Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-19T19:29:31.887Z Has data issue: false hasContentIssue false
  • English
  • Français

Midichloria mitochondrii is widespread in hard ticks (Ixodidae) and resides in the mitochondria of phylogenetically diverse species

Published online by Cambridge University Press:  21 January 2008

S. EPIS ,
D. SASSERA ,
T. BENINATI ,
N. LO ,
L. BEATI ,
J. PIESMAN ,
L. RINALDI ,
K. D. McCOY ,
A. TORINA  and
L. SACCHI
...Show all authors
S. EPIS
Affiliation:
Dipartimento di Patologia Animale, Igiene e Sanità Pubblica Veterinaria, Università degli Studi di Milano, Milano, Italy
D. SASSERA
Affiliation:
Dipartimento di Patologia Animale, Igiene e Sanità Pubblica Veterinaria, Università degli Studi di Milano, Milano, Italy
T. BENINATI
Affiliation:
School of Biological Sciences, The University of Sydney, New South Wales, Australia
N. LO
Affiliation:
School of Biological Sciences, The University of Sydney, New South Wales, Australia
L. BEATI
Affiliation:
Institute of Arthropodology and Parasitology, Georgia Southern University, Statesboro, GA, USA
J. PIESMAN
Affiliation:
Division of Vector Borne Infectious Diseases, Coordinating Center for Infectious Diseases, Centers for Disease Control and Prevention, Fort Collins, CO, USA
L. RINALDI
Affiliation:
Dipartimento di Patologia e Sanità Animale, Universita degli Studi di Napoli Federico II, Napoli, Italy
K. D. McCOY
Affiliation:
Génétique et Evolution des Maladies Infectieuses, UMR CNRS-IRD 2724, IRD, Montpellier, France
A. TORINA
Affiliation:
Istituto Zooprofilattico Sperimentale della Sicilia, Palermo, Italy
L. SACCHI
Affiliation:
Dipartimento di Biologia Animale, Università di Pavia, Piazza Botta 9, Pavia, Italy
E. CLEMENTI
Affiliation:
Dipartimento di Biologia Animale, Università di Pavia, Piazza Botta 9, Pavia, Italy
M. GENCHI
Affiliation:
Dipartimento di Biologia Animale, Università di Pavia, Piazza Botta 9, Pavia, Italy
S. MAGNINO
Affiliation:
Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna, Sezione di Pavia, Italy
C. BANDI*
Affiliation:
Dipartimento di Patologia Animale, Igiene e Sanità Pubblica Veterinaria, Università degli Studi di Milano, Milano, Italy
*
*Corresponding author: Dipartimento di Patologia Animale, Igiene e Sanità Pubblica Veterinaria, Università degli Studi di Milano, Milano, Italy. Tel: +39 02 50318093. Fax: +39 02 50318095. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The hard tick Ixodes ricinus (Ixodidae) is the sole animal thus far shown to harbour an intra-mitochondrial bacterium, which has recently been named Midichloria mitochondrii. The objectives of this work were (i) to screen ixodid ticks for Midichloria-related bacteria and (ii) to determine whether these bacteria exploit the intra-mitochondrial niche in other tick species. Our main goal was to discover further models of this peculiar form of symbiosis. We have thus performed a PCR screening for Midichloria-related bacteria in samples of ixodid ticks collected in Italy, North America and Iceland. A total of 7 newly examined species from 5 genera were found positive for bacteria closely related to M. mitochondrii. Samples of the tick species Rhipicephalus bursa, found positive in the PCR screening, were analysed with transmission electron microscopy, which revealed the presence of bacteria both in the cytoplasm and in the mitochondria of the oocytes. There is thus evidence that bacteria invade mitochondria in at least 2 tick species. Phylogenetic analysis on the bacterial 16S rRNA gene sequences generated from positive specimens revealed that the bacteria form a monophyletic group within the order Rickettsiales. The phylogeny of Midichloria symbionts and related bacteria does not appear completely congruent with the phylogeny of the hosts.

Keywords

Midichloria mitochondriiIxodes ricinushard ticksintra-mitochondrialPCR screeningphylogeny
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 4 , April 2008 , pp. 485 - 494
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bandi, C., Dunn, A. M., Hurst, G. D. and Rigaud, T. (2001). Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends in Parasitology 17, 88–94.CrossRefGoogle ScholarPubMed
Barker, S. C. and Murrel, A. (2004). Systematics and evolution of ticks with a list of valid genus and species names. Parasitology 129 (Suppl.), S15–S36.Google Scholar
Beati, L. and Keirans, J. E. (2001). Analysis of systematic relationship among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA gene sequences and morphological characters. Journal of Parasitology 87, 32–48.Google Scholar
Beninati, T., Lo, N., Sacchi, L., Bandi, C., Noda, H. and Genchi, C. (2004). A novel alpha-Proteobacterium resides in the mitochondria of the tick Ixodes ricinus. Applied and Environmental Microbiology 70, 2596–2602.CrossRefGoogle ScholarPubMed
Black, W. C., Klompen, J. S. and Keirans, J. E. (1997). Phylogenetic relationships among tick subfamilies (Ixodida: Ixodidae: Argasidae) based on the 18S nuclear rRNA gene. Molecular Phylogenetics and Evolution 7, 129–144.CrossRefGoogle Scholar
Bowman, A. S. and Nuttall, P. A. (Eds.) (2004). Tick biology, disease and control. Parasitology 129 (Suppl. 2004).CrossRefGoogle Scholar
Cole, J. R., Chai, B., Marsh, T. L., Farris, R. J., Wang, Q., Kulam, S. A., Chandra, S., McGarrell, D. M., Schmidt, T. M., Garrity, G. M. and Tiedje, J. M., Ribosomal Database Project (2003). The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Research 31, 442–443.CrossRefGoogle ScholarPubMed
Fritsche, T. R., Horn, M., Seyedirashti, S., Gautom, R. K., Schleifer, K. H. and Wagner, M. (1999). In situ detection of novel bacterial endosymbionts of Acanthamoeba spp. phylogenetically related to members of the order Rickettsiales. Applied and Environmental Microbiology 65, 206–212.Google Scholar
Hickson, R. E., Simon, C., Cooper, A., Spicer, G. S., Sullivan, J. and Penny, D. (1996). Conserved sequence motifs, alignment, and secondary structure for the third domain of animal 12S rRNA. Molecular Biology and Evolution 13, 150–169.Google Scholar
Hoogstraal, H. and Aeschlimann, A. (1982). Tick–host specificity. Buletin de la Société Entomologique Suisse 55, 5–32.Google Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Klompen, J. S. H., Black, W. C., Keirans, J. E. and Norris, D. E. (2000). Systematics and biogeography of hard ticks, a total evidence approach. Cladistics 16, 79–102.CrossRefGoogle ScholarPubMed
Kumar, S., Tamura, K. and Nei, M. (2004). MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.CrossRefGoogle ScholarPubMed
Lewis, D. (1979). The detection of rickettsia-like microorganisms within the ovaries of female Ixodes ricinus ticks. Zeitschrift für Parasitenkunde 59, 295–298.Google Scholar
Lo, N., Beninati, T., Sassera, D., Bouman, E. A. P., Santagati, S., Gern, L., Sambri, V., Masuzawa, T., Gray, J., Jaenson, T. G. T., Bouattour, A., Bitam, I., Kenny, M. J., Guner, E. S., Kharitonenkov, I. G. and Bandi, C. (2006 a). Widespread distribution and high prevalence of an alpha-proteobacterial symbiont in the tick Ixodes ricinus. Environmental Microbiology 8, 1280–1287.CrossRefGoogle ScholarPubMed
Lo, N., Beninati, T., Sacchi, L. and Bandi, C. (2006 b). An alpha-proteobacterium invades the mitochondria of the tick Ixodes ricinus. In Insect Symbiosis II (ed. Bourtzis, K. and Miller, T.), pp. 25–37. CRC Press, Taylor and Francis Group, Boca Raton, FL, USA.Google Scholar
Mediannikov, O. I., Ivanov, L. I., Nishikawa, M., Saito, R., Sidel'nikov, I. N., Zdanovskaia, N. I., Mokretsova, E. V., Tarasevich, I. V. and Suzuki, H. (2004). Microorganism ‘Montezuma’ of the order Rickettsiales: the potential causative agent of tick-borne disease in the Far East of Russia. Zhurnal mikrobiologii, epidemiologii, i immunobiologii 1, 7–13 (in Russian).Google Scholar
Parola, P., Cornet, J. P., Sanogo, J. O., Miller, R. S., Thien, H. V., Gonzalez, J. P., Raoult, D., Telford, S. R. and Wongsrichanalai, C. (2003). Detection of Ehrlichia spp., Anaplasma spp., Rickettsia spp., and other eubacteria in ticks from the Thai-Myanmar border and Vietnam. Journal of Clinical Microbiology 41, 1600–1608.CrossRefGoogle ScholarPubMed
Sacchi, L., Bigliardi, E., Corona, S., Beninati, T., Lo, N. and Franceschi, A. (2004). A symbiont of the tick Ixodes ricinus invades and consumes mitochondria in a mode similar to that of the parasitic bacterium Bdellovibrio bacteriovorus. Tissue and Cell 36, 43–53.CrossRefGoogle Scholar
Sassera, D., Beninati, T., Bandi, C., Bouman, E. A., Sacchi, L., Fabbi, M. and Lo, N. (2006). ‘Candidatus Midichloria mitochondrii’, an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle. International Journal of Systematic and Evolutionary Microbiology 56, 2535–2540.CrossRefGoogle ScholarPubMed
Skarphedinsson, S., Jensen, P. M. and Kristiansen, K. (2005). Survey of tickborne infections in Denmark. Emerging Infectious Diseases 11, 1055–1061.CrossRefGoogle ScholarPubMed
Taylor, M. W., Shupp, P. J., de Nys, R., Kjelleberg, S. and Steinberg, P. D. (2005). Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environmental Microbiology 7, 419–433.Google Scholar
Thompson, J. D., Gibson, T. J., Jeanmougin, F. and Higgins, D. G. (1997). The Clustal X interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.Google Scholar
Werren, J. H. (1997). Biology of Wolbachia. Annual Review of Entomology 42, 587–609.CrossRefGoogle ScholarPubMed