1887

Abstract

We obtained a rickettsial isolate from the ovaries of the blacklegged tick, . The isolate (ISO7) was grown in the embryonic cell line IRE11. We characterized the isolate by transmission electron microscopy and gene sequencing. Phylogenetic analysis of 11 housekeeping genes demonstrated that the isolate fulfils the criteria to be classified as a representative of a novel rickettsial species closely related to ‘ ’. These rickettsiae form a clade separate from other species of rickettsiae. Gene sequences indicated that several genes important in rickettsial motility, invasiveness and temperature adaptation were mutated (e.g. , , , and ). We propose the name sp. nov. for this bacterium that infects the ovaries of the tick to acknowledge the pioneering contributions of Professor Paul Buchner (1886–1978) to research on bacterial symbionts. The type strain of sp. nov. is strain ISO-7 ( = DSM 29016 = ATCC VR-1814).

Funding
This study was supported by the:
  • National Institutes of Health (Award R01 AI49424 and R01 AI081690)
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2015-03-01
2024-04-23
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References

  1. Baldridge G. D., Burkhardt N. Y., Labruna M. B., Pacheco R. C., Paddock C. D., Williamson P. C., Billingsley P. M., Felsheim R. F., Kurtti T. J., Munderloh U. G. ( 2010 ). Wide dispersal and possible multiple origins of low-copy-number plasmids in rickettsia species associated with blood-feeding arthropods. . Appl Environ Microbiol 76, 17181731. [View Article] [PubMed]
    [Google Scholar]
  2. Balraj P., El Karkouri K., Vestris G., Espinosa L., Raoult D., Renesto P. ( 2008 ). RickA expression is not sufficient to promote actin-based motility of Rickettsia raoultii . . PLoS ONE 3, e2582. [View Article] [PubMed]
    [Google Scholar]
  3. Bechah Y., El Karkouri K., Mediannikov O., Leroy Q., Pelletier N., Robert C., Médigue C., Mege J. L., Raoult D. ( 2010 ). Genomic, proteomic, and transcriptomic analysis of virulent and avirulent Rickettsia prowazekii reveals its adaptive mutation capabilities. . Genome Res 20, 655663. [View Article] [PubMed]
    [Google Scholar]
  4. Benson M. J., Gawronski J. D., Eveleigh D. E., Benson D. R. ( 2004 ). Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellfleet, Cape Cod, Massachusetts. . Appl Environ Microbiol 70, 616620. [View Article] [PubMed]
    [Google Scholar]
  5. Billings A. N., Teltow G. J., Weaver S. C., Walker D. H. ( 1998 ). Molecular characterization of a novel Rickettsia species from Ixodes scapularis in Texas. . Emerg Infect Dis 4, 305309. [View Article] [PubMed]
    [Google Scholar]
  6. Buchner P. ( 1926 ). Studien an intrazellularen symbionten VI. Zur acarinen-symbiose. . Zeitschrift für Morphologie und Oekologie der Tiere 6, 625644. [View Article]
    [Google Scholar]
  7. Buchner P. ( 1965 ). Endosymbiosis of Animals with Plant Microorganisms. New York:: Interscience Publishers;.
    [Google Scholar]
  8. Burkhardt N. Y., Baldridge G. D., Williamson P. C., Billingsley P. M., Heu C. C., Felsheim R. F., Kurtti T. J., Munderloh U. G. ( 2011 ). Development of shuttle vectors for transformation of diverse Rickettsia species. . PLoS ONE 6, e29511. [View Article] [PubMed]
    [Google Scholar]
  9. Corrain R., Drigo M., Fenati M., Menandro M. L., Mondin A., Pasotto D., Martini M. ( 2012 ). Study on ticks and tick-borne zoonoses in public parks in Italy. . Zoonoses Public Health 59, 468476. [View Article] [PubMed]
    [Google Scholar]
  10. Cowdry E. V. ( 1925 ). A group of microorganisms transmitted hereditarily in ticks and apparently unassociated with disease. . J Exp Med 41, 817830. [View Article] [PubMed]
    [Google Scholar]
  11. Duh D., Punda-Polic V., Avsic-Zupanc T., Bouyer D., Walker D. H., Popov V. L., Jelovsek M., Gracner M., Trilar T. & other authors ( 2010 ). Rickettsia hoogstraalii sp. nov., isolated from hard- and soft-bodied ticks. . Int J Syst Evol Microbiol 60, 977984. [View Article] [PubMed]
    [Google Scholar]
  12. Edgar R. C. ( 2004 ). muscle: multiple sequence alignment with high accuracy and high throughput. . Nucleic Acids Res 32, 17921797. [View Article] [PubMed]
    [Google Scholar]
  13. Felsheim R. F., Kurtti T. J., Munderloh U. G. ( 2009 ). Genome sequence of the endosymbiont Rickettsia peacockii and comparison with virulent Rickettsia rickettsii: identification of virulence factors. . PLoS ONE 4, e8361. [View Article] [PubMed]
    [Google Scholar]
  14. Fournier P.-E., Dumler J. S., Greub G., Zhang J., Wu Y., Raoult D. ( 2003 ). Gene sequence-based criteria for identification of new rickettsia isolates and description of Rickettsia heilongjiangensis sp. nov.. J Clin Microbiol 41, 54565465. [View Article] [PubMed]
    [Google Scholar]
  15. Gillespie J. J., Joardar V., Williams K. P., Driscoll T., Hostetler J. B., Nordberg E., Shukla M., Walenz B., Hill C. A. & other authors ( 2012 ). A Rickettsia genome overrun by mobile genetic elements provides insight into the acquisition of genes characteristic of an obligate intracellular lifestyle. . J Bacteriol 194, 376394. [View Article] [PubMed]
    [Google Scholar]
  16. Kleba B., Clark T. R., Lutter E. I., Ellison D. W., Hackstadt T. ( 2010 ). Disruption of the Rickettsia rickettsii Sca2 autotransporter inhibits actin-based motility. . Infect Immun 78, 22402247. [View Article] [PubMed]
    [Google Scholar]
  17. Kurtti T. J., Munderloh U. G., Hughes C. A. N., Engstrom S. M., Johnson R. C. ( 1996 ). Resistance to tick-borne spirochete challenge induced by Borrelia burgdorferi strains that differ in expression of outer surface proteins. . Infect Immun 64, 41484153.[PubMed]
    [Google Scholar]
  18. Lee K.-M., Choi Y.-J., Shin S.-H., Choi M. K., Song H. J., Kim H. C., Klein T. A., Richards A. L., Park K. H., Jang W. J. ( 2013 ). Spotted fever group rickettsia closely related to Rickettsia monacensis isolated from ticks in South Jeolla province, Korea. . Microbiol Immunol 57, 487495.[PubMed] [CrossRef]
    [Google Scholar]
  19. Madeddu G., Mancini F., Caddeo A., Ciervo A., Babudieri S., Maida I., Fiori M. L., Rezza G., Mura M. S. ( 2012 ). Rickettsia monacensis as cause of Mediterranean spotted fever-like illness, Italy. . Emerg Infect Dis 18, 702704. [View Article] [PubMed]
    [Google Scholar]
  20. Magnarelli L. A., Andreadis T. G., Stafford K. C. III, Holland C. J. ( 1991 ). Rickettsiae and Borrelia burgdorferi in ixodid ticks. . J Clin Microbiol 29, 27982804.[PubMed]
    [Google Scholar]
  21. Moreno C. X., Moy F., Daniels T. J., Godfrey H. P., Cabello F. C. ( 2006 ). Molecular analysis of microbial communities identified in different developmental stages of Ixodes scapularis ticks from Westchester and Dutchess Counties, New York. . Environ Microbiol 8, 761772. [View Article] [PubMed]
    [Google Scholar]
  22. Munderloh U. G., Kurtti T. J. ( 1989 ). Formulation of medium for tick cell culture. . Exp Appl Acarol 7, 219229. [View Article] [PubMed]
    [Google Scholar]
  23. Munderloh U. G., Kurtti T. J. ( 2011 ). Emerging and re-emerging tick-borne diseases: new challenges at the interface of human and animal health. . In Critical Needs and Gaps in Understanding Prevention, Amelioration, and Resolution of Lyme and Other Tick-Borne Diseases: the Short-Term and Long-Term outcomes: Workshop Report, pp. 376404. Washington, DC:: The National Academies Press;.
    [Google Scholar]
  24. Munderloh U. G., Jauron S. D., Fingerle V., Leitritz L., Hayes S. F., Hautman J. M., Nelson C. M., Huberty B. W., Kurtti T. J. & other authors ( 1999 ). Invasion and intracellular development of the human granulocytic ehrlichiosis agent in tick cell culture. . J Clin Microbiol 37, 25182524.[PubMed]
    [Google Scholar]
  25. Munderloh U. G., Jauron S. D., Kurtti T. J. ( 2005 ). The tick: a different kind of host for human pathogens. . In Tick-Borne Diseases of Humans, pp. 3764. Edited by Goodman J. L., Dennis D. T., Sonenshine D. E. . Washington, DC:: American Society for Microbiology;. [View Article]
    [Google Scholar]
  26. Noda H., Munderloh U. G., Kurtti T. J. ( 1997 ). Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. . Appl Environ Microbiol 63, 39263932.[PubMed]
    [Google Scholar]
  27. Oliver J. D., Burkhardt N. Y., Felsheim R. F., Kurtti T. J., Munderloh U. G. ( 2014 ). Motility characteristics are altered for Rickettsia bellii transformed to overexpress a heterologous rickA gene. . Appl Environ Microbiol 80, 11701176. [View Article] [PubMed]
    [Google Scholar]
  28. Phan J. N., Lu C. R., Bender W. G., Smoak R. M. III, Zhong J. ( 2011 ). Molecular detection and identification of Rickettsia species in Ixodes pacificus in California. . Vector Borne Zoonotic Dis 11, 957961. [View Article] [PubMed]
    [Google Scholar]
  29. Rahman M. S., Gillespie J. J., Kaur S. J., Sears K. T., Ceraul S. M., Beier-Sexton M., Azad A. F. ( 2013 ). Rickettsia typhi possesses phospholipase A2 enzymes that are involved in infection of host cells. . PLoS Pathog 9, e1003399. [View Article] [PubMed]
    [Google Scholar]
  30. Roux V., Raoult D. ( 1995 ). Phylogenetic analysis of the genus Rickettsia by 16S rDNA sequencing. . Res Microbiol 146, 385396. [View Article] [PubMed]
    [Google Scholar]
  31. Roux V., Raoult D. ( 2000 ). Phylogenetic analysis of members of the genus Rickettsia using the gene encoding the outer-membrane protein rOmpB (ompB). . Int J Syst Evol Microbiol 50, 14491455. [View Article] [PubMed]
    [Google Scholar]
  32. Roux V., Rydkina E., Eremeeva M., Raoult D. ( 1997 ). Citrate synthase gene comparison, a new tool for phylogenetic analysis, and its application for the rickettsiae. . Int J Syst Bacteriol 47, 252261. [View Article] [PubMed]
    [Google Scholar]
  33. Rutherford K., Parkhill J., Crook J., Horsnell T., Rice P., Rajandream M. A., Barrell B. ( 2000 ). Artemis: sequence visualization and annotation. . Bioinformatics 16, 944945. [View Article] [PubMed]
    [Google Scholar]
  34. Saitou N., Nei M. ( 1987 ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. . Mol Biol Evol 4, 406425.[PubMed]
    [Google Scholar]
  35. Schicht S., Schnieder T., Strube C. ( 2012 ). Rickettsia spp. and coinfections with other pathogenic microorganisms in hard ticks from northern Germany. . J Med Entomol 49, 766771. [View Article] [PubMed]
    [Google Scholar]
  36. Seemann T. ( 2014 ). Prokka: rapid prokaryotic genome annotation. . Bioinformatics 30, 20682069. [View Article] [PubMed]
    [Google Scholar]
  37. Sekeyova Z., Roux V., Raoult D. ( 2001 ). Phylogeny of Rickettsia spp. inferred by comparing sequences of ‘gene D’, which encodes an intracytoplasmic protein. . Int J Syst Evol Microbiol 51, 13531360.[PubMed]
    [Google Scholar]
  38. Shin S.-H., Seo H.-J., Choi Y.-J., Choi M. K., Kim H. C., Klein T. A., Chong S. T., Richards A. L., Park K. H., Jang W. J. ( 2013 ). Detection of Rickettsia monacensis from Ixodes nipponensis collected from rodents in Gyeonggi and Gangwon Provinces, Republic of Korea. . Exp Appl Acarol 61, 337347. [View Article] [PubMed]
    [Google Scholar]
  39. Simser J. A., Palmer A. T., Munderloh U. G., Kurtti T. J. ( 2001 ). Isolation of a spotted fever group Rickettsia, Rickettsia peacockii, in a Rocky Mountain wood tick, Dermacentor andersoni, cell line. . Appl Environ Microbiol 67, 546552. [View Article] [PubMed]
    [Google Scholar]
  40. Simser J. A., Palmer A. T., Fingerle V., Wilske B., Kurtti T. J., Munderloh U. G. ( 2002 ). Rickettsia monacensis sp. nov., a spotted fever group Rickettsia, from ticks (Ixodes ricinus) collected in a European city park. . Appl Environ Microbiol 68, 45594566. [View Article] [PubMed]
    [Google Scholar]
  41. Simser J. A., Rahman M. S., Dreher-Lesnick S. M., Azad A. F. ( 2005 ). A novel and naturally occurring transposon, ISRpe1 in the Rickettsia peacockii genome disrupting the rickA gene involved in actin-based motility. . Mol Microbiol 58, 7179. [View Article] [PubMed]
    [Google Scholar]
  42. Swofford D. L. ( 2002 ). paup*: Phylogenetic analysis using parsimony (and other methods), version 4. . Sunderland, MA:: Sinauer Associates;.
    [Google Scholar]
  43. Troughton D. R., Levin M. L. ( 2007 ). Life cycles of seven ixodid tick species (Acari: Ixodidae) under standardized laboratory conditions. . J Med Entomol 44, 732740. [View Article] [PubMed]
    [Google Scholar]
  44. Troyo A., Carranza M., Moreira A., Calderon-Arguedas O., Hun L., Taylor L. ( 2013 ). Detection of a Rickettsia closely related to R. monacensis in Ixodes boliviensis from Costa Rica. Am Soc Trop Med Hyg Abstract Book Abstract 747 http://www.astmh.org/Meeting_Archives.htm.
    [Google Scholar]
  45. Vitorino L., Chelo I. M., Bacellar F., Zé-Zé L. ( 2007 ). Rickettsiae phylogeny: a multigenic approach. . Microbiology 153, 160168. [View Article] [PubMed]
    [Google Scholar]
  46. Weller S. J., Baldridge G. D., Munderloh U. G., Noda H., Simser J., Kurtti T. J. ( 1998 ). Phylogenetic placement of rickettsiae from the ticks Amblyomma americanum and Ixodes scapularis . . J Clin Microbiol 36, 13051317.[PubMed]
    [Google Scholar]
  47. Zhang J. Z., Hao J. F., Walker D. H., Yu X. J. ( 2006 ). A mutation inactivating the methyltransferase gene in avirulent Madrid E strain of Rickettsia prowazekii reverted to wild type in the virulent revertant strain Evir. . Vaccine 24, 23172323. [View Article] [PubMed]
    [Google Scholar]
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