Journal:2005. 13 (1)
PECULIARITIES OF CADMIUM-TOLERANT POPULATIONS OF IXODES TICKS: SPECIFICITY OF THEIR MICROBIOCENOSES, IMMUNITY AND VECTOR CAPACITY
About authors:A. N. Alekseev, Zoological Institute, Russian Academy of Sciences, Universitetskaya emb., 1, 199034 St. Petersburg,
This study was financially supported in part by a grant of the Russian Foundation for Basic Re-search (No. 04-04-49119), in part by a grant of Russian Academy of Sciences Presidium Pro-gramme «Fundamental Sciences for Medicine" (2005). We would like to thank Sergei Golovatch, who corrected the English of an advanced draft.
The appearance and prevalence of exoskeleton anomalies in Ixodes ticks chosen as markers of anthropogenic press allows to reveal their distribu-tion and the rate of occurrence in Russia and several Western European countries. Chemical analyses show the appearance of anomalies as being related to the accumulation of heavy metal ions, first of all cadmium which prevails in specimens and is known as changing tick metabolism. Cd concentrations are 1.5-2 times higher in anomalous ticks than in normal ones, cadmium supposedly suppressing tick immunity. To provide indirect evidence of this, microflora of anomalous and normal ticks has been compared, with 73 hungry tick females collected in April 2003 and 2004 in a focus of tick-borne diseases near St. Petersburg, Russia screened micro-biologically. A study of "vulgar" microflora in both parts of the Ixodes persulcatus Schulze population shows the whole microbiocenosis of anomalous and normal ticks as being quite different. Microflo-ra of Gram-negative and Gram-positive bacteria, bacilli, cocci and fungi appears to be much richer in anomalous ticks than in normal ones (47 versus 28 species). Only 14 (of 61) species representing the "vulgar" microflora are coincided in both groups of ticks. Not more than 4 species of microorganisms are present per normal tick, whereas one tick with exoskeleton anomalies can contain 5, 6 or even 7 species simultaneously. Only in anomalous ticks do the cocci of the genus Staphylococcus and the
fungi of the genus Penicillum absolutely prevail. Staphylococci are known as active stimulants of lysozyme and defensin production, both the main tools of the tick immune system. Scarcity of these cocci and fungi in normal ticks and their abundance in anomalous ones, as well as the great prevalence of multi infections in anomalous ticks are accepted as markers of their immune system suppression. Revised (6,169 adult ticks screened using PCR; 1996-2000) data concerning the prevalence of tick-borne multi infections (such as mixtures of Borre-lia, Ehrlichia, Anaplasma, Babesia or tick-borne encephalitis virus) confirm that exoskeleton anom-alies represent external markers of cadmium accu-mulation, increased tick vector capacity and dan-gerousness. Analysis of anomalous tick microflora supports this observation as well, because only among anomalous tick numerous phyto- or zoo-pathogenic bacteria and, especially, fungi have been revealed, which can be very dangerous for man with an immune system suppressed by any factor or associated disease.
Alekseev A.N., Dubinina E.V. 1993. Abnormalities in Ixodes ticks (Ixodoidea, Ixodinae). Acarina, 1 (1): 73-85.
Alekseev A.N., Dubinina H.V. 1996. Some aspects of mite (Oppiidae) and tick (Ixodidae) pathology as a result of anthropogenic pressure. In: R. Mitchell, D.J. Horn, G.R. Needham, W.C. Welbourn (Eds). Acarology IX. Columbus, Ohio. Proceeding. Vol. l,p. 117-120.
Alekseev A.N., Dubinina H.V. 2001. Heterogeneity of Ixodes persulcatus Schulze (Acarina: Ixodidae) population determines the qualities of infected spec-imen as a host and vector of parasite. Acarina, 9 (2): 277-298.
Alekseev A.N., Dubinina H.V. 2002. Stability of par-asitic systems under conditions of anthropogenic pressure. Contributions from the Zoological Insti-tute, No. 6. St. Petersburg. 43 pp.
Alekseev A.N., Dubinina H.V. 2004. Eurasian Ixodes tick types, their properties and vector capacity. Acarina, 12 (2): 121-139.
Alekseev A.N., Dubinina H.V., Van de Pol I., Schouls L.M. 2001. Identification of Ehrlichia
spp. and Borrelia burgdorferi in Ixodes ticks in the Baltic regions of Russia. Journal of Clinical Microbiol-ogy, 39 (6): 2237-2242.
Anigstein L., Whithey D., Micks D. 1950. Antibacterial activity of a substance present in ticks (Ixodidae) of Texas. Nature, 4212: 141-143.
Ceraul S.M., Sonenshine D.E., Hynes W.L. 2002. Re-sistance of the tick Dermacentor variabilis (Acari: Ixodidae) following challenge with the bacterium Escherichia coli (Enterobacteriales: Enterobacte-riaceae). Journal of Medical Entomology, 39 (2): 376-383.
[Change-over in taxonomy and nomenclature of bacte-ria]. Klinicheskaya microbiologiya i antimikrob-naya khemoterapiya, 2004.6(1): 4-9. [In Russian] Cherepanova N.P. 1964. [Fungi on ticks]. Botanichesky Zhurnal, 49 (5): 696-699. [In Russian]
Chirov P. A., Peterson A.M., Turtseva M.A. 2003. [Native microbial association ofgastrointestinal tract ofhorse-flies Tabanus bovinus and Hybomitra ciureai]. En-tomologicheskie i parasitologicheskie issledovani-ya v Povolzh'e.
Saratov, 2: 95-105. [In Russian]
Chirov P.A., Turtseva M.A., Peterson A.M. 2004. [Com-parative characteristics of associations of symbiot-ic microorganisms revealed from two species of ticks of the genus Dermacentor Koch.] In: Yu.S. Balashov (Ed.) VIII Vserossiyskoe akarolog-icheskoe soveshchanie (Saint-Petersburg, Novem-ber 30 - December 2,2004). Publisher: Zoological Institute of Russian Academy of Sciences, St. Pe-tersburg, pp. 144-145. [In Russian]
Dobler G., Braveny I. 2003. Recent taxonomic changes and update of nomenclature for bacteria identified in clinical material. European Journal ofClinicalMicro-biology and Infectious Disease, 22: 643-646.
Dubinina H.V., Alekseev A.N. 1994. Skeleton changes in the oribatid mites under the influence of theheavy metal ions accumulation. Acarina, 2 (1-2): 81-93.
Dubinina H.V., Alekseev A.N., Svetashova E.S. 2004. New Ixodes tick populations appearing as a result of, and tolerant to, cadmium contamination. Acari-na, 12 (2): 141-149.
Duncan J.T. 1925. On a bactericidal principle present in the alimentary canal of insects and arachnids. Par-asitology, 18 (2): 238-252.
Flemming A. 1922. On a remarkable bacteriolytic ele-ment found in tissues and secretions. Proceeding of Royal Society, 93: 306-317.
Hindle E., Duncan J.T. 1925. The viability of bacteria in Argas persicus. Parasitology, 17 (2): 434-446.
Holt J.G., Krieg N.R., Sneath H. A., Staley J.T. Williams S.T. 1997. [Bergey's Manual of Determinative Bacteriology]. Ninth edition. Publisher: Mir, Mos-cow. Ò. 1: 430 pp.; Ò. 2: 800 pp. [In Russian]
Johns R., Ohnishi J., Broadwater A., Sonenshine D.E., de Silva A.M., Hynes W.L. 2001. Contrasts in tick innate immune responses to Borrelia burgdorferi challenge: Immunotolerance in Ixodes scapularis versus immunocompetence in Dermacentor varia-bilis (Acari: Ixodidae). Journal of Medical Ento-mology, 38 (1): 99-107.
Johns R., Sonenshine D.E., Hynes W.L. 1998. Control of bacterial infections in the hard tick Dermacentor variabilis (Acari: Ixodidae): Evidence for the exist-ence of antimicrobial proteins in tick hemolymph. Journal of Medical Entomology, 35 (4): 458-464.
Johns R., Sonenshine D.E., Hynes W.L. 2000. Response of the tick Dermacentor variabilis (Acari: Ixodi-dae) to hemocoelic inoculation of Borrelia burg-dorferi (Spirochetales). Journal of Medical Ento-mology, 37 (2): 265-270.
Jollés P. 1964. Neuere Untersuchungen an Lysozymen. Angewandte Chemie, 76: 20-28. [In German] Kopacek P., Vogt R., Jindrak L., Weise C., Safarik I.
1999. Purification and characterization of the lys-ozyme from the gut of the soft tick Ornithodoros mubata. Insect Biochem istry and Molecular Biolo-gy, 29: 989-997.
Kryuchechnikov V.N. 1991. Protective responses of Ixodoidea hemocytes. In: F. Dusbabek and V. Buk-va (Eds.) Modern acarology. SPB Academic, Prague, p. 331-334.
Nakajima Y., van der Goes van Naters-Yasui A., Taylor D., Yamakawa M. 2002. Antibacterial peptide de-fensin is involved in midgut immunity of the soft tick, Ornithodoros moubata (Acari: Argasidae). Insect Molecular Biology, 11: 611-618.
Petrov V.G. 1959. [Summing-up of Ixodes tick study as of tularemia vectors]. In: E.N. Pavlovsky (Ed.). X soveshchanie po parazitologicheskim problemam i prirodnoochagovym boleznyam (22-29 October 1959). Proceedings. Publisher: Academy of Sci-ences USSR, Moscow, Leningrad, pp. 160-162. [In Russian]
Petrov V.G. 1968. [Comparative study of the ticks Dermacentor marginatus Sulz. and Ixodes ricinus L. as reservoirs of causative agent of tularemia]. Parazitologiya, 2 (6): 424^29. [In Russian]
Podboronov V.M. 1990. [Lysozyme from Ixodes per-sulcatus ticks]. Meditsinskaya parazitologiya i parazitarnye bolezni, 3: 21-23. [In Russian]
Podboronov V.M. 2004. [The Pathogens of Human and Animal Diseases and the Ticks] .-Publisher: Med-itsina, Moscow, 224 pp. [In Russian]
Rudakova S.A., Matuscenko E.V., Yakimenko V.V., Tokarevich N.K., Andreychuk Yu.V. 2004. [Ex-perimental study of participation of the tick Derma-centor reticulates in the circulation of borreliae in natural foci of tick-borne borrelioses]. In: Yu.S. Balashov (Ed.) VIII Vserossiyskoe akarolog-icheskoe soveshchanie (Saint-Petersburg, Novem-ber 30 - December 2,2004). Publisher: Zoological Institute of Russian Academy of Sciences, St. Pe-tersburg, pp. 90-93. [In Russian]
Semenov A. V. 2003. [Multiformity of infection by path-ogens of the population of Ixodes persulcatus ticks on the territory with hard anthropogenic pressure]. Abstract of the Candidate of Biological Sciences thesis. Moscow. 21 pp. [In Russian]
Sutton D. A., Fothergill A. W., Rinaldi M.G. 2001. [Guide to Clinically Significant Fungi]. Publisher: Mir, Moscow, 468 pp. [In Russian]
Zhioua E., Ginsberg H.S., Humber R.A., Lebrun R.A. 1999. Preliminary survey for entomopathogenic fungi associated with Ixodes scapularis (Acari: Ixodidae) in Southern New York and New Eng-land, USA. Journal ofMedical Entomology, 36 (5): 635-637.