Ultrastructural evidence of the ehrlichial developmental cycle in naturally infected Ixodes persulcatus ticks in the course of coinfection with rickettsia, borrelia, and a flavivirus

Vsevolod Popov, Edward I. Korenberg, Valentina V. Nefedova, Violet C. Han, Julie W. Wen, Yurii V. Kovalevskii, Natalia B. Gorelova, David Walker

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Ehrlichiae are small gram-negative obligately intracellular bacteria that multiply within vacuoles of their host cells and are associated for a part of their life cycle with ticks, which serve as vectors for vertebrate hosts. Two morphologically and physiologically different ehrlichial cell types, reticulate cells (RC) and dense-cored cells (DC), are observed during experimental infection of cell cultures, mice, and ticks. Dense-cored cells and reticulate cells in vertebrate cell lines alternate in a developmental cycle. We observed ultrastructure of RC and DC of Ehrlichia muris in morulae in salivary gland cells and coinfection with Borrelia burgdorferi sensu lato (sl), "Candidatus Rickettsia tarasevichiae," and a flavivirus (presumably, tick-borne encephalitis virus [TBEV]) of Ixodes persulcatusticks collected in the Cis-Ural region of Russia. Polymerase chain reaction revealed 326 (81.5%) of 400 ticks carrying at least one infectious agent, and 41.5% (166 ticks) were coinfected with two to four agents. Ehrlichiae and rickettsiae were identified by sequencing of 359 bp of the 16S rRNA gene of E. muris and of 440 bp of the 16S rRNA gene and 385 bp of the gltA gene of "R. tarasevichiae." Different organs of the same tick harbored different microorganisms: TBEV in salivary gland and borreliae in midgut; E. muris in salivary gland; and "R. tarasevichiae" in midgut epithelium. Salivary gland cells contained both RC and DC, a finding that confirmed the developmental cycle in naturally infected ticks. Dense-cored cells in tick salivary glands were denser and of more irregular shape than DC in cell cultures. Ehrlichia-infected salivary gland cells had lysed cytoplasm, suggesting pathogenicity of E. muris for the tick host at the cellular level, as well as potential transmission during feeding. Rickettsiae in the midgut epithelial cells multiplied to significant numbers without altering the host cell ultrastructure. This is the first demonstration of E. muris, "R. tarasevichiae," and the ehrlichial developmental cycle in naturally infected I. persulcatus sticks.

Original languageEnglish (US)
Pages (from-to)699-716
Number of pages18
JournalVector-Borne and Zoonotic Diseases
Volume7
Issue number4
DOIs
StatePublished - Dec 1 2007

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Borrelia
Flavivirus
Rickettsia
Ixodes
Ticks
Coinfection
Salivary Glands
Ehrlichia
Tick-Borne Encephalitis Viruses
rRNA Genes
Vertebrates
Cell Culture Techniques
Borrelia burgdorferi Group
vpr Genes
Morula
Russia

Keywords

  • "Candidatus Rickettsia tarasevichiae"
  • Borrelia burgdorferi sensu lato (sl)
  • Coinfection
  • Developmental cycle
  • Ehrlichia muris
  • Ixodes persulcatus

ASJC Scopus subject areas

  • Infectious Diseases
  • Parasitology

Cite this

Ultrastructural evidence of the ehrlichial developmental cycle in naturally infected Ixodes persulcatus ticks in the course of coinfection with rickettsia, borrelia, and a flavivirus. / Popov, Vsevolod; Korenberg, Edward I.; Nefedova, Valentina V.; Han, Violet C.; Wen, Julie W.; Kovalevskii, Yurii V.; Gorelova, Natalia B.; Walker, David.

In: Vector-Borne and Zoonotic Diseases, Vol. 7, No. 4, 01.12.2007, p. 699-716.

Research output: Contribution to journalArticle

Popov, Vsevolod ; Korenberg, Edward I. ; Nefedova, Valentina V. ; Han, Violet C. ; Wen, Julie W. ; Kovalevskii, Yurii V. ; Gorelova, Natalia B. ; Walker, David. / Ultrastructural evidence of the ehrlichial developmental cycle in naturally infected Ixodes persulcatus ticks in the course of coinfection with rickettsia, borrelia, and a flavivirus. In: Vector-Borne and Zoonotic Diseases. 2007 ; Vol. 7, No. 4. pp. 699-716.
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AU - Popov, Vsevolod

AU - Korenberg, Edward I.

AU - Nefedova, Valentina V.

AU - Han, Violet C.

AU - Wen, Julie W.

AU - Kovalevskii, Yurii V.

AU - Gorelova, Natalia B.

AU - Walker, David

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N2 - Ehrlichiae are small gram-negative obligately intracellular bacteria that multiply within vacuoles of their host cells and are associated for a part of their life cycle with ticks, which serve as vectors for vertebrate hosts. Two morphologically and physiologically different ehrlichial cell types, reticulate cells (RC) and dense-cored cells (DC), are observed during experimental infection of cell cultures, mice, and ticks. Dense-cored cells and reticulate cells in vertebrate cell lines alternate in a developmental cycle. We observed ultrastructure of RC and DC of Ehrlichia muris in morulae in salivary gland cells and coinfection with Borrelia burgdorferi sensu lato (sl), "Candidatus Rickettsia tarasevichiae," and a flavivirus (presumably, tick-borne encephalitis virus [TBEV]) of Ixodes persulcatusticks collected in the Cis-Ural region of Russia. Polymerase chain reaction revealed 326 (81.5%) of 400 ticks carrying at least one infectious agent, and 41.5% (166 ticks) were coinfected with two to four agents. Ehrlichiae and rickettsiae were identified by sequencing of 359 bp of the 16S rRNA gene of E. muris and of 440 bp of the 16S rRNA gene and 385 bp of the gltA gene of "R. tarasevichiae." Different organs of the same tick harbored different microorganisms: TBEV in salivary gland and borreliae in midgut; E. muris in salivary gland; and "R. tarasevichiae" in midgut epithelium. Salivary gland cells contained both RC and DC, a finding that confirmed the developmental cycle in naturally infected ticks. Dense-cored cells in tick salivary glands were denser and of more irregular shape than DC in cell cultures. Ehrlichia-infected salivary gland cells had lysed cytoplasm, suggesting pathogenicity of E. muris for the tick host at the cellular level, as well as potential transmission during feeding. Rickettsiae in the midgut epithelial cells multiplied to significant numbers without altering the host cell ultrastructure. This is the first demonstration of E. muris, "R. tarasevichiae," and the ehrlichial developmental cycle in naturally infected I. persulcatus sticks.

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