Strain diversity of Treponema pallidum subsp. pertenue suggests rare interspecies transmission in African nonhuman primates

Chuma, Idrissa S.; Roos, Christian; Atickem, Anagaw; Böhm, T.; Collins, Dave; Grillová, Linda; Hallmaier‐Wacker, Luisa K.; Kazwala, Rudovick; Keyyu, Julius D.; Lüert, Simone; Maloueki, Ulrich; Oppelt, Jan; Petrželková, Klára J.; Piel, A.; Stewart, Fiona; Šmajs, David; Knauf, Sascha

doi:10.1038/s41598-019-50779-9

Cited by 18 publications

(48 citation statements)

References 33 publications

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“…Notably, in all TPE strains sampled from this ecosystem, there is no indication that strains were epidemiologically linked, as no identical genomes were sampled. In contrast, in other species in different ecosystems, nearly identical genomes were observed, potentially indicative of an epidemiological link: particularly the two green monkey populations in Bijilo In agreement with a recent study of TPE strain diversity among NHPs from Tanzania using multi-locus sequence typing [52], simian derived isolates included in our analyses did not form monophyletic clades based on host species or the type of symptoms caused by an isolate, but rather clustered based on geography. Three geographical clades were prominent; the east African clade consisting of isolates from Tanzania and the two West African sister clades that formed well-supported monophyletic groups.…”

Section: Discussionsupporting

confidence: 89%

Geographically structured genomic diversity of non-human primate-infecting Treponema pallidum subsp. pertenue

Mubemba

Gogarten

Schuenemann

et al. 2019

Preprint

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BackgroundIncreasing evidence suggests many non-human primate (NHP) species in sub-Saharan Africa are infected with Treponema pallidum subsp. pertenue (TPE), the bacterium causing yaws in humans. In humans, yaws is characterized by lesions of the extremities and face, while Treponema pallidum subsp. pallidum (TPA) causes venereal syphilis and is characterized by primary lesions on the genital, anal or oral mucosae, and has not been detected in NHPs. Due to a paucity of genetic data, it remains unclear whether other Treponema pallidum (TP) subspecies found in humans also occur in NHP and how the genomic diversity of TPE lineages that do occur in NHPs is distributed across hosts and space. MethodologyWe observed a combination of yaws-and syphilis-like symptoms in sooty mangabeys (Cercocebus atys atys) in Taï National Park (TNP), Côte d'Ivoire and collected swabs and biopsies from symptomatic animals. We also collected NHP bones from eight species from TNP, as well as from 19 species at 12 field sites across sub-Saharan Africa. Samples were screened for TP DNA using PCRs. In-solution hybridization capture coupled with high throughput sequencing was used to sequence TP genomes from positive samples. Principal findingsWe generated four nearly complete TP genomes from biopsies and swabs and five partial genomes from bones. Phylogenomic analyses revealed that both syphilis-and yaws-like lesions of sooty mangabeys within a single social group in TNP were caused by TPE. All TPE genomes determined from these sooty mangabeys were different and exhibited divergence levels not observed in TPE from a single species at any other field site where the disease seems to be epizootic. In general, simian TPE isolates did not form monophyletic clades based on host species or the type of symptoms caused by an isolate, but rather clustered based on geography. ConclusionsThere is a large diversity of TPE strains infecting NHPs in TNP. Our observations within a single social group of sooty mangabeys do not support the epizootic spread of a single clone, but rather points towards frequent independent introductions of the bacterium, which can cause syphilis-and yaws-like lesions. On a larger scale, the geographic clustering of TPE genomes might be compatible with cross-species transmission of TPE within ecosystems or environmental exposure leading to acquisition of closely related strains. Author's summaryIndividuals in several populations of wild non-human primates (NHP) in sub-Saharan Africa are infected with Treponema pallidum subsp. pertenue (TPE), a pathogen causing yaws disease in humans. In humans, yaws is characterized by skin lesions of the extremities and face. In contrast, Treponema pallidum subsp. pallidum, which causes venereal syphilis in humans, has not been observed in NHPs. We describe a combination of yaws-and syphilislike symptoms in a sooty mangabey (Cercocebus atys atys) social group in Taï National Park (TNP), Côte d'Ivoire. We sampled lesioned animals and collected and tested NHP bones from field sites across sub-Saha...

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Section: Discussionsupporting

confidence: 89%

Geographically structured genomic diversity of non-human primate-infecting Treponema pallidum subsp. pertenue

Mubemba

Gogarten

Schuenemann

et al. 2019

Preprint

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“…This study links yaws-like pathology to the actual detection of TPE in a wild chimpanzee, providing evidence that at least part of the suggestive lesions often observed in wild great apes are caused by this pathogen. These data join a growing body of evidence demonstrating that many NHP species across sub-Saharan Africa are infected with TPE (1,9). This finding could potentially be problematic for the ongoing campaign to eradicate TPE globally by 2030 (13), although, clearly, data from TPE-infected humans in this region are needed to determine whether zoonotic transmission of this pathogen occurs.…”

Section: Discussionmentioning

confidence: 55%

“…The lesions observed in these images closely resembled those of the wild female from the Sangaredi region described in this article, including shrunken eyes, deformation of the face, absence of the nose, and hypertrophied and depigmented lips (in 1 case, the lips were completely missing; Figure 1, panels B, C). Molecular investigations of the pathogen(s) causing these infections is clearly warranted, perhaps through noninvasive screening of TPE in feces, bones, or primate-associated flies (9,12).…”

Section: The Studymentioning

confidence: 99%

See 1 more Smart Citation

Yaws Disease Caused by Treponema pallidum subspecies pertenue in Wild Chimpanzee, Guinea, 2019

Mubemba¹,

Chanove²,

Mätz‐Rensing³

et al. 2020

Emerg. Infect. Dis.

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“…pertenue , the Serengeti National Park and Fribourg‐Blanc strains were more basal to the human T. pallidum subspecies strains (Harper et al, ). In a survey of 85 individuals from six primate species, Chuma et al () analyzed two genes ( tp0548 and tp0448 ) and showed that strains, all classed as T. pallidum subsp. pertenue despite differing clinical phenotypes, appear to cluster based on geography rather than host species, which suggests that there has been transmission among primate species.…”

Section: Epidemiological and Genetic Researchmentioning

confidence: 99%

Advancing the understanding of treponemal disease in the past and present

Baker

Crane-Kramer

Dee

et al. 2020

American J Phys Anthropol

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Syphilis was perceived to be a new disease in Europe in the late 15th century, igniting a debate about its origin that continues today in anthropological, historical, and medical circles. We move beyond this age-old debate using an interdisciplinary approach that tackles broader questions to advance the understanding of treponemal infection (syphilis, yaws, bejel, and pinta). How did the causative organism(s) and humans co-evolve? How did the related diseases caused by Treponema pallidum emerge in different parts of the world and affect people across both time and space? How are T. pallidum subspecies related to the treponeme causing pinta? The current state of scholarship in specific areas is reviewed with recommendations made to stimulate future work. Understanding treponemal biology, genetic relationships, epidemiology, and clinical manifestations is crucial for vaccine development today and for investigating the distribution of infection in both modern and past populations.Paleopathologists must improve diagnostic criteria and use a standard approach for recording skeletal lesions on archaeological human remains. Adequate contextualization of cultural and environmental conditions is necessary, including site dating and justification for any corrections made for marine or freshwater reservoir effects. Biogeochemical analyses may assess aquatic contributions to diet, physiological changes arising from treponemal disease and its treatments (e.g., mercury), or residential mobility of those affected. Shifting the focus from point of origin to investigating who is affected (e.g., by age/sex or socioeconomic status) and disease distribution (e.g., coastal/ inland, rural/urban) will advance our understanding of the treponemal disease and its impact on people through time. K E Y W O R D S archaeological biogeochemistry,

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Strain diversity of Treponema pallidum subsp. pertenue suggests rare interspecies transmission in African nonhuman primates

Cited by 18 publications

References 33 publications

Geographically structured genomic diversity of non-human primate-infecting Treponema pallidum subsp. pertenue

Geographically structured genomic diversity of non-human primate-infecting Treponema pallidum subsp. pertenue

Yaws Disease Caused by Treponema pallidum subspecies pertenue in Wild Chimpanzee, Guinea, 2019

Advancing the understanding of treponemal disease in the past and present

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