Global phylogeny of Treponema pallidum lineages reveals recent expansion and spread of contemporary syphilis
Syphilis, which is caused by the sexually transmitted bacterium Treponema pallidum subsp. pallidum , has an estimated 6.3 million cases worldwide per annum. In the past ten years, the incidence of syphilis has increased by more than 150% in some high-income countries, but the evolution and epidemiol...
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| Published in | Nature microbiology Vol. 6; no. 12; pp. 1549 - 1560 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.12.2021
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2058-5276 2058-5276 |
| DOI | 10.1038/s41564-021-01000-z |
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| Abstract | Syphilis, which is caused by the sexually transmitted bacterium
Treponema pallidum
subsp.
pallidum
, has an estimated 6.3 million cases worldwide per annum. In the past ten years, the incidence of syphilis has increased by more than 150% in some high-income countries, but the evolution and epidemiology of the epidemic are poorly understood. To characterize the global population structure of
T. pallidum
, we assembled a geographically and temporally diverse collection of 726 genomes from 626 clinical and 100 laboratory samples collected in 23 countries. We applied phylogenetic analyses and clustering, and found that the global syphilis population comprises just two deeply branching lineages, Nichols and SS14. Both lineages are currently circulating in 12 of the 23 countries sampled. We subdivided
T. p.
pallidum
into 17 distinct sublineages to provide further phylodynamic resolution. Importantly, two Nichols sublineages have expanded clonally across 9 countries contemporaneously with SS14. Moreover, pairwise genome analyses revealed examples of isolates collected within the last 20 years from 14 different countries that had genetically identical core genomes, which might indicate frequent exchange through international transmission. It is striking that most samples collected before 1983 are phylogenetically distinct from more recently isolated sublineages. Using Bayesian temporal analysis, we detected a population bottleneck occurring during the late 1990s, followed by rapid population expansion in the 2000s that was driven by the dominant
T. pallidum
sublineages circulating today. This expansion may be linked to changing epidemiology, immune evasion or fitness under antimicrobial selection pressure, since many of the contemporary syphilis lineages we have characterized are resistant to macrolides.
Global syphilis prevalence has been increasing. Sequencing and analysis of a global collection of 726
Treponema pallidum
samples reveal globally circulating lineages linked to a rapid expansion occurring since the end of the twentieth century. |
|---|---|
| AbstractList | Syphilis, which is caused by the sexually transmitted bacterium Treponema pallidum subsp. pallidum, has an estimated 6.3 million cases worldwide per annum. In the past ten years, the incidence of syphilis has increased by more than 150% in some high-income countries, but the evolution and epidemiology of the epidemic are poorly understood. To characterize the global population structure of T. pallidum, we assembled a geographically and temporally diverse collection of 726 genomes from 626 clinical and 100 laboratory samples collected in 23 countries. We applied phylogenetic analyses and clustering, and found that the global syphilis population comprises just two deeply branching lineages, Nichols and SS14. Both lineages are currently circulating in 12 of the 23 countries sampled. We subdivided T. p. pallidum into 17 distinct sublineages to provide further phylodynamic resolution. Importantly, two Nichols sublineages have expanded clonally across 9 countries contemporaneously with SS14. Moreover, pairwise genome analyses revealed examples of isolates collected within the last 20 years from 14 different countries that had genetically identical core genomes, which might indicate frequent exchange through international transmission. It is striking that most samples collected before 1983 are phylogenetically distinct from more recently isolated sublineages. Using Bayesian temporal analysis, we detected a population bottleneck occurring during the late 1990s, followed by rapid population expansion in the 2000s that was driven by the dominant T. pallidum sublineages circulating today. This expansion may be linked to changing epidemiology, immune evasion or fitness under antimicrobial selection pressure, since many of the contemporary syphilis lineages we have characterized are resistant to macrolides.Syphilis, which is caused by the sexually transmitted bacterium Treponema pallidum subsp. pallidum, has an estimated 6.3 million cases worldwide per annum. In the past ten years, the incidence of syphilis has increased by more than 150% in some high-income countries, but the evolution and epidemiology of the epidemic are poorly understood. To characterize the global population structure of T. pallidum, we assembled a geographically and temporally diverse collection of 726 genomes from 626 clinical and 100 laboratory samples collected in 23 countries. We applied phylogenetic analyses and clustering, and found that the global syphilis population comprises just two deeply branching lineages, Nichols and SS14. Both lineages are currently circulating in 12 of the 23 countries sampled. We subdivided T. p. pallidum into 17 distinct sublineages to provide further phylodynamic resolution. Importantly, two Nichols sublineages have expanded clonally across 9 countries contemporaneously with SS14. Moreover, pairwise genome analyses revealed examples of isolates collected within the last 20 years from 14 different countries that had genetically identical core genomes, which might indicate frequent exchange through international transmission. It is striking that most samples collected before 1983 are phylogenetically distinct from more recently isolated sublineages. Using Bayesian temporal analysis, we detected a population bottleneck occurring during the late 1990s, followed by rapid population expansion in the 2000s that was driven by the dominant T. pallidum sublineages circulating today. This expansion may be linked to changing epidemiology, immune evasion or fitness under antimicrobial selection pressure, since many of the contemporary syphilis lineages we have characterized are resistant to macrolides. Syphilis, which is caused by the sexually transmitted bacterium Treponema pallidum subsp. pallidum, has an estimated 6.3 million cases worldwide per annum. In the past ten years, the incidence of syphilis has increased by more than 150% in some high-income countries, but the evolution and epidemiology of the epidemic are poorly understood. To characterize the global population structure of T. pallidum, we assembled a geographically and temporally diverse collection of 726 genomes from 626 clinical and 100 laboratory samples collected in 23 countries. We applied phylogenetic analyses and clustering, and found that the global syphilis population comprises just two deeply branching lineages, Nichols and SS14. Both lineages are currently circulating in 12 of the 23 countries sampled. We subdivided T. p. pallidum into 17 distinct sublineages to provide further phylodynamic resolution. Importantly, two Nichols sublineages have expanded clonally across 9 countries contemporaneously with SS14. Moreover, pairwise genome analyses revealed examples of isolates collected within the last 20 years from 14 different countries that had genetically identical core genomes, which might indicate frequent exchange through international transmission. It is striking that most samples collected before 1983 are phylogenetically distinct from more recently isolated sublineages. Using Bayesian temporal analysis, we detected a population bottleneck occurring during the late 1990s, followed by rapid population expansion in the 2000s that was driven by the dominant T. pallidum sublineages circulating today. This expansion may be linked to changing epidemiology, immune evasion or fitness under antimicrobial selection pressure, since many of the contemporary syphilis lineages we have characterized are resistant to macrolides. Syphilis, which is caused by the sexually transmitted bacterium Treponema pallidum subsp. pallidum, has an estimated 6.3 million cases worldwide per annum. In the past ten years, the incidence of syphilis has increased by more than 150% in some high-income countries, but the evolution and epidemiology of the epidemic are poorly understood. To characterize the global population structure of T. pallidum, we assembled a geographically and temporally diverse collection of 726 genomes from 626 clinical and 100 laboratory samples collected in 23 countries. We applied phylogenetic analyses and clustering, and found that the global syphilis population comprises just two deeply branching lineages, Nichols and SS14. Both lineages are currently circulating in 12 of the 23 countries sampled. We subdivided T. p. pallidum into 17 distinct sublineages to provide further phylodynamic resolution. Importantly, two Nichols sublineages have expanded clonally across 9 countries contemporaneously with SS14. Moreover, pairwise genome analyses revealed examples of isolates collected within the last 20 years from 14 different countries that had genetically identical core genomes, which might indicate frequent exchange through international transmission. It is striking that most samples collected before 1983 are phylogenetically distinct from more recently isolated sublineages. Using Bayesian temporal analysis, we detected a population bottleneck occurring during the late 1990s, followed by rapid population expansion in the 2000s that was driven by the dominant T. pallidum sublineages circulating today. This expansion may be linked to changing epidemiology, immune evasion or fitness under antimicrobial selection pressure, since many of the contemporary syphilis lineages we have characterized are resistant to macrolides. Global syphilis prevalence has been increasing. Sequencing and analysis of a global collection of 726 Treponema pallidum samples reveal globally circulating lineages linked to a rapid expansion occurring since the end of the twentieth century. Syphilis, which is caused by the sexually transmitted bacterium Treponema pallidum subsp. pallidum , has an estimated 6.3 million cases worldwide per annum. In the past ten years, the incidence of syphilis has increased by more than 150% in some high-income countries, but the evolution and epidemiology of the epidemic are poorly understood. To characterize the global population structure of T. pallidum , we assembled a geographically and temporally diverse collection of 726 genomes from 626 clinical and 100 laboratory samples collected in 23 countries. We applied phylogenetic analyses and clustering, and found that the global syphilis population comprises just two deeply branching lineages, Nichols and SS14. Both lineages are currently circulating in 12 of the 23 countries sampled. We subdivided T. p. pallidum into 17 distinct sublineages to provide further phylodynamic resolution. Importantly, two Nichols sublineages have expanded clonally across 9 countries contemporaneously with SS14. Moreover, pairwise genome analyses revealed examples of isolates collected within the last 20 years from 14 different countries that had genetically identical core genomes, which might indicate frequent exchange through international transmission. It is striking that most samples collected before 1983 are phylogenetically distinct from more recently isolated sublineages. Using Bayesian temporal analysis, we detected a population bottleneck occurring during the late 1990s, followed by rapid population expansion in the 2000s that was driven by the dominant T. pallidum sublineages circulating today. This expansion may be linked to changing epidemiology, immune evasion or fitness under antimicrobial selection pressure, since many of the contemporary syphilis lineages we have characterized are resistant to macrolides. Global syphilis prevalence has been increasing. Sequencing and analysis of a global collection of 726 Treponema pallidum samples reveal globally circulating lineages linked to a rapid expansion occurring since the end of the twentieth century. Syphilis, which is caused by the sexually transmitted bacterium Treponema pallidum subsp. pallidum, has an estimated 6.3 million cases worldwide per annum. In the past ten years, the incidence of syphilis has increased by more than 150% in some high-income countries, but the evolution and epidemiology of the epidemic are poorly understood. To characterize the global population structure of T. pallidum, we assembled a geographically and temporally diverse collection of 726 genomes from 626 clinical and 100 laboratory samples collected in 23 countries. We applied phylogenetic analyses and clustering, and found that the global syphilis population comprises just two deeply branching lineages, Nichols and SS14. Both lineages are currently circulating in 12 of the 23 countries sampled. We subdivided T. p.pallidum into 17 distinct sublineages to provide further phylodynamic resolution. Importantly, two Nichols sublineages have expanded clonally across 9 countries contemporaneously with SS14. Moreover, pairwise genome analyses revealed examples of isolates collected within the last 20 years from 14 different countries that had genetically identical core genomes, which might indicate frequent exchange through international transmission. It is striking that most samples collected before 1983 are phylogenetically distinct from more recently isolated sublineages. Using Bayesian temporal analysis, we detected a population bottleneck occurring during the late 1990s, followed by rapid population expansion in the 2000s that was driven by the dominant T. pallidum sublineages circulating today. This expansion may be linked to changing epidemiology, immune evasion or fitness under antimicrobial selection pressure, since many of the contemporary syphilis lineages we have characterized are resistant to macrolides.Global syphilis prevalence has been increasing. Sequencing and analysis of a global collection of 726 Treponema pallidum samples reveal globally circulating lineages linked to a rapid expansion occurring since the end of the twentieth century. |
| Author | Kenyon, Chris R. Morshed, Muhammad G. Williamson, Deborah A. Obukhov, Andrey Balla, Eszter Lee, Min-Kuang Molini, Barbara J. Krajden, Mel Smit, Erasmus Cole, Michelle J. Sweeney, Emma L. Wennerås, Christine Ruis, Christopher Hughes, Gwenda Guiver, Malcolm Pitt, Rachel Whiley, David M. Kularatne, Ranmini Page, Emma E. Naidu, Prenilla Fifer, Helen Marks, Michael Khairullin, Rafil Taiaroa, George Beale, Mathew A. Rowley, Dominic Rietmeijer, Cornelis Unemo, Magnus Lukehart, Sheila A. Grankvist, Anna Shokoples, Sandy Thomson, Nicholas R. Crucitti, Tania Ewens, Michael Fernández-Naval, Candela Petrovay, Fruzsina Arando, Maider Vera, Jaime H. |
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Division, UK Health Security Agency – sequence: 6 givenname: Christopher orcidid: 0000-0003-0977-5534 surname: Ruis fullname: Ruis, Christopher organization: Molecular Immunity Unit, MRC-Laboratory of Molecular Biology, Department of Medicine, University of Cambridge, Department of Veterinary Medicine, University of Cambridge – sequence: 7 givenname: Eszter orcidid: 0000-0001-8519-9511 surname: Balla fullname: Balla, Eszter organization: Bacterial STIs Reference Laboratory, Department of Bacteriology, National Public Health Centre – sequence: 8 givenname: Tania surname: Crucitti fullname: Crucitti, Tania organization: Department of Clinical Sciences, Institute of Tropical Medicine – sequence: 9 givenname: Michael surname: Ewens fullname: Ewens, Michael organization: Brotherton Wing Clinic, Brotherton Wing, Leeds General Infirmary – sequence: 10 givenname: Candela orcidid: 0000-0002-5584-3537 surname: Fernández-Naval fullname: Fernández-Naval, Candela organization: Microbiology 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Maider surname: Arando fullname: Arando, Maider organization: STI Unit Vall d’Hebron-Drassanes, Infectious Diseases Department, Hospital Vall d’Hebron – sequence: 17 givenname: Barbara J. surname: Molini fullname: Molini, Barbara J. organization: Department of Medicine, University of Washington – sequence: 18 givenname: Andrey orcidid: 0000-0001-6320-9651 surname: Obukhov fullname: Obukhov, Andrey organization: Tuvan Republican Skin and Venereal Diseases Dispensary, Ministry of Health of Tuva Republic – sequence: 19 givenname: Emma E. surname: Page fullname: Page, Emma E. organization: Virology Department, Old Medical School, Leeds Teaching Hospitals Trust – sequence: 20 givenname: Fruzsina surname: Petrovay fullname: Petrovay, Fruzsina organization: Bacterial STIs Reference Laboratory, Department of Bacteriology, National Public Health Centre – sequence: 21 givenname: Cornelis surname: Rietmeijer fullname: Rietmeijer, Cornelis organization: Colorado School of Public Health, University 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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34819643$$D View this record in MEDLINE/PubMed https://urn.kb.se/resolve?urn=urn:nbn:se:oru:diva-95586$$DView record from Swedish Publication Index https://gup.ub.gu.se/publication/310867$$DView record from Swedish Publication Index |
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| DOI | 10.1038/s41564-021-01000-z |
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| Snippet | Syphilis, which is caused by the sexually transmitted bacterium
Treponema pallidum
subsp.
pallidum
, has an estimated 6.3 million cases worldwide per annum. In... Syphilis, which is caused by the sexually transmitted bacterium Treponema pallidum subsp. pallidum , has an estimated 6.3 million cases worldwide per annum. In... Syphilis, which is caused by the sexually transmitted bacterium Treponema pallidum subsp. pallidum, has an estimated 6.3 million cases worldwide per annum. In... |
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| Title | Global phylogeny of Treponema pallidum lineages reveals recent expansion and spread of contemporary syphilis |
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