Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-06T06:05:53.983Z Has data issue: false hasContentIssue false

Three strains of Wolbachia pipientis and high rates of infection in Iranian sandfly species

Published online by Cambridge University Press:  03 February 2014

A. Bordbar
Affiliation:
Molecular Systematics Laboratory, Parasitology Department, Pasteur Institute of Iran, Tehran, Iran
S. Soleimani
Affiliation:
Molecular Systematics Laboratory, Parasitology Department, Pasteur Institute of Iran, Tehran, Iran Microbiology Department, Qom Branch, Islamic Azad University, Qom, Iran
F. Fardid
Affiliation:
Molecular Systematics Laboratory, Parasitology Department, Pasteur Institute of Iran, Tehran, Iran
M.R. Zolfaghari
Affiliation:
Microbiology Department, Qom Branch, Islamic Azad University, Qom, Iran
P. Parvizi*
Affiliation:
Molecular Systematics Laboratory, Parasitology Department, Pasteur Institute of Iran, Tehran, Iran
*
*Author for Correspondence Phone: +00 98216649 6414 Fax: +00982166968855 E-mail: [email protected]

Abstract

Individual wild-caught sandflies from Iran were examined for infections of Wolbachia pipientis by targeting the major surface protein gene wsp of this intracellular α-proteobacterium. In total, 638 male and female sandflies were screened, of which 241 were found to be positive for one of three wsp haplotypes. Regardless of geographical origins and habitats, Phlebotomus (Phlebotomus) papatasi and other sandfly species were found to be infected with one common, widespread strain of A-group W. pipientis (Turk 54, GenBank accession EU780683; AY288297). In addition, a new A-group haplotype (Turk07, GenBank accession KC576916) was isolated from Phlebotomus (Paraphlebotomus) mongolensis and Phlebotomus (Pa.) caucasicus, and a new B-group haplotype (AZ2331, GenBank accession JX488735) was isolated from Phlebotomus (Larroussius) perfiliewi. Therefore, Wolbachia was found to occur in at least three of the incriminated vectors of zoonotic cutaneous leishmaniasis and zoonotic visceral leishmaniasis in different geographical regions of Iran. It may provide a new tool for the future control of leishmaniasis.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2014 

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

Akhavan, A.A., Yaghoobi-Ershadi, M.R., Khamesipour, A., Mirhendi, H., Alimohammadian, M.H., Rassi, Y., Arandian, M.H., Jafari, R., Abdoli, H., Shareghi, N., Ghanei, M. & Jalali-zand, N. (2010) Dynamics of infection rates in Rhombomys opimus (Rodentia: Gerbillinae) population of an endemic focus of zoonotic cutaneous leishmaniasis in Iran. Bulletin de la Société de Pathologie Exotique 103, 8489.CrossRefGoogle ScholarPubMed
Azpurua, J., Cruz, D.D.L., Valderama, A. & Windsor, D. (2010) Lutzomyia sand fly diversity and rates of infection by Wolbachia and an Exotic Leishmania species on Barro Colorado Island, Panama. PLoS Neglected Tropical Diseases 4(3), e627. doi:10.1371. journal.pntd.0000627.CrossRefGoogle Scholar
Baldo, L., Bartos, J.D., Werren, J.H., Bazzocchi, C., Casiraghi, M. & Panelli, S. (2002) Different rates of nucleotide substitutions in Wolbachia endosymbionts of arthropods and nematodes: arms race or host shifts? Parasitologia 44, 179187.Google Scholar
Baldo, L., Dunning Hotopp, J.C., Jolley, A.K., Bordenstein, S.R., Biber, S.A., Choudhury, R.R., Hayashi, C., Maiden, M.C.J., Tettelin, H. & Werren, J.H. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis . Applied and Environmental Microbiology 11, 70987110.CrossRefGoogle Scholar
Benlarbi, M. & Ready, P.D. (2003) Host-specific Wolbachia strains in widespread populations of Phlebotomus perniciosus and P. papatasi (Diptera: Psychodidae), and prospects for driving genes into these vectors of Leishmania . Bulletin of Entomological Research 93, 383391.Google Scholar
Brennan, L.J., Keddie, B.A., Braig, H.R. & Harris, H.L. (2008) The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line. PLoS Neglected Tropical Diseases 3 (5), e2083. doi:10.1371.journal.pone.0002083.Google Scholar
Cordaux, R., Bouchon, D. & Grève, P. (2011) The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends in Genetics 27, 8.Google Scholar
Cui, L., Chang, S.H., Stickman, D. & Rowton, E. (1999) Frequency of Wolbachia infection in laboratory and field sand fly Diptera Psychodidae populations. Journal of the American Mosquito Control Association 15, 571572.Google Scholar
Dobson, S.L., Fox, C.W. & Jiggins, F.M. (2002) The effect of Wolbachia-induced cytoplasmic incompatibility on host population size in natural and manipulated systems. Proceedings of the Royal Society of London, B 269, 437445.CrossRefGoogle ScholarPubMed
Henri, H. & Mouton, L. (2012) High-resolution melting technology: a new tool for studying the Wolbachia endosymbiont diversity in the field. Molecular Ecology Resource 12, 7581.Google Scholar
Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A. & Werren, J.H. (2008) How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiology Letters 281, 215220.CrossRefGoogle Scholar
Kassem, H.A., Hassan, A.N., Abdel Hamed, I., Osman, G.E.l., Khalab, E.M. & Madkour, M.A. (2003) Wolbachia infection and the expression of cytoplasmic incompatibility in sandflies Diptera Psychodidae from Egypt. Annals of Tropical Medicine and Parasitology 97, 639644.Google Scholar
Killick-Kendrick, R. (1990) Phlebotomine vectors of the leishmaniases: a review. Medical and Veterinary Entomology 4, 124.Google Scholar
Kyei-Poku, G.K., Colwell, D.D., Coghlin, P., Benkel, B. & Floate, K.D. (2005) On the ubiquity and phylogeny of Wolbachia in lice. Molecular Ecology 14, 285294.Google Scholar
Matsumoto, K., Izri, A., Dumon, H., Raoult, D. & Parola, Ph. (2008) First detection of Wolbachia spp., including a new genotype, in sand flies collected in Marseille, France. Journal of Medical Entomology 45, 466469.Google Scholar
Mitsuhashi, W., Saiki, T., Wei, W., Kawakita, H. & Sato, M. (2002) Two novel strains of Wolbachia coexisting in both species of mulberry leafhoppers. Insect Molecular Biology 11, 577584.Google Scholar
Mitsuhashi, W., Fukuda, H., Nicho, K. & Murakami, R. (2004) Male-killing Wolbachia in the butterfly Hypolimnas Bolina . Entomologia Experimentalis et Applicata 112, 5764.Google Scholar
Motazedian, M.H., Parhizkari, M., Mehrabani, D., Hatam, Gh.R. & Asghari, Q. (2010) First detection of Leishmania major in Rattus norvegicus from Fars Province, Southern Iran. Vector-Borne and Zoonotic Diseases 10, 969975.CrossRefGoogle ScholarPubMed
Nadim, A. & Seyedi-rashti, M.A. (1971) A brief review of the epidemiology of various types of leishmaniases in Iran. Acta Medica Iranica 14, 99106.Google Scholar
Nadim, A., Javadian, E., Tahvildare-Bidruni, G., Mottaghi, M. & Abai, M.R. (1992) Epidemiological aspects of Kala-Azar in Meshkin-Shahr, Iran: investigation on vectors. Iranian Journal of Public Health 21, 6172.Google Scholar
Nirgianaki, A., Banks, G.K., Frohlich, D.R., Veneti, Z., Braig, H.R., Miller, T.A., Bedford, I.D., Markham, P.G., Savakis, C. & Bourtzis, K. (2003) Wolbachia infections of the whitefly Bemisia tabaci . Current Microbiology 47, 93101.Google Scholar
O'Neill, S.L., Giordano, R., Colbert, A.M., Karr, T.L. & Robertson, H.M. (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proceedings of the National Academy of Sciences of the United States of America 89, 26992702.Google Scholar
Ono, M., Braig, H.R., Munstermann, L.E., Ferro, C. & O'Neill, S.L. (2001) Wolbachia infections of phlebotomine sand flies (Diptera: Psychodidae). Journal of Medical Entomology 38, 237241.Google Scholar
Parvizi, P. & Ready, P.D. (2008) Nested PCRs of nuclear ITS-rDNA fragments detect three Leishmania species of gerbils in sandflies from Iranian Foci of zoonotic cutaneous leishmaniasis. Tropical Medicine and International Health 13, 11591171.Google Scholar
Parvizi, P., Benlarbi, M. & Ready, P.D. (2003) Mitochondrial and Wolbachia markers for the sandfly Phlebotomus papatasi: little population differentiation between peridomestic sites and gerbil burrows in Isfahan province, Iran. Medical and Veterinary Entomology 17, 351362.Google Scholar
Parvizi, P., Mazloumi-Gavgani, A.S., Davies, C.R., Courtenay, O. & Ready, P.D. (2008) Two Leishmania species circulating in the Kaleybar focus of ‘infantile visceral leishmaniasis’, Northwest Iran: implications for deltamethrin dog collar intervention. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 891897.Google Scholar
Parvizi, P., Fardid, F. & Amirkhani, A. (2009) Isolation process of two genes of wsp and 16 s rRNA in the intracellular bacterium; Wolbachia pipientis in Phlebotomus papatasi sandfly vector of Zoonotic Cutaneous leishmaniasis in Iran. Iranian Journal of Medical Microbiology 4, 5360. (in Farsi).Google Scholar
Parvizi, P., Tahehrkhani, H. & Ready, P.D. (2010 a) Phlebotomus caucasicus and Phlebotomus mongolensis (Diptera: Psychodidae): indistinguishable by the mitochondrial cytochrome b gene in Iran. Bulletin of Entomological Research 100, 415420.Google Scholar
Parvizi, P., Naddaf, S.R. & AlaeeNovin, E. (2010 b) Molecular typing and phylogenetic analysis of some species belonging to Phlebotomus (Larroussius) and Phlebotomus (Adlerius) subgenera (Diptera: Psychodidae) from two locations in Iran. Iranian Journal of Arthropod Borne Diseases 4, 110.Google ScholarPubMed
Parvizi, P., Bordbar, A. & Najafzadeh, N. (2013 a) Detection of Wolbachia pipientis, including a new strain containing the wsp gene, in two sister species of Paraphlebotomus sandflies, potential vectors of zoonotic cutaneous leishmaniasis. Mem Ins Oswaldo Cruz 108, 414420.CrossRefGoogle ScholarPubMed
Parvizi, P., Fardid, F. & Soleimani, S. (2013 b) Detection of a New Strain of Wolbachia pipientis in Phlebotomus perfiliewi transcaucasicus, a Potential Vector of Visceral Leishmaniasis in North West of Iran, by Targeting the Major Surface Protein Gene. J Arthropod Borne Dis 7, 4655.Google ScholarPubMed
Perez-Losada, M., Viscidi, R.P., Demma, J.C., Zenilman, J. & Crandall, K.A. (2005) Population genetics of Neisseria gonorrhoeae in a high-prevalence community using a hypervariable outer membrane porB and 13 slowly evolving housekeeping genes. Molecular Biology and Evolution 22, 18871902.Google Scholar
Perlman, S.J., Magnus, S.A. & Copley, C.R. (2010) Pervasive associations between Cybaeus spiders and the bacterial symbiont Cardinium. Journal of Invertebrate Pathology 103, 150155.CrossRefGoogle ScholarPubMed
Pintureau, B., Chaudier, S., Lassabliere, F., Charles, H. & Grenier, S. (2000) Addition of wsp sequences to the Wolbachia phylogenetic tree and stability of the classification. Journal of Molecular Evolution 51, 374377.Google Scholar
Rasgon, J.L. & Scott, T.W. (2003) Wolbachia and cytoplasmic incompatibility in the California Culex pipiens Mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics Society of America 165, 20292038.Google Scholar
Rasgon, J.L., Styer, L.M. & Scott, T.W. (2003) Wolbachia-induced mortality as a mechanism to modulate pathogen transmission by vector arthropods. Journal of Medical Entomology 40, 125132.Google Scholar
Ready, P.D. (2013) Biology of phlebotomine sandflies as vectors of disease agents. Annual Review of Entomology 58, 227250.Google Scholar
Rousset, F., Bouchon, D., Pintureau, B., Juchault, P. & Solignac, M. (1992) Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proceedings of the Royal Society of London B 250, 9198.Google Scholar
Saiful Islam, M. (2007) Wolbachia-mediated reproductive alterations in invertebrate hosts and biocontrol implications of the bacteria: an update. Rajshahi University Zoological Society 26, 119.Google Scholar
Shoemaker, D.D., Machado, C.A., Molbo, D., Werren, J.H., Windsor, D.M. & Herre, E.A. (2002) The distribution of Wolbachia in fig wasps: correlations with host phylogeny, ecology and population structure. Proceedings of the Royal Society of London B 269, 22572267.Google Scholar
Siozios, S., Loannidis, P., Lisa, K., Andersson, S.G.E. & Braig, H.R. (2013) The diversity and evolution of Wolbachia ankyrin repeat domain genes. PLoS ONE 8 (2), e55390.Google Scholar
Tamura, K., Dudley, J., Nei, M. & Kamur, S. (2007) Molecular evolutionary genetic analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.Google Scholar
Tanaka, K., Furukawa, S., Nikoh, N., Sasaki, T. & Fukatsu, T. (2009) Complete WO phage sequences reveal their dynamic evolutionary trajectories and putative functional elements required for integration into the Wolbachia genome. Applied and Environmental Microbiology 75, 56765686.Google Scholar
Theodor, O. & Mesghali, A. (1964) On the phlebotominae of Iran. Journal of Medical Entomology 1, 285300.Google Scholar
Turelli, M. & Hoffmann, A.A. (1999) Microbe-induced cytoplasmic incompatibility as a mechanism for introducing transgenes into arthropod populations. Insect Molecular Biology 8, 243255.Google Scholar
Van Meer, M.M.M., Witteveldt, J. & Stouthamer, R. (1999) Phylogeny of the arthropod endosymbiont Wolbachia based on wsp gene. Insect Molecular Biology 8, 399408.CrossRefGoogle ScholarPubMed
Weeks, A.R., Reynolds, K.T. & Hoffmann, A.A. (2002) Wolbachia dynamics: what has (and has not) been demonstrated? Trends in Ecology and Evolution 17, 257262.Google Scholar
Werren, J.H. (1998) Wolbachia and speciation. pp. 245260 in Harvard, D. & Berlocher, S. (Eds) Endless Forms: Species and Speciation. Oxford, Oxford University Press.Google Scholar
Werren, J.H., Zhang, W. & Guo, L.R. (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proceeding of the Royal Society of London. B 261, 5563.Google ScholarPubMed
Werren, J.H., Baldo, L. & Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6, 741751.Google Scholar
Wu, K. & Hoy, M.A. (2012) Extended starvation reduced and eliminated Wolbachia, but not Cardinium, from Metaseiulus occidentalis females (Acari: Phytoseiidae): a need to reassess Wolbachia's status in this predatory mite? Journal of Invertebrate Pathology 109, 2026.Google Scholar
Zhou, W., Rousset, F. & O'Neill, S.L. (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society of London. Series B 265, 509515.CrossRefGoogle ScholarPubMed