Whole genome sequence of the Treponema pallidum subsp. endemicum strain Iraq B: A subpopulation of bejel treponemes contains full-length tprF and tprG genes similar to those present in T. p. subsp. pertenue strains

Mikalová, Lenka; Janečková, Klára; Nováková, Markéta; Strouhal, Michal; Čejková, Darina; Harper, Kristin N.; Šmajs, David

doi:10.1371/journal.pone.0230926

Cited by 9 publications

(12 citation statements)

References 54 publications

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“…Although the methods used to detect recombination are different from our workflow, most of the results previously reported were confirmed by our findings. For instance, recombination in tp0136, tp0326 , tp0462 , tp0488 , tp0548 , and tp0865 , has also been detected in other studies ( Gray et al 2006 ; Harper et al 2008 ; Pětrošová et al 2012 ; Čejková et al 2013 ; Staudová et al 2014 ; Arora et al 2016 ; Mikalová et al 2017 , 2020 ; Tong et al 2017 ; Kumar, Caimano, et al 2018 ; Marks et al 2018 ; Pospíšilová et al 2018 ; Schuenemann et al 2018 ; Strouhal et al 2018 ; Grillová et al 2019 ; Majander et al 2020 ) but we have identified additional genes ( tp0164, tp0179, tp0515, tp0558, tp0967 , and tp0968 ) not previously reported as recombinant, probably as a result of the systematic analysis of 75 genomes. On the contrary, loci tp0117/tp0131, tp0119, tp0317, tp0621, tp0856 , and tp0858 , and the spacers of rRNA operons, which were detected in previous studies ( Brinkman et al 2008 ; Kumar, Caimano, et al 2018 ; Marks et al 2018 ; Strouhal et al 2018 ; Grillová et al 2019 ) were not detected as recombinant in our analyses because of the large number of missing positions resulting from mapping of short reads with stringent conditions applied to paralogous/duplicated genes.…”

Section: Discussionsupporting

confidence: 70%

“…The study of recombination and natural selection in T. pallidum has been hindered by its low levels of genetic variability and lack of identification of molecular mechanisms for horizontal gene transfer ( Šmajs et al 2012 ), which has led researchers to refer to it as a clonal species ( Achtman 2008 ; Šmajs et al 2012 ). Nonetheless, several studies have pointed at the occurrence of recombination or exchange of genetic material in TPA ( Gray et al 2006 ; Harper et al 2008 ; Pětrošová et al 2012 ; Čejková et al 2013 ; Staudová et al 2014 ; Arora et al 2016 ; Tong et al 2017 ; Marks et al 2018 ; Pospíšilová et al 2018 ; Schuenemann et al 2018 ; Strouhal et al 2018 ; Majander et al 2020 ; Mikalová et al 2020 ) and the presence of natural selection acting in these bacteria ( Čejková et al 2012 ; Giacani, Brandt, et al 2012 ; Giacani, Chattopadhyay, et al 2012 ; Kumar, Caimano, et al 2018 ). For example, genes coding for TPA integral membrane proteins appear to be involved in genetic changes ( Staudová et al 2014 ; Arora et al 2016 ; Mikalová et al 2017 ), while also being subjected to human host selective pressures ( Kumar, Caimano, et al 2018 ).…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary Processes in the Emergence and Recent Spread of the Syphilis Agent,Treponema pallidum

Pla-Díaz

Sánchez-Busó

Giacani

et al. 2021

Molecular Biology and Evolution

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The incidence of syphilis has risen worldwide in the last decade in spite of being an easily treated infection. The causative agent of this sexually transmitted disease is the bacterium Treponema pallidum subspecies pallidum (TPA), very closely related to subsp. pertenue (TPE) and endemicum (TEN), responsible for the human treponematoses yaws and bejel, respectively. Although much focus has been placed on the question of the spatial and temporary origins of TPA, the processes driving the evolution and epidemiological spread of TPA since its divergence from TPE and TEN are not well understood. Here, we investigate the effects of recombination and selection as forces of genetic diversity and differentiation acting during the evolution of T. pallidum subspecies. Using a custom-tailored procedure, named phylogenetic incongruence method, with 75 complete genome sequences, we found strong evidence for recombination among the T. pallidum subspecies, involving 12 genes and 21 events. In most cases, only one recombination event per gene was detected and all but one event corresponded to intersubspecies transfers, from TPE/TEN to TPA. We found a clear signal of natural selection acting on the recombinant genes, which is more intense in their recombinant regions. The phylogenetic location of the recombination events detected and the functional role of the genes with signals of positive selection suggest that these evolutionary processes had a key role in the evolution and recent expansion of the syphilis bacteria and significant implications for the selection of vaccine candidates and the design of a broadly protective syphilis vaccine.

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Section: Discussionsupporting

confidence: 70%

Section: Introductionmentioning

confidence: 99%

Evolutionary Processes in the Emergence and Recent Spread of the Syphilis Agent,Treponema pallidum

Pla-Díaz

Sánchez-Busó

Giacani

et al. 2021

Molecular Biology and Evolution

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“…However, these changes are not visible in phylogenetic trees due to the differences in sequenced genome segments and omission of undetermined positions (N nucleotides) from the phylogenetic tree. This extent of genetic diversity is comparable to differences between TEN Bosnia and Iraq B with an average value of nucleotide diversity of 3.1, with 37 single-nucleotide differences, four indels, two differences in the number of tandem repetitions, and 18 differences in the length of homopolymeric regions were found in the Iraq B genome [12] compared to Bosnia A [37]. While TEN strain Iraq B was isolated in Iraq (the Middle East, southwestern Asia) in 1951, the strain Bosnia A was isolated in 1950 in Bosnia, southern Europe.…”

Section: Discussionmentioning

confidence: 80%

“…In the case of TEN, there are very few genomic analyses, and the two available whole genome sequences, differing in 37 single nucleotide variants, come from the reference strains Bosnia A [11] (CP007548) and Iraq B [12] (CP032303). In addition, nine recombinant loci have been detected in TEN isolates during typing studies [13].…”

Section: Introductionmentioning

confidence: 99%

Whole genome sequences of Treponema pallidum subsp. endemicum isolated from Cuban patients: the non-clonal character of isolates suggests a persistent human infection rather than a single outbreak

Vrbová

Noda

Grillová

et al. 2021

Preprint

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Bejel (endemic syphilis) is a neglected non-venereal disease caused by Treponema pallidum subsp. endemicum (TEN). Although it is mostly present in hot, dry climates, a few cases have been found outside of these areas. The aim of this work was the sequencing and analysis of TEN isolates obtained from "syphilis patients" in Cuba, which is not considered an endemic area for bejel. Genomes were obtained by pool segment genome sequencing or direct sequencing methods, and the bioinformatics analysis was performed according to an established pipeline. We obtained four genomes with 100%, 81.7%, 52.6%, and 21.1% of broad coverage, respectively. The sequenced genomes revealed a non-clonal character, with nucleotide variability ranging between 0.2–10.3 nucleotide substitutions per 100 kbp among the TEN isolates. Nucleotide changes affected 27 genes, and the analysis of the completely sequenced genome also showed a recombination event between tprC and tprI, in TP0488 as well as in the intergenic region between TP0127–TP0129. Despite limitations in the quality of samples affecting broad sequencing coverage, the determined non-clonal character of the isolates suggests a persistent infection in the Cuban population rather than a single outbreak caused by imported case.

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“…Samples were tested for the presence of treponemal DNA using an advanced nested PCR protocol (developed for TPA molecular typing) containing touchdown PCR and using PrimeS-TAR GXL polymerase (Takara, BioEurope, France) to increase detection power of nested PCR [18][19][20][21][22][23][24]. PCR was performed for four to six loci, including TP0136, TP0548, TP0705, 23S rRNA genes, TP0319 (tmpC), and TP0105 (polA) as described previously [17][18][19][20]25].…”

Section: Pcr Detectionmentioning

confidence: 99%

A retrospective study on nested PCR detection of syphilis treponemes in clinical samples: PCR detection contributes to the diagnosis of syphilis in patients with seronegative and serodiscrepant results

et al. 2020

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Syphilis, caused by Treponema pallidum ssp. pallidum (TPA), is a persisting global health problem. Although syphilis diagnostics relies mainly on serology, serological tests have some limitations, and it is recommended that the final diagnosis be supported by additional tests. The purpose of this study was to analyze the relationship between serology and PCR in syphilis diagnostics. From the year 2004 to May 2019, a total of 941 samples were taken from 833 patients suspected of having syphilis, in Czech Republic. In all these samples, both nested PCR detection of TPA and serology testing were performed. Of the 941 samples, 126 were seronegative, 651 were seropositive, and 164 were serodiscrepant. Among seronegative samples (n = 126), 11 were PCR-positive (8.7%). Among seropositive samples (n = 651; i.e., samples positive for both non-treponemal and treponemal serology tests), 368 samples were PCR-positive (56.5%). The remaining 164 serodiscrepant samples included RPR negative and treponemal serological test-positive samples (n = 154) and a set of 10 RPR-positive samples negative in treponemal serological tests. While the first group revealed 73 PCR-positive samples (47.4%), the second revealed 5 PCR positive samples (50.0%). PCR detection rates were highest in primary syphilis, with lower rates in the secondary and undetermined syphilis stages. As shown here, the nested PCR can improve diagnostics of syphilis, especially in seronegative patients and in patients with discrepant serology.

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Whole genome sequence of the Treponema pallidum subsp. endemicum strain Iraq B: A subpopulation of bejel treponemes contains full-length tprF and tprG genes similar to those present in T. p. subsp. pertenue strains

Cited by 9 publications

References 54 publications

Evolutionary Processes in the Emergence and Recent Spread of the Syphilis Agent,Treponema pallidum

Evolutionary Processes in the Emergence and Recent Spread of the Syphilis Agent,Treponema pallidum

Whole genome sequences of Treponema pallidum subsp. endemicum isolated from Cuban patients: the non-clonal character of isolates suggests a persistent human infection rather than a single outbreak

A retrospective study on nested PCR detection of syphilis treponemes in clinical samples: PCR detection contributes to the diagnosis of syphilis in patients with seronegative and serodiscrepant results

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