 50 kb 'plasticity zone' near the termination origins. In this region MoPn contained three copies of a novel gene encoding a >3000 amino acid toxin homologous to a predicted toxin from Escherichia coli O157:H7 but had apparently lost the tryptophan biosyntheis genes found in serovar D in this region. The C. pneumoniae AR39 chromosome was >99.9% identical to the previously sequenced C.pneumoniae CWL029 genome, however, comparative analysis identified an invertible DNA segment upstream of the uridine kinase gene which was in different orientations in the two genomes. AR39 also contained a novel 4524 nt circular single-stranded (ss)DNA bacteriophage, the first time a virus has been reported infecting C. pneumoniae. Although the chlamydial genomes were highly conserved, there were intriguing differences in key nucleotide salvage pathways: C.pneumoniae has a uridine kinase gene for dUTP production, MoPn has a uracil phosphororibosyl transferase, while C.trachomatis serovar D contains neither gene. Chromosomal comparison revealed that there had been multiple large inversion events since the species divergence of C.trachomatis and C.pneumoniae, apparently oriented around the axis of the origin of replication and the termination region. The striking synteny of the Chlamydia genomes and prevalence of tandemly duplicated genes are evidence of minimal chromosome rearrangement and foreign gene uptake, presumably owing to the ecological isolation of the obligate intracellular parasites. In the absence of genetic analysis, comparative genomics will continue to provide insight into the virulence mechanisms of these important human pathogens.

Dataset Information

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

Publications

Comprehensive global genome dynamics of <i>Chlamydia trachomatis</i> show ancient diversification followed by contemporary mixing and recent lineage expansion.

Similar Datasets

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