Complete genome sequences of two strains of Treponema pallidum subsp. pertenue from Indonesia: Modular structure of several treponemal genes
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
30303967
PubMed Central
PMC6197692
DOI
10.1371/journal.pntd.0006867
PII: PNTD-D-18-00942
Knihovny.cz E-zdroje
- MeSH
- genom bakteriální * MeSH
- lidé MeSH
- pořadí genů MeSH
- rekombinace genetická MeSH
- repetitivní sekvence nukleových kyselin MeSH
- sekvenční analýza DNA * MeSH
- Treponema pallidum genetika MeSH
- výpočetní biologie MeSH
- vysoce účinné nukleotidové sekvenování MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Indonésie MeSH
BACKGROUND: Treponema pallidum subsp. pertenue (TPE) is the causative agent of yaws, a multistage disease endemic in tropical regions in Africa, Asia, Oceania, and South America. To date, seven TPE strains have been completely sequenced and analyzed including five TPE strains of human origin (CDC-2, CDC 2575, Gauthier, Ghana-051, and Samoa D) and two TPE strains isolated from the baboons (Fribourg-Blanc and LMNP-1). This study revealed the complete genome sequences of two TPE strains, Kampung Dalan K363 and Sei Geringging K403, isolated in 1990 from villages in the Pariaman region of Sumatra, Indonesia and compared these genome sequences with other known TPE genomes. METHODOLOGY/PRINCIPAL FINDINGS: The genomes were determined using the pooled segment genome sequencing method combined with the Illumina sequencing platform resulting in an average coverage depth of 1,021x and 644x for the TPE Kampung Dalan K363 and TPE Sei Geringging K403 genomes, respectively. Both Indonesian TPE strains were genetically related to each other and were more distantly related to other, previously characterized TPE strains. The modular character of several genes, including TP0136 and TP0858 gene orthologs, was identified by analysis of the corresponding sequences. To systematically detect genes potentially having a modular genetic structure, we performed a whole genome analysis-of-occurrence of direct or inverted repeats of 17 or more nucleotides in length. Besides in tpr genes, a frequent presence of repeats was found in the genetic regions spanning TP0126-TP0136, TP0856-TP0858, and TP0896 genes. CONCLUSIONS/SIGNIFICANCE: Comparisons of genome sequences of TPE Kampung Dalan K363 and Sei Geringging K403 with other TPE strains revealed a modular structure of several genomic loci including the TP0136, TP0856, and TP0858 genes. Diversification of TPE genomes appears to be facilitated by intra-strain genome recombination events.
CEITEC Central European Institute of Technology Masaryk University Brno Czech Republic
Department of Biology Faculty of Medicine Masaryk University Brno Czech Republic
Department of Immunology Veterinary Research Institute Brno Czech Republic
Izore Centrum Infectieziekten Friesland EN Leeuwarden the Netherlands
National Centre for Biomolecular Research Faculty of Science Masaryk University Brno Czech Republic
Zobrazit více v PubMed
Giacani L, Lukehart SA. The endemic treponematoses. Clin Microbiol Rev. 2014;27: 89–115. 10.1128/CMR.00070-13 PubMed DOI PMC
Grange PA, Mikalová L, Gaudin C, Strouhal M, Janier M, Benhaddou N, et al. Treponema pallidum 11qj subtype may correspond to a Treponema pallidum subsp. endemicum strain. Sex Transm Dis. 2016;43: 517–518. 10.1097/OLQ.0000000000000474 PubMed DOI
Mikalová L, Strouhal M, Oppelt J, Grange PA, Janier M, Benhaddou N, et al. Human Treponema pallidum 11q/j isolate belongs to subsp. endemicum but contains two loci with a sequence in TP0548 and TP0488 similar to subsp. pertenue and subsp. pallidum, respectively. PLoS Negl Trop Dis. 2017;11: e0005434 10.1371/journal.pntd.0005434 PubMed DOI PMC
Noda AA, Grillová L, Lienhard R, Blanco O, Rodríguez I, Šmajs D. Bejel in Cuba: molecular identification of Treponema pallidum subsp. endemicum in patients diagnosed with venereal syphilis. Clin Microbiol Infect. 2018. February 15 pii: S1198-743X(18)30154-X. 10.1016/j.cmi.2018.02.006 PubMed DOI
Edmondson DG, Hu B, Norris SJ. Long-term in vitro culture of the syphilis spirochete Treponema pallidum subsp. pallidum. MBio 2018;9: e01153–18. 10.1128/mBio.01153-18 PubMed DOI PMC
Čejková D, Zobaníková M, Chen L, Pospíšilová P, Strouhal M, Qin X, et al. Whole genome sequences of three Treponema pallidum ssp. pertenue strains: yaws and syphilis treponemes differ in less than 0.2% of the genome sequence. PLoS Negl Trop Dis. 2012;6: e1471 10.1371/journal.pntd.0001471 PubMed DOI PMC
Strouhal M, Mikalová L, Havlíčková P, Tenti P, Čejková D, Rychlík I, et al. Complete genome sequence of two strains of Treponema pallidum subsp. pertenue from Ghana, Africa: identical genome sequences in samples isolated more than 7 years apart. PLoS Negl Trop Dis. 2017;11: e0005894 10.1371/journal.pntd.0005894 PubMed DOI PMC
Zobaníková M, Strouhal M, Mikalová L, Čejková D, Ambrožová L, Pospíšilová P, et al. Whole genome sequence of the Treponema Fribourg-Blanc: unspecified simian isolate is highly similar to the yaws subspecies. PLoS Negl Trop Dis. 2013;7: e2172 10.1371/journal.pntd.0002172 PubMed DOI PMC
Knauf S, Gogarten J, Schuenemann VJ, De Nys HM, Duex A, Strouhal M, et al. African nonhuman primates are infected with the yaws bacterium Treponema pallidum subsp. pertenue; 2017. Preprint. Available from: bioRxiv. doi.org/10.1101/135491. PubMed PMC
Marks M, Fookes M, Wagner J, Butcher R, Ghinai R, Sokana O, et al. Diagnostics for yaws eradication: insights from direct next generation sequencing of cutaneous strains of Treponema pallidum. Clin Infect Dis. 2017. October 16 10.1093/cid/cix892 PubMed DOI PMC
Štaudová B, Strouhal M, Zobaníková M, Čejková D, Fulton LL, Chen L, et al. Whole genome sequence of the Treponema pallidum subsp. endemicum strain Bosnia A: the genome is related to yaws treponemes but contains few loci similar to syphilis treponemes. PLoS Negl Trop Dis. 2014;8: e3261 10.1371/journal.pntd.0003261 PubMed DOI PMC
Šmajs D, Norris SJ, Weinstock GM. Genetic diversity in Treponema pallidum: implications for pathogenesis, evolution and molecular diagnostics of syphilis and yaws. Infect Genet Evol. 2012;12: 191–202. 10.1016/j.meegid.2011.12.001 PubMed DOI PMC
Šmajs D, Strouhal M, Knauf S. Genetics of human and animal uncultivable treponemal pathogens. Infect Genet Evol. 2018; 61:92–107. 10.1016/j.meegid.2018.03.015 PubMed DOI
Noordhoek GT, Engelkens HJ, Judanarso J, van der Stek J, Aelbers GN, van der Sluis JJ, et al. Yaws in West Sumatra, Indonesia: clinical manifestations, serological findings and characterisation of new Treponema isolates by DNA probes. Eur J Clin Microbiol Infect Dis. 1991;10: 12–19. PubMed
Weinstock GM, Šmajs D, Hardham J, Norris SJ. From microbial genome sequence to applications. Res Microbiol. 2000;151: 151–158. PubMed
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC
Mikalová L, Strouhal M, Čejková D, Zobaníková M, Pospíšilová P, Norris SJ, et al. Genome analysis of Treponema pallidum subsp. pallidum and subsp. pertenue strains: most of the genetic differences are localized in six regions. PLoS One. 2010;5: e15713 10.1371/journal.pone.0015713 PubMed DOI PMC
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28: 1647–1649. 10.1093/bioinformatics/bts199 PubMed DOI PMC
Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10: 512–526. 10.1093/oxfordjournals.molbev.a040023 PubMed DOI
Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33: 1870–1874. 10.1093/molbev/msw054 PubMed DOI PMC
Pětrošová H, Pospíšilová P, Strouhal M, Čejková D, Zobaníková M, Mikalová L, et al. Resequencing of Treponema pallidum ssp. pallidum strains Nichols and SS14: correction of sequencing errors resulted in increased separation of syphilis treponeme subclusters. PLoS One. 2013;8: e74319 10.1371/journal.pone.0074319 PubMed DOI PMC
Zobaníková M, Mikolka P, Čejková D, Pospíšilová P, Chen L, Strouhal M, et al. Complete genome sequence of Treponema pallidum strain DAL-1. Stand Genomic Sci. 2012;7: 12–21. 10.4056/sigs.2615838 PubMed DOI PMC
Pětrošová H, Zobaníková M, Čejková D, Mikalová L, Pospíšilová P, Strouhal M, et al. Whole genome sequence of Treponema pallidum ssp. pallidum, strain Mexico A, suggests recombination between yaws and syphilis strains. PLoS Negl Trop Dis. 2012;6: e1832 10.1371/journal.pntd.0001832 PubMed DOI PMC
Giacani L, Jeffrey BM, Molini BJ, Le HT, Lukehart SA, Centurion-Lara A, et al. Complete genome sequence and annotation of the Treponema pallidum subsp. pallidum Chicago strain. J Bacteriol. 2010;192: 2645–2646. 10.1128/JB.00159-10 PubMed DOI PMC
Giacani L, Iverson-Cabral SL, King JC, Molini BJ, Lukehart SA, Centurion-Lara A. Complete genome sequence of the Treponema pallidum subsp. pallidum Sea81-4 strain. Genome Announc. 2014;2: e00333–14. 10.1128/genomeA.00333-14 PubMed DOI PMC
Šmajs D, Zobaníková M, Strouhal M, Čejková D, Dugan-Rocha S, Pospíšilová P, et al. Complete genome sequence of Treponema paraluiscuniculi, strain Cuniculi A: the loss of infectivity to humans is associated with genome decay. PLoS One. 2011;6: e20415 10.1371/journal.pone.0020415 PubMed DOI PMC
Marcais G, Kingsford C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics. 2011;27: 764–770. 10.1093/bioinformatics/btr011 PubMed DOI PMC
Rice P, Longden I, Bleasby A. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 2000;16: 276–277. PubMed
Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26: 841–842. 10.1093/bioinformatics/btq033 PubMed DOI PMC
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: 2017. Available from: https://www.R-project.org/
Harper KN, Liu H, Ocampo PS, Steiner BM, Martin A, Levert K, et al. The sequence of the acidic repeat protein (arp) gene differentiates venereal from nonvenereal Treponema pallidum subspecies, and the gene has evolved under strong positive selection in the subspecies that causes syphilis. FEMS Immunol Med Microbiol. 2008;53: 322–332. 10.1111/j.1574-695X.2008.00427.x PubMed DOI
Čejková D, Zobaníková M, Pospíšilová P, Strouhal M, Mikalová L, Weinstock GM, et al. Structure of rrn operons in pathogenic non-cultivable treponemes: sequence but not genomic position of intergenic spacers correlates with classification of Treponema pallidum and T. paraluiscuniculi strains. J Med Microbiol. 2013;62: 196–207. 10.1099/jmm.0.050658-0 PubMed DOI PMC
Centurion-Lara A, Giacani L, Godornes C, Molini BJ, Brinck Reid T, Lukehart SA. Fine analysis of genetic diversity of the tpr gene family among treponemal species, subspecies and strains. PLoS Negl Trop Dis. 2013;7: e2222 10.1371/journal.pntd.0002222 PubMed DOI PMC
Centurion-Lara A, LaFond RE, Hevner K, Godornes C, Molini BJ, Van Voorhis WC, et al. Gene conversion: a mechanism for generation of heterogeneity in the tprK gene of Treponema pallidum during infection. Mol Microbiol. 2004;52: 1579–1596. 10.1111/j.1365-2958.2004.04086.x PubMed DOI
LaFond RE, Centurion-Lara A, Godornes C, Rompalo AM, Van Voorhis WC, Lukehart SA. Sequence diversity of Treponema pallidum subsp. pallidum tprK in human syphilis lesions and rabbit-propagated isolates. J Bacteriol. 2003;185: 6262–6268. 10.1128/JB.185.21.6262-6268.2003 PubMed DOI PMC
LaFond RE, Centurion-Lara A, Godornes C, Van Voorhis WC, Lukehart SA. TprK sequence diversity accumulates during infection of rabbits with Treponema pallidum subsp. pallidum Nichols strain. Infect Immun. 2006;74: 1896–1906. 10.1128/IAI.74.3.1896-1906.2006 PubMed DOI PMC
Heymans R, Kolader ME, van der Helm JJ, Coutinho RA, Bruisten SM. TprK gene regions are not suitable for epidemiological syphilis typing. Eur J Clin Microbiol Infect Dis. 2009;28: 875–878. 10.1007/s10096-009-0717-5 PubMed DOI
Čejková D, Strouhal M, Norris SJ, Weinstock GM, Šmajs D. A retrospective study on genetic heterogeneity within Treponema strains: subpopulations are genetically distinct in a limited number of positions. PLoS Negl Trop Dis. 2015;9: e0004110 10.1371/journal.pntd.0004110 PubMed DOI PMC
Giacani L, Lukehart S, Centurion-Lara A. Length of guanosine homopolymeric repeats modulates promoter activity of subfamily II tpr genes of Treponema pallidum ssp. pallidum. FEMS Immunol Med Microbiol. 2007;51: 289–301. 10.1111/j.1574-695X.2007.00303.x PubMed DOI PMC
Pinto M, Borges V, Antelo M, Pinheiro M, Nunes A, Azevedo J, et al. Genome-scale analysis of the non-cultivable Treponema pallidum reveals extensive within-patient genetic variation. Nat Microbiol. 2016;2: 16190 10.1038/nmicrobiol.2016.190 PubMed DOI
Radolf JD, Kumar S. The Treponema pallidum outer membrane. Curr Top Microbiol Immunol. 2018;415: 1–38. 10.1007/82_2017_44 PubMed DOI PMC
Yang J, Zhang Y. I-TASSER server: new development for protein structure and function predictions. Nucleic Acids Res. 2015;43: W174–W181. 10.1093/nar/gkv342 PubMed DOI PMC
Naqvi AA, Shahbaaz M, Ahmad F, Hassan MI. Identification of functional candidates amongst hypothetical proteins of Treponema pallidum ssp. pallidum. PLoS One. 2015;10: e0124177 10.1371/journal.pone.0124177 PubMed DOI PMC
Turner TB, Hollander DH. Biology of the treponematoses based on studies carried out at the International Treponematosis Laboratory Center of the Johns Hopkins University under the auspices of the World Health Organization. Monogr Ser World Health Organ. 1957;35: 3–266. PubMed
Chi KH, Danavall D, Taleo F, Pillay A, Ye T, Nachamkin E, et al. Molecular differentiation of Treponema pallidum subspecies in skin ulceration clinically suspected as yaws in Vanuatu using real-time multiplex PCR and serological methods. Am J Trop Med Hyg. 2015;92: 134–138. 10.4269/ajtmh.14-0459 PubMed DOI PMC
Mikalová L, Šmajs D. Low-dose versus standard-dose azithromycin for treatment of yaws. Lancet Glob Health. 2018; 4: e357–e358. 10.1016/S2214-109X(18)30067-6 PubMed DOI
Gray RR, Mulligan CJ, Molini BJ, Sun ES, Giacani L, Godornes C, et al. Molecular evolution of the tprC, D, I, K, G, and J genes in the pathogenic genus Treponema. Mol Biol Evol. 2006;23: 2220–2233. 10.1093/molbev/msl092 PubMed DOI
Godornes C, Giacani L, Barry AE, Mitja O, Lukehart SA. Development of a Multilocus Sequence Typing (MLST) scheme for Treponema pallidum subsp. pertenue: application to yaws in Lihir Island, Papua New Guinea. PLoS Negl Trop Dis. 2017;11: e60006113 10.1371/journal.pntd.0006113 PubMed DOI PMC
Pillay A, Liu H, Chen CY, Holloway B, Sturm AW, Steiner B, et al. Molecular subtyping of Treponema pallidum subspecies pallidum. Sex Transm Dis. 1998;25: 408–414. PubMed
Flasarová M, Šmajs D, Matějková P, Woznicová V, Heroldová-Dvoráková M, Votava M. Molecular detection and subtyping of Treponema pallidum subsp. pallidum in clinical specimens. Epidemiol Mikrobiol Imunol. 2006;55: 105–111. PubMed
Woznicová V, Šmajs D, Wechsler D, Matějková P, Flasarová M. Detection of Treponema pallidum subsp. pallidum from skin lesions, serum, and cerebrospinal fluid in an infant with congenital syphilis after clindamycin treatment of the mother during pregnancy. J Clin Microbiol. 2007;45: 659–661. 10.1128/JCM.02209-06 PubMed DOI PMC
Flasarová M, Pospíšilová P, Mikalová L, Vališová Z, Dastychová E, Strnadel R, et al. Sequencing-based molecular typing of Treponema pallidum strains in the Czech Republic: all identified genotypes are related to the sequence of the SS14 strain. Acta Derm Venereol. 2012;92: 669–674. 10.2340/00015555-1335 PubMed DOI
Grillová L, Pĕtrošová H, Mikalová L, Strnadel R, Dastychová E, Kuklová I, et al. Molecular typing of Treponema pallidum in the Czech Republic during 2011 to 2013: increased prevalence of identified genotypes and of isolates with macrolide resistance. J Clin Microbiol. 2014;52: 3693–3700. 10.1128/JCM.01292-14 PubMed DOI PMC
Mikalová L, Grillová L, Osbak K, Strouhal M, Kenyon C, Crucitti T, et al. Molecular typing of syphilis-causing strains among human immunodeficiency virus-positive patients in Antwerp, Belgium. Sex Transm Dis. 2017;44: 376–379. 10.1097/OLQ.0000000000000600 PubMed DOI
Gallo Vaulet L, Grillová L, Mikalová L, Casco R, Rodríguez Fermepin M, Pando MA, et al. Molecular typing of Treponema pallidum isolates from Buenos Aires, Argentina: frequent Nichols-like isolates and low levels of macrolide resistance. PLoS One. 2017;12: e0172905 10.1371/journal.pone.0172905 PubMed DOI PMC
Brinkman MB, McGill MA, Pettersson J, Rogers A, Matějková P, Šmajs D, et al. A novel Treponema pallidum antigen, TP0136, is an outer membrane protein that binds human fibronectin. Infect Immun. 2008;76: 1848–1857. 10.1128/IAI.01424-07 PubMed DOI PMC
Ke W, Molini BJ, Lukehart SA, Giacani L. Treponema pallidum subsp. pallidum TP0136 protein is heterogeneous among isolates and binds cellular and plasma fibronectin via its NH2-terminal end. PLoS Negl Trop Dis. 2015;9: e0003662 10.1371/journal.pntd.0003662 PubMed DOI PMC
Giacani L, Brandt SL, Puray-Chavez M, Brinck Reid T, Godornes C, Molini BJ, et al. Comparative investigation of the genomic regions involved in antigenic variation of the TprK antigen among treponemal species, subspecies, and strains. J Bacteriol. 2012;194: 4208–4225. 10.1128/JB.00863-12 PubMed DOI PMC
Anand A, Luthra A, Dunham-Ems S, Caimano MJ, Karanian C, LeDoyt M, et al. TprC/D (Tp0117/131), a trimeric, pore-forming rare outer membrane protein of Treponema pallidum, has a bipartite domain structure. J Bacteriol. 2012;194: 2321–2333. 10.1128/JB.00101-12 PubMed DOI PMC
Anand A, LeDoyt M, Karanian C, Luthra A, Koszelak-Rosenblum M, Malkowski MG, et al. Bipartite topology of Treponema pallidum repeat proteins C/D and I: outer membrane insertion, trimerization, and porin function require a C-terminal β-barrel domain. J Biol Chem. 2015;290: 12313–12331. 10.1074/jbc.M114.629188 PubMed DOI PMC
The hare syphilis agent is related to, but distinct from, the treponeme causing rabbit syphilis
Evolutionary Processes in the Emergence and Recent Spread of the Syphilis Agent, Treponema pallidum