1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 71, Issue 7

Characterization of a novel transitional group species ( sp. nov.) from the western black-legged tick, No Access

A corrigendum to this paper has been published here.

Abstract

A previously unrecognized species was isolated in 1976 from a pool of ticks collected in 1967 from Tillamook County, Oregon, USA. The isolate produced low fever and mild scrotal oedema following intraperitoneal injection into male guinea pigs (). Subsequent serotyping characterized this isolate as distinct from recognized typhus and spotted fever group species; nonetheless, the isolate remained unevaluated by molecular techniques and was not identified to species level for the subsequent 30 years. is the most frequently identified human-biting tick in the western United States, and as such, formal identification and characterization of this potentially pathogenic species is warranted. Whole-genome sequencing of the Tillamook isolate revealed a genome 1.43 Mbp in size with 32.4 mol% G+C content. Maximum-likelihood phylogeny of core proteins places it in the transitional group of basal to both and . It is distinct from existing named species, with maximum average nucleotide identity of 95.1% to and maximum digital DNA–DNA hybridization score similarity to at 80.1%. The closest similarity at the 16S rRNA gene (97.9%) and 4 (97.5%/97.6% respectively) is to ‘Rickettsia senegalensis’ and sp. cf9, both isolated from cat fleas (). We characterized growth at various temperatures and in multiple cell lines. The Tillamook isolate grows aerobically in Vero E6, RF/6A and DH82 cells, and growth is rapid at 28 °C and 32 °C. Using accepted genomic criteria, we propose the name sp. nov., with the type strain Tillamook 23. Strain Tillamook 23 is available from the Centers for Disease Control and Prevention Rickettsial Isolate Reference Collection (WDCM 1093), Atlanta, GA, USA (CRIRC accession number RTI001) and the Collection de Souches de l’Unité des Rickettsies (WDCM 875), Marseille, France (CSUR accession number R5043). Using accepted genomic criteria, we propose the name sp. nov., with the type strain Tillamook 23 (=CRIRC RTI001=R5043).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Ixodes pacificus , Rickettsia and Rickettsia tillamookensis
Funding
This study was supported by the:
  • National Institutes of Health (Award 1R01AI136035)
    • Principle Award Recipient: DavidGauthier
© Microbiology Society

Erratum

An erratum has been published for this content:
Corrigendum: Characterization of a novel transitional group species ( sp. nov.) from the western black-legged tick,
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004880
2021-07-02
2024-04-26
Loading full text...

Full text loading...

References

  1. Hughes LE, Clifford CM, Gresbrink R, Thomas LA, Keirans JE. Isolation of a spotted fever group Rickettsia from the Pacific Coast tick, Ixodes pacificus, in Oregon. Am J Trop Med Hyg 1976; 25:513–516 [View Article] [PubMed]
     [Google Scholar]
  2. Philip RN, Casper EA, Burgdorfer W, Gerloff RK, Hughes LE et al. Serologic typing of rickettsiae of the spotted fever group by microimmunofluorescence. J Immunol 1978; 121:1961–1968 [PubMed]
     [Google Scholar]
  3. Philip RN, Lane RS, Casper EA. Serotypes of tick-borne spotted fever group rickettsiae from western California. Am J Trop Med Hyg 1981; 30:722–727 [View Article] [PubMed]
     [Google Scholar]
  4. Lane R, Philip R, Casper E. Ecology of tick-borne agents in California. II. Further observations on rickettsiae. Burgdorfer W, Anacker R. eds In Rickettsiae and Rickettsial Diseases New York, NY: Academic Press; 1981
     [Google Scholar]
  5. Phan JN, CR L, Bender WG, Smoak III RM, Zhong J. Molecular detection and identification of Rickettsia species in Ixodes pacificus in California. Vector-Borne and Zoonotic Diseases 2011; 11:957–961
     [Google Scholar]
  6. Cheng D, Vigil K, Schanes P, Brown RN, Zhong J. Prevalence and burden of two rickettsial phylotypes (G021 and G022) in Ixodes pacificus from California by real-time quantitative PCR. Ticks and Tick-borne Diseases 2013; 4:280–287 [View Article]
     [Google Scholar]
  7. Alowaysi M, Chen J, Stark S, Teague K, LaCourse M et al. Isolation and characterization of a Rickettsia from the ovary of a western black-legged tick, Ixodes pacificus. Ticks and Tick-borne Diseases 2019; 10:918–923 [View Article]
     [Google Scholar]
  8. Diop A, El Karkouri K, Raoult D, Fournier PE. Genome sequence-based criteria for demarcation and definition of species in the genus Rickettsia. Int J Syst Evol Microbiol 2020; 70:1738–1750 [View Article] [PubMed]
     [Google Scholar]
  9. Furman DP, Loomis EC. The Ticks of California (Acari: Ixodida) Univ of California Press; 1984
     [Google Scholar]
  10. Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 2019; 37:540–546 [View Article] [PubMed]
     [Google Scholar]
  11. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
     [Google Scholar]
  12. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article] [PubMed]
     [Google Scholar]
  13. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011; 27:2987–2993 [View Article] [PubMed]
     [Google Scholar]
  14. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES et al. Integrative genomics viewer. Nat Biotechnol 2011; 29:24–26 [View Article] [PubMed]
     [Google Scholar]
  15. Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2013; 14:178–192 [View Article] [PubMed]
     [Google Scholar]
  16. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
     [Google Scholar]
  17. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
     [Google Scholar]
  18. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PloS one 2014; 9:e112963 [View Article]
     [Google Scholar]
  19. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  20. Seppey M, Manni M, Zdobnov EM. BUSCO: Assessing Genome Assembly and Annotation Completeness Gene Prediction: Springer; 2019 pp 227–245
     [Google Scholar]
  21. Ogata H, Audic S, Barbe V, Artiguenave F, Fournier PE et al. Selfish DNA in protein-coding genes of Rickettsia. Science 2000; 290:347–350 [View Article] [PubMed]
     [Google Scholar]
  22. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article]
     [Google Scholar]
  23. Mediannikov O, Aubadie-Ladrix M, Raoult D. Candidatus “Rickettsia senegalensis” in cat fleas in Senegal. New Microbes New Infect 2014; 3:24–28 [View Article] [PubMed]
     [Google Scholar]
  24. Lee I, Kim YO, Park SC, Chun J. Orthoani: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103
     [Google Scholar]
  25. Lechner M, Findeiß S, Steiner L, Marz M, Stadler PF et al. Proteinortho: detection of (co-) orthologs in large-scale analysis. BMC Bioinformatics 2011; 12:1–9
     [Google Scholar]
  26. Guindon S, Delsuc F, Dufayard JF, Gascuel O. Estimating Maximum Likelihood Phylogenies with PhyML Springer: Bioinformatics for DNA sequence analysis; 2009 pp 113–137
     [Google Scholar]
  27. Rambaut A. Figtree, a graphical viewer of phylogenetic trees [Internet]; 2014 http://treebioedacuk/software/figtree
  28. Gillespie JJ, Williams K, Shukla M, Snyder EE, Nordberg EK et al. Rickettsia phylogenomics: unwinding the intricacies of obligate intracellular life. PloS one 2008; 3:e2018 [View Article] [PubMed]
     [Google Scholar]
  29. Huebner RJ, Jellison WL, Pomerantz C. Rickettsialpox, a newly recognized rickettsial disease; isolation of a Rickettsia apparently identical with the causative agent of rickettsialpox from Allodermanyssus sanguineus, a rodent mite. Public Health Rep 1946; 61:1677–1682 [PubMed]
     [Google Scholar]
  30. Ogata H, Renesto P, Audic S, Robert C, Blanc G et al. The genome sequence of Rickettsia felis identifies the first putative conjugative plasmid in an obligate intracellular parasite. PLoS Biol 2005; 3:e248 [View Article] [PubMed]
     [Google Scholar]
  31. Maina AN, Luce-Fedrow A, Omulo S, Hang J, Chan T-C et al. Isolation and characterization of a novel Rickettsia species (Rickettsia asembonensis sp. nov.) obtained from cat fleas (Ctenocephalides felis. Int J Syst Evol Microbiol 2016; 66:4512–4517 [View Article] [PubMed]
     [Google Scholar]
  32. Duh D, Punda-Polic V, Avsic-Zupanc T, Bouyer D, Walker DH et al. Rickettsia hoogstraalii sp. nov., isolated from hard-and soft-bodied ticks. Int J Syst Evol Microbiol 2010; 60:977–984 [View Article] [PubMed]
     [Google Scholar]
  33. Campbell RW, Domrow R. Rickettsioses in Australia: isolation of Rickettsia tsutsugamushi and R. australis from naturally infected arthropods. Trans R Soc Trop Med Hyg 1974; 68:397–402 [View Article] [PubMed]
     [Google Scholar]
  34. Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM. Evolution and diversity of Rickettsia bacteria. BMC Biol 2009; 7:1–15
     [Google Scholar]
  35. Narra HP, Sahni A, Walker DH, Sahni SK. Recent research milestones in the pathogenesis of human rickettsioses and opportunities ahead. Future Microbiol 2020; 15:753–765 [View Article] [PubMed]
     [Google Scholar]
  36. Noriea NF, Clark TR, Hackstadt T. Targeted knockout of the Rickettsia rickettsii OmpA surface antigen does not diminish virulence in a mammalian model system. mBio 2015; 6:e00323–15 [View Article] [PubMed]
     [Google Scholar]
  37. Li H, Walker DH. rOmpA is a critical protein for the adhesion of Rickettsia rickettsii to host cells. Microb Pathog 1998; 24:289–298 [View Article] [PubMed]
     [Google Scholar]
  38. de la Fuente J, Garcia-Garcia JC, Barbet AF, Blouin EF, Kocan KM. Adhesion of outer membrane proteins containing tandem repeats of Anaplasma and Ehrlichia species (Rickettsiales: Anaplasmataceae) to tick cells. Vet Microbiol 2004; 98:313–322 [View Article] [PubMed]
     [Google Scholar]
  39. Fournier PE, Roux V, Raoult D. Phylogenetic analysis of spotted fever group rickettsiae by study of the outer surface protein rOmpA. Int J Syst Evol Microbiol 1998; 48:839–849
     [Google Scholar]
  40. Regnery RL, Spruill CL, Plikaytis BD. Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol 1991; 173:1576–1589 [View Article] [PubMed]
     [Google Scholar]
  41. Stenos J, Walker DH. The rickettsial outer-membrane protein A and B genes of Rickettsia australis, the most divergent rickettsia of the spotted fever group. Int J Syst Evol Microbiol 2000; 50:1775–1779 [View Article]
     [Google Scholar]
  42. Thu MJ, Qiu Y, Yamagishi J, Kusakisako K, Ogata S et al. Complete genome sequence of Rickettsia asiatica strain Maytaro1284, a member of spotted fever group rickettsiae isolated from an Ixodes ovatus tick in Japan. Microbiol Resour Announc 2019; 8:e00886–19 [View Article] [PubMed]
     [Google Scholar]
  43. Roux V, Fournier PE, Raoult D. Differentiation of spotted fever group rickettsiae by sequencing and analysis of restriction fragment length polymorphism of PCR-amplified DNA of the gene encoding the protein rOmpA. J Clin Microbiol 1996; 34:2058–2065 [View Article] [PubMed]
     [Google Scholar]
  44. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PloS one 2010; 5:e11147 [View Article] [PubMed]
     [Google Scholar]
  45. Kato CY, Chung IH, Robinson LK, Austin AL, Dasch GA et al. Assessment of real-time PCR assay for detection of Rickettsia spp. and Rickettsia rickettsii in banked clinical samples. J Clin Microbiol 2013; 51:314–317 [View Article] [PubMed]
     [Google Scholar]
  46. Brinkmann A, Hekimoğlu O, Dinçer E, Hagedorn P, Nitsche A et al. A cross-sectional screening by next-generation sequencing reveals Rickettsia, Coxiella, Francisella, Borrelia, Babesia, Theileria and Hemolivia species in ticks from Anatolia. Parasites & Vectors 2019; 12:1–13
     [Google Scholar]
  47. Parola P, Sanogo O, Lerdthusnee K, Zeaiter Z, Chauvancy G et al. Identification of Rickettsia spp. and Bartonella spp. in fleas from the Thai‐Myanmar border. Ann N Y Acad Sci 2003; 990:173–181 [View Article] [PubMed]
     [Google Scholar]
  48. Phoosangwalthong P, Hii SF, Kamyingkird K, Kengradomkij C, Pinyopanuwat N et al. Cats as potential mammalian reservoirs for Rickettsia sp. genotype RF2125 in Bangkok, Thailand. Vet Parasitol Reg Stud Reports 2018; 13:188–192 [View Article]
     [Google Scholar]
  49. Šlapeta Š, Šlapeta J. Molecular identity of cat fleas (Ctenocephalides felis) from cats in Georgia, USA carrying Bartonella clarridgeiae, Bartonella henselae and Rickettsia sp. RF2125. Vet Parasitol Reg Stud Reports 2016; 3:36–40
     [Google Scholar]
  50. Supriyono Takano A, Kuwata R, Shimoda H, Hadi UK et al. Detection and isolation of tick-borne bacteria (Anaplasma spp., Rickettsia spp., and Borrelia spp.) in Amblyomma varanense ticks on lizard (Varanus salvator. Microbiol Immunol 2019; 63:328–333 [View Article] [PubMed]
     [Google Scholar]
  51. Vilcins I-ME, Fournier P-E, Old JM, Deane E. Evidence for the presence of Francisella and spotted fever group rickettsia DNA in the tick Amblyomma fimbriatum (Acari: Ixodidae), Northern Territory, Australia. J Med Entomol 2009; 46:926–933 [View Article] [PubMed]
     [Google Scholar]
  52. Krueger L, Bai Y, Bennett S, Fogarty C, Sun S et al. Identification of zoonotic and vector-borne infectious agents associated with opossums (Didelphis Virginiana) in residential neighborhoods of Orange County, California. vertebrate_pest_conference 2016; 27: [View Article]
     [Google Scholar]
  53. Maina AN, Klein TA, Kim H-C, Chong S-T, Yang Y et al. Molecular characterization of novel mosquito-borne Rickettsia spp. from mosquitoes collected at the demilitarized zone of the Republic of Korea. PloS one 2017; 12:e0188327 [View Article]
     [Google Scholar]
  54. Toju H, Tanabe AS, Notsu Y, Sota T, Fukatsu T. Diversification of endosymbiosis: replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils. ISME J 2013; 7:1378–1390 [View Article] [PubMed]
     [Google Scholar]
  55. Thu MJ, Qiu Y, Matsuno K, Kajihara M, Mori-Kajihara A et al. Diversity of spotted fever group rickettsiae and their association with host ticks in Japan. Sci Rep 2019; 9:1–10
     [Google Scholar]
  56. Rydkina E, Roux V, Fetisova N, Rudakov N, Gafarova M et al. New rickettsiae in ticks collected in territories of the former Soviet Union. Emerging Infect Dis 1999; 5:811
     [Google Scholar]
  57. Tsui P-Y, Tsai K-H, Weng M-H, Hung Y-W, Liu Y-T et al. Molecular detection and characterization of spotted fever group Rickettsiae in Taiwan. Am J Trop Med Hyg 2007; 77:883–890
     [Google Scholar]
  58. Tahir D, Socolovschi C, Marié J-L, Ganay G, Berenger J-M et al. New Rickettsia species in soft ticks Ornithodoros hasei collected from bats in French Guiana. Ticks and Tick-borne Diseases 2016; 7:1089–1096 [View Article]
     [Google Scholar]
  59. Fournier PE, Xeridat B, Raoult D. Isolation of a rickettsia related to Astrakhan fever rickettsia from a patient in Chad. Ann N Y Acad Sci 2003; 990:152–157 [View Article] [PubMed]
     [Google Scholar]
  60. Mura A, Masala G, Tola S, Satta G, Fois F et al. First direct detection of rickettsial pathogens and a new rickettsia,‘Candidatus Rickettsia barbariae’, in ticks from Sardinia, Italy. Clin Microbiol Infect 2008; 14:1028–1033 [View Article] [PubMed]
     [Google Scholar]
  61. Sekeyova Z, Fournier P, Řeháček J, Raoult D. Characterization of a new spotted fever group rickettsia detected in Ixodes ricinus (Acari: Ixodidae) collected in Slovakia. J Med Entomol 2000; 37:707–713 [View Article] [PubMed]
     [Google Scholar]
  62. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009; 25:119–120 [View Article] [PubMed]
     [Google Scholar]
  63. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004880
Loading
Characterization of a novel transitional group Rickettsia species (Rickettsia tillamookensis sp. nov.) from the western black-legged tick, Ixodes pacificus
Int J Syst Evol Microbiol 71, 004880 (2021); https://doi.org/10.1099/ijsem.0.004880
/content/journal/ijsem/10.1099/ijsem.0.004880
/content/journal/ijsem/10.1099/ijsem.0.004880
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error