High prevalence and genetic diversity of Treponema paraluisleporidarum isolates in European lagomorphs
ABSTRACT The bacterium Treponema paraluisleporidarum causes syphilis in lagomorphs. In a set of 1,095 samples from four species—European brown hare, mountain hare, Corsican hare, and European rabbit—we tested for infection and genotyped the strains that infect wild lagomorphs. Samples originate from...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-01-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01774-23 |
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| author | Sascha Knauf Linda Hisgen Erik O. Ågren Alexander M. Barlow Marcus Faehndrich Ulrich Voigt Luisa Fischer Linda Grillová Luisa K. Hallmaier-Wacker Marja J. L. Kik Jana C. Klink Jitka Křenová Antonio Lavazza Simone Lüert Markéta Nováková Darina Čejková Carlo Pacioni Tiziana Trogu David Šmajs Christian Roos |
| author_facet | Sascha Knauf Linda Hisgen Erik O. Ågren Alexander M. Barlow Marcus Faehndrich Ulrich Voigt Luisa Fischer Linda Grillová Luisa K. Hallmaier-Wacker Marja J. L. Kik Jana C. Klink Jitka Křenová Antonio Lavazza Simone Lüert Markéta Nováková Darina Čejková Carlo Pacioni Tiziana Trogu David Šmajs Christian Roos |
| author_sort | Sascha Knauf |
| collection | DOAJ |
| description | ABSTRACT The bacterium Treponema paraluisleporidarum causes syphilis in lagomorphs. In a set of 1,095 samples from four species—European brown hare, mountain hare, Corsican hare, and European rabbit—we tested for infection and genotyped the strains that infect wild lagomorphs. Samples originate from Sweden, the Netherlands, the United Kingdom, Germany, the Czech Republic, and Italy. The phylogenetic analyses of two informative gene targets (tp0488 and tp0548) showed high genetic diversity among the lagomorph-infecting treponemes. More specifically, we found a high number of nucleotide variants and various short repeat units in the tp0548 locus that have not been described for human syphilis and primate yaws causing Treponema pallidum. While the functional aspect of these short repeat units remains subject to ongoing investigations, it likely enables the pathogen to better survive in its lagomorph host. Our data did not support any geographic clustering, which is equally reflected in the host population genetics as shown by mitochondrial genome data corresponding to the sampled lagomorph populations. This is unexpected and in contrast with what has been shown for nonhuman primate infection with T. pallidum. In the future, the combination of multi-locus sequence typing and whole genome data from modern and ancient samples from a wide geographic range and multiple lagomorph species will contribute to a better understanding of the epidemiology and evolutionary path of lagomorph-infecting treponemes. In conclusion, our current study demonstrates widespread infection and a high genetic variation of the syphilis-causing pathogen in a higher number of positively PCR-tested European lagomorphs (n = 302/1,095). IMPORTANCE Syphilis is an ancient disease of humans and lagomorphs caused by two distinct but genetically closely related bacteria (>98% sequence identity based on the whole genome) of the genus Treponema. While human syphilis is well studied, little is known about the disease in the lagomorph host. Yet, comparative studies are needed to understand mechanisms in host–pathogen coevolution in treponematoses. Importantly, Treponema paraluisleporidarum–infected hare populations provide ample opportunity to study the syphilis-causing pathogen in a naturally infected model population without antibiotic treatment, data that cannot be obtained from syphilis infection in humans. We provide data on genetic diversity and are able to highlight various types of repetitions in one of the two hypervariable regions at the tp0548 locus that have not been described in the human syphilis-causing sister bacterium Treponema pallidum subsp. pallidum. |
| first_indexed | 2024-03-08T14:43:41Z |
| format | Article |
| id | doaj.art-30adc775f9044ad9a1e3360071fd24be |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-08T14:43:41Z |
| publishDate | 2024-01-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-30adc775f9044ad9a1e3360071fd24be2024-01-11T14:04:37ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-01-0112110.1128/spectrum.01774-23High prevalence and genetic diversity of Treponema paraluisleporidarum isolates in European lagomorphsSascha Knauf0Linda Hisgen1Erik O. Ågren2Alexander M. Barlow3Marcus Faehndrich4Ulrich Voigt5Luisa Fischer6Linda Grillová7Luisa K. Hallmaier-Wacker8Marja J. L. Kik9Jana C. Klink10Jitka Křenová11Antonio Lavazza12Simone Lüert13Markéta Nováková14Darina Čejková15Carlo Pacioni16Tiziana Trogu17David Šmajs18Christian Roos19Institute of International Animal Health/One Health, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , Greifswald, GermanyInstitute of International Animal Health/One Health, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , Greifswald, GermanyDepartment of Pathology and Wildlife Diseases, National Veterinary Institute , Uppsala, SwedenWildlife Network for Disease Surveillance, Bristol Veterinary School , Langford, Somerset, United KingdomInstitute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hanover, Foundation , Hanover, GermanyInstitute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hanover, Foundation , Hanover, GermanyWildlife Research Institute, State Agency for Nature, Environment and Consumer Protection North Rhine-Westphalia , Bonn, GermanyDepartment of Biology, Masaryk University , Brno, CzechiaInfection Biology Unit, Deutsches Primatenzentrum GmbH, Leibniz Institute for Primate Research , Göttingen, GermanyPathology Division, Department of Biomedical Health Sciences, Veterinary Medicine, Utrecht University , Utrecht, the NetherlandsInstitute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hanover, Foundation , Hanover, GermanyDepartment of Biology, Masaryk University , Brno, CzechiaDepartment of Animal Health and Welfare – Virology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna , Brescia, ItalyInstitute of International Animal Health/One Health, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , Greifswald, GermanyDepartment of Biology, Masaryk University , Brno, CzechiaDepartment of Biomedical Engineering, Brno University of Technology , Brno, CzechiaDepartment of Environment, Land, Water and Planning, Arthur Rylah Institute for Environmental Research , Heidelberg, Victoria, AustraliaDepartment of Animal Health and Welfare – Virology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna , Brescia, ItalyDepartment of Biology, Masaryk University , Brno, CzechiaPrimate Genetics Laboratory, Deutsches Primatenzentrum GmbH, Leibniz Institute for Primate Research , Göttingen, GermanyABSTRACT The bacterium Treponema paraluisleporidarum causes syphilis in lagomorphs. In a set of 1,095 samples from four species—European brown hare, mountain hare, Corsican hare, and European rabbit—we tested for infection and genotyped the strains that infect wild lagomorphs. Samples originate from Sweden, the Netherlands, the United Kingdom, Germany, the Czech Republic, and Italy. The phylogenetic analyses of two informative gene targets (tp0488 and tp0548) showed high genetic diversity among the lagomorph-infecting treponemes. More specifically, we found a high number of nucleotide variants and various short repeat units in the tp0548 locus that have not been described for human syphilis and primate yaws causing Treponema pallidum. While the functional aspect of these short repeat units remains subject to ongoing investigations, it likely enables the pathogen to better survive in its lagomorph host. Our data did not support any geographic clustering, which is equally reflected in the host population genetics as shown by mitochondrial genome data corresponding to the sampled lagomorph populations. This is unexpected and in contrast with what has been shown for nonhuman primate infection with T. pallidum. In the future, the combination of multi-locus sequence typing and whole genome data from modern and ancient samples from a wide geographic range and multiple lagomorph species will contribute to a better understanding of the epidemiology and evolutionary path of lagomorph-infecting treponemes. In conclusion, our current study demonstrates widespread infection and a high genetic variation of the syphilis-causing pathogen in a higher number of positively PCR-tested European lagomorphs (n = 302/1,095). IMPORTANCE Syphilis is an ancient disease of humans and lagomorphs caused by two distinct but genetically closely related bacteria (>98% sequence identity based on the whole genome) of the genus Treponema. While human syphilis is well studied, little is known about the disease in the lagomorph host. Yet, comparative studies are needed to understand mechanisms in host–pathogen coevolution in treponematoses. Importantly, Treponema paraluisleporidarum–infected hare populations provide ample opportunity to study the syphilis-causing pathogen in a naturally infected model population without antibiotic treatment, data that cannot be obtained from syphilis infection in humans. We provide data on genetic diversity and are able to highlight various types of repetitions in one of the two hypervariable regions at the tp0548 locus that have not been described in the human syphilis-causing sister bacterium Treponema pallidum subsp. pallidum.https://journals.asm.org/doi/10.1128/spectrum.01774-23spirochetesEuropean brown hareLepusrabbitOryctolagussyphilis |
| spellingShingle | Sascha Knauf Linda Hisgen Erik O. Ågren Alexander M. Barlow Marcus Faehndrich Ulrich Voigt Luisa Fischer Linda Grillová Luisa K. Hallmaier-Wacker Marja J. L. Kik Jana C. Klink Jitka Křenová Antonio Lavazza Simone Lüert Markéta Nováková Darina Čejková Carlo Pacioni Tiziana Trogu David Šmajs Christian Roos High prevalence and genetic diversity of Treponema paraluisleporidarum isolates in European lagomorphs Microbiology Spectrum spirochetes European brown hare Lepus rabbit Oryctolagus syphilis |
| title | High prevalence and genetic diversity of Treponema paraluisleporidarum isolates in European lagomorphs |
| title_full | High prevalence and genetic diversity of Treponema paraluisleporidarum isolates in European lagomorphs |
| title_fullStr | High prevalence and genetic diversity of Treponema paraluisleporidarum isolates in European lagomorphs |
| title_full_unstemmed | High prevalence and genetic diversity of Treponema paraluisleporidarum isolates in European lagomorphs |
| title_short | High prevalence and genetic diversity of Treponema paraluisleporidarum isolates in European lagomorphs |
| title_sort | high prevalence and genetic diversity of treponema paraluisleporidarum isolates in european lagomorphs |
| topic | spirochetes European brown hare Lepus rabbit Oryctolagus syphilis |
| url | https://journals.asm.org/doi/10.1128/spectrum.01774-23 |
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