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Detection and molecular characterization of the Wolbachia Endobacteria in the Culex pipiens (Diptera: Culicidae) specimens collected from Kayseri province of Turkey

Year 2013, Volume: 60 Issue: 3, 189 - 194, 01.09.2013

Alparslan Yıldırım Abdullah Incı Onder Duzlu Zuhal Onder Arif Cıloglu

https://doi.org/10.1501/Vetfak_0000002577
Cited By: 7

Abstract

This study was performed to investigate Wolbachia endobacteria in Culex pipiens specimens collected from Kayseri province of Turkey. For this aim, totally 10 genomic DNA pools each including 6-15 Cx. pipiens specimens which were collected and identified within the scope of a project (No: 107O533) supported by TUBITAK, were examined by using the amplification of surface protein gene (wsp) region of the Wolbachia. The sequences from this gene were highly variable and could be used to resolve the phylogenetic relationships of different Wolbachia strains. After the genomic DNA extraction from the pools, PCR analyses were carried out with Wolbachia specific primer pair which was amplified a 590-632 bp region of the wsp gene. Out of 6 of the 10 examined genomic DNA pools were found to be positive (60.0%) by PCR analyses. The minimum infection rate of Wolbachia spp. in the totally analyzed 118 Cx. pipens specimens was determined as 5.08. One of the amplicon from the positive isolates was gel purified and sequenced in terms of wsp gene region of Wolbachia by using the same primers. Pair wise analyses of the obtained DNA sequences and multiple alignments with some other Wolbachia strains available in the GenBank were done and phylogenies were investigated. The obtained isolate (WolKys1) was deposited in GenBank International Nucleotide Sequence Database with the accession number JX474753. The phylogenetic analyses revealed that the obtained WolKys1 isolate belongs to Wolbachia Super Group B and wPIP group. According to the phylogenetic comparisons the WolKys1 showed 100.0% identity with some other Wolbachia isolates under the Group B. In conclusion, this study reports the first molecular detection and characterization of Wolbachia endobacteria in Cx. pipiens populations in Turkey

Keywords

Cx. pipiens molecular characterization Turkey Wolbachia

References

  • Almeida F, Moura AS, Cardoso AF, Winter CE, Tania Bijovsky A, Suesdek L (2011): Effects of Wolbachia on fitness of Culex quinquefasciatus (Diptera; Culicidae). Infect Genet Evol, 11, 2138-2143.
  • Arakaki N, Miyoshi T, Noda H (2001): Wolbachia- mediated parthenogenesis in the predatory thrips Franklinothripsvespiformis (Thysanoptera: Insecta). Proc R Soc Lond B Biol Sci, 268, 1011-1016.
  • Baldo L, Prendini L, Corthals A, Werren JH (2007): Wolbachia are present in southern African scorpions and cluster with supergroup F. Curr Microbiol, 55, 367-373.
  • Bandi C, Anderson TJ, Genchi C, Blaxter ML (1998): Phylogeny of Wolbachia in filarial nematodes. Proc R Soc, 265, 2407-2413.
  • Barr AR (1980): Cytoplasmic incompatibility in natural populations of a mosquito, Culex pipiens L. Nature, 283, 71-72.
  • Behbahani A (2012): Wolbachia infection and mitochondrial DNA comparisons among Culex mosquitoes in South West Iran. Pak J Biol Sci, 15, 54-57.
  • Bordenstein S, Rosengaus RB (2005): Discovery of a novel Wolbachia super group in Isoptera. Curr Microbiol, 51, 393-398.
  • Breeuwer JAJ, Stouthamer R, Burns DA, Pelletier DA, Weisburg WG, Werren JH (1992): Phylogeny of cytoplasmic cytoplasmic incompatibility microorganisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16s ribosomal DNA sequences. Insect Mol Biol, 1, 25-36.
  • Casiraghi M, Favia G, Cancrini G, Bartoloni A, Bandi C (2001): Molecular identification of Wolbachia from the filarial Nematode Mansonella ozzardi. Parasitol Res, 87, 417-420.
  • Casiraghi M, Bordenstein SR, Baldo L, Lo N, Beninati T, Wernegreen JJ, Werren JH, Bandi C (2005): Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiol, 151, 4015-4022.
  • Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstädter J, Hurst GD (2008): The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol, 6, 27.
  • Duron O, Raymond M, Weill M (2011): Many compatible Wolbachia strains coexist within natural populations of Culex pipiens mosquito. Heredity, 106, 986- 993.
  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011): Geneious v5.5, Available from http://www.geneious.com. (18.10.2011).
  • Fialho RF, Stevens L (1997): Molecular evidence for single Wolbachia infections among geographic strains of the flour beetle Tribolium confusum. Proc R Soc Lond B Biol Sci, 264, 1065-1068.
  • Fialho RF, Stevens L (2000): Male-killing Wolbachia in a flour beetle. Proc R Soc Lond B Biol Sci, 267, 1469-1474.
  • Goward CR, Scawen MD, Murphy JP, Atkinson T (1993): Molecular evolution of bacterial cell-surface proteins. Trends Biochem Sci, 18, 136-140.
  • Guz N, Kocak E, Akpınar E, Gurkan O, Kılıncer N (2012): Wolbachia infection in Trissolcus species (Hymenoptera: Scelionidae). Eur J Entomol, 109, 169-174.
  • Hertig M (1936): The rickettsia Wolbachia pipientis (gen. et. sp. n) and associated inclusions of the mosquito, Culex pipiens. Parasitol, 28, 453-486.
  • Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008): How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol Lett, 281, 215-220.
  • Hurst GDD, Jiggins FM, von der Schulenburg JHG, Bertrand D, West SA, Goriacheva II, Zakhrov IA, Werren JH, Stouthamer R, Majerus MEN (1999): Male-killingWolbachia in two species of insect. Proc R Soc Lond B Biol Sci, 266, 735-740.
  • Hurst GDD, Johnson AP, von der Schulenburg JHG, Fuyama Y (2000): Male-killing Wolbachia. Drosophila: a temperature sensitive trait with a threshold bacteria density. Genetics, 156, 699-709.
  • Lo N, Casiraghi M, Salati E, Bazzocchi C, Bandi C (2002): How many Wolbachia supergroups exist? Mol Biol Evol, 19, 341-346.
  • McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M, Wang YF, O’Neill SL (2009): Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science, 323, 141-144.
  • O’Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM (1992): 16srRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA, 89, 2699-2702.
  • Pidiyar VJ, Jangid K, Patole MS, Shouche YS (2003): Detection and phylogenetic affiliation of Wolbachia sp. from Indian mosquitoes Culex quinquefasciatus and Aedes albopictus. Curr Sci, 84, 1136-1139.
  • Rasgon JL, Scott TW (2003): Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics, 165, 2029- 2038.
  • Rasgon JL, Scott TW (2004): An initial survey for Wolbachia (Rickettsiales: Rickettsiaceae) infections in selected California mosquitoes (Diptera: Culicidae). J Med Entomol, 41, 255-257.
  • Ravikumar H, Ramachandraswamy N, Sampathkumar S, Prakash BM, Huchesh HC, Uday J, Puttaraju HP (2010): A preliminary survey for Wolbachia and bacteriophage WO infections in Indian mosquitoes (Diptera: Culicidae). Trop Biomed, 27, 384-393.
  • Rowley SM, Raven RJ, McGraw EA (2004): Wolbachia pipientis in Australian spiders. Curr Microbiol, 49, 208- 214.
  • Ruang-Areerate T, Kittayapong P (2006): Wolbachia trans infection in Aedes aegypti: A potential gene driver of dengue vectors. Proc Natl Acad Sci USA, 103, 12534- 12539.
  • Stouthamer R, Luck RF, Hamilton WD (1990): Antibiotics cause parthenogenetic Trichogramma to revert to sex. Proc Natl Acad Sci USA, 87, 2424-2427.
  • Stouthamer R, Breeuwer JAJ, Luck RF, Werren JH (1993): Molecular identification of microorganisms associated with parthenogenesis. Nature, 361, 66-68.
  • Sungpradit S, Nuchprayoon S (2010): Wolbachia of arthropods and filarial nematodes: biology and applications. Chula Med J, 54, 605-621.
  • Sunish IP, Rajendran R, Paramasivan R, Dhananjeyan KJ, Tyagi BK (2011): Wolbachia endobacteria in a natural population of Culex quinquefasciatus from filariasis endemic villages of South India and its phylogenetic implication. Trop Biomed, 28, 569-576.
  • Vandekerckhove TT, Watteyne S, Willems A, Swings JG, Mertens J, Gillis M (1999): Phylogenetic analysis of the 16S rDNA of the cytoplasmic bacterium Wolbachia from then ovel host Folsomia candida (Hexapoda, Collembola) and its implications for Wolbachial taxonomy. FEMS Microbiol Lett, 180, 279-286.
  • Werren JH (1997): Biology of Wolbachia. Annu Rev Entomol, 42, 587-609.
  • Werren JH, Windsor DM (2000): Wolbachia infection frequencies in insects:evidence of a global equilibrium? Proc R Soc Lond B, 267, 1277-1285.
  • Werren JH, Zhang W, Guo LR. (1995): Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc R Soc Lond B, 261, 55-63.
  • White BJ, Andrew DR, Mans NZ, Ohajuruka OA, Garvin MC (2006): West Nile virus in mosquitoes of northern Ohio, 2003. Am J Trop Med Hyg, 75, 346-349.
  • Xi Z, Khoo CC, Dobson SL (2005): Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science, 310, 326-328.
  • Yen JH, Barr AR (1971): New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature, 232, 657-658.
  • Yildirim A, Inci A, Duzlu O, Biskin Z, Ica A, Sahin I (2011): Aedes vexans and Culex pipiens as the potential vectors of Dirofilaria immitis in Central Turkey. Vet Parasitol 178,143-147.
  • Zhou W, Rousset F, O’Neill SL (1998): Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc R Soc Lond Ser B, 265, 509-515. Geliş tarihi: 14.02.2013 / Kabul tarihi: 27.03.2013 Address for correspondence: Doç. Dr. Alparslan Yıldırım Department of Parasitology, Faculty of Veterinary Medicine, Erciyes University, 38090 Melikgazi, Kayseri, Turkey e-mail: yildirima@erciyes.edu.tr

Kayseri yöresinden toplanmış Culex pipiens örneklerinde Wolbachia Endobakterisinin belirlenmesi ve moleküler karakterizasyonu

Year 2013, Volume: 60 Issue: 3, 189 - 194, 01.09.2013

Alparslan Yıldırım Abdullah Incı Onder Duzlu Zuhal Onder Arif Cıloglu

https://doi.org/10.1501/Vetfak_0000002577
Cited By: 7

Abstract

Bu çalışma, Kayseri yöresinden toplanmış Culex pipiens örneklerinde Wolbachia endobakterisini araştırmak amacıyla yapılmıştır. Bu amaçla TÜBİTAK tarafından desteklenen 107O533 kod no’lu araştırma projesi kapsamında, Kayseri yöresinden toplanmış, Cx. pipiens olarak identifiye edilmiş ve her birinde 6-15 adet C. pipiens türü içeren 10 adet genomik DNA havuzu materyal olarak belirlenmiştir. Genomik DNA havuzları Wolbachia yüzey protein (wsp) gen bölgesinin amplifikasyonu yönünden incelenmiştir. Bu gen bölgesinin sekansı yüksek değişkenlik göstermekte olup farklı Wolbachia suşları arasındaki filogenetik ilişkilerin analizinde kullanılabilmektedir. Havuzlardan genomik DNA ekstraksiyonunu takiben wsp gen bölgesinin 590-632 bp’lik kısmını amplifiye eden Wolbachia spesifik primerler ile PCR analizleri yapılmıştır. İncelenen 10 havuzun 6’sı (%60,0) PCR analizleriyle pozitif bulunmuştur. İncelenen toplam 118 Cx. pipiens türünde Wolbachia spp. ile minimum enfeksiyon oranı 5.08 olarak belirlenmiştir. Pozitif izolatlardan birine ait amplikon jel pürifiye edilmiş ve söz konusu gen bölgesi yönünden aynı primerler ile sekanslanmıştır. Elde edilen DNA dizisinin GenBank’ta mevcut diğer bazı Wolbachia suşları ile pairwise analizleri ve multiple alignmentları yapılarak filogenisi araştırılmıştır. Elde edilen izolat (WolKys1) JX474753 aksesyon numarası ile GenBank International Nucleotide Sequence Database’e kaydedilmiştir. Filogenetik analiz sonucu WolKys1 izolatının Wolbachia B süper grubu ve wPIP grubu içinde yer aldığı belirlenmiştir. Filogenetik kıyaslamalara göre WolKys1 izolatının B grubu altındaki diğer bazı Wolbachia izolatları ile %100 identiklik gösterdiği saptanmıştır. Sonuç olarak bu çalışma ile Türkiye’de ilk kez Cx. pipiens populasyonlarında Wolbachia endobakterisinin moleküler olarak belirlenmesi ve karakterizasyonu yapılmıştır

Keywords

Cx. pipiens moleküler karakterize Türkiye Wolbachia

References

  • Almeida F, Moura AS, Cardoso AF, Winter CE, Tania Bijovsky A, Suesdek L (2011): Effects of Wolbachia on fitness of Culex quinquefasciatus (Diptera; Culicidae). Infect Genet Evol, 11, 2138-2143.
  • Arakaki N, Miyoshi T, Noda H (2001): Wolbachia- mediated parthenogenesis in the predatory thrips Franklinothripsvespiformis (Thysanoptera: Insecta). Proc R Soc Lond B Biol Sci, 268, 1011-1016.
  • Baldo L, Prendini L, Corthals A, Werren JH (2007): Wolbachia are present in southern African scorpions and cluster with supergroup F. Curr Microbiol, 55, 367-373.
  • Bandi C, Anderson TJ, Genchi C, Blaxter ML (1998): Phylogeny of Wolbachia in filarial nematodes. Proc R Soc, 265, 2407-2413.
  • Barr AR (1980): Cytoplasmic incompatibility in natural populations of a mosquito, Culex pipiens L. Nature, 283, 71-72.
  • Behbahani A (2012): Wolbachia infection and mitochondrial DNA comparisons among Culex mosquitoes in South West Iran. Pak J Biol Sci, 15, 54-57.
  • Bordenstein S, Rosengaus RB (2005): Discovery of a novel Wolbachia super group in Isoptera. Curr Microbiol, 51, 393-398.
  • Breeuwer JAJ, Stouthamer R, Burns DA, Pelletier DA, Weisburg WG, Werren JH (1992): Phylogeny of cytoplasmic cytoplasmic incompatibility microorganisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16s ribosomal DNA sequences. Insect Mol Biol, 1, 25-36.
  • Casiraghi M, Favia G, Cancrini G, Bartoloni A, Bandi C (2001): Molecular identification of Wolbachia from the filarial Nematode Mansonella ozzardi. Parasitol Res, 87, 417-420.
  • Casiraghi M, Bordenstein SR, Baldo L, Lo N, Beninati T, Wernegreen JJ, Werren JH, Bandi C (2005): Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiol, 151, 4015-4022.
  • Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstädter J, Hurst GD (2008): The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol, 6, 27.
  • Duron O, Raymond M, Weill M (2011): Many compatible Wolbachia strains coexist within natural populations of Culex pipiens mosquito. Heredity, 106, 986- 993.
  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011): Geneious v5.5, Available from http://www.geneious.com. (18.10.2011).
  • Fialho RF, Stevens L (1997): Molecular evidence for single Wolbachia infections among geographic strains of the flour beetle Tribolium confusum. Proc R Soc Lond B Biol Sci, 264, 1065-1068.
  • Fialho RF, Stevens L (2000): Male-killing Wolbachia in a flour beetle. Proc R Soc Lond B Biol Sci, 267, 1469-1474.
  • Goward CR, Scawen MD, Murphy JP, Atkinson T (1993): Molecular evolution of bacterial cell-surface proteins. Trends Biochem Sci, 18, 136-140.
  • Guz N, Kocak E, Akpınar E, Gurkan O, Kılıncer N (2012): Wolbachia infection in Trissolcus species (Hymenoptera: Scelionidae). Eur J Entomol, 109, 169-174.
  • Hertig M (1936): The rickettsia Wolbachia pipientis (gen. et. sp. n) and associated inclusions of the mosquito, Culex pipiens. Parasitol, 28, 453-486.
  • Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008): How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol Lett, 281, 215-220.
  • Hurst GDD, Jiggins FM, von der Schulenburg JHG, Bertrand D, West SA, Goriacheva II, Zakhrov IA, Werren JH, Stouthamer R, Majerus MEN (1999): Male-killingWolbachia in two species of insect. Proc R Soc Lond B Biol Sci, 266, 735-740.
  • Hurst GDD, Johnson AP, von der Schulenburg JHG, Fuyama Y (2000): Male-killing Wolbachia. Drosophila: a temperature sensitive trait with a threshold bacteria density. Genetics, 156, 699-709.
  • Lo N, Casiraghi M, Salati E, Bazzocchi C, Bandi C (2002): How many Wolbachia supergroups exist? Mol Biol Evol, 19, 341-346.
  • McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M, Wang YF, O’Neill SL (2009): Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science, 323, 141-144.
  • O’Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM (1992): 16srRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA, 89, 2699-2702.
  • Pidiyar VJ, Jangid K, Patole MS, Shouche YS (2003): Detection and phylogenetic affiliation of Wolbachia sp. from Indian mosquitoes Culex quinquefasciatus and Aedes albopictus. Curr Sci, 84, 1136-1139.
  • Rasgon JL, Scott TW (2003): Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics, 165, 2029- 2038.
  • Rasgon JL, Scott TW (2004): An initial survey for Wolbachia (Rickettsiales: Rickettsiaceae) infections in selected California mosquitoes (Diptera: Culicidae). J Med Entomol, 41, 255-257.
  • Ravikumar H, Ramachandraswamy N, Sampathkumar S, Prakash BM, Huchesh HC, Uday J, Puttaraju HP (2010): A preliminary survey for Wolbachia and bacteriophage WO infections in Indian mosquitoes (Diptera: Culicidae). Trop Biomed, 27, 384-393.
  • Rowley SM, Raven RJ, McGraw EA (2004): Wolbachia pipientis in Australian spiders. Curr Microbiol, 49, 208- 214.
  • Ruang-Areerate T, Kittayapong P (2006): Wolbachia trans infection in Aedes aegypti: A potential gene driver of dengue vectors. Proc Natl Acad Sci USA, 103, 12534- 12539.
  • Stouthamer R, Luck RF, Hamilton WD (1990): Antibiotics cause parthenogenetic Trichogramma to revert to sex. Proc Natl Acad Sci USA, 87, 2424-2427.
  • Stouthamer R, Breeuwer JAJ, Luck RF, Werren JH (1993): Molecular identification of microorganisms associated with parthenogenesis. Nature, 361, 66-68.
  • Sungpradit S, Nuchprayoon S (2010): Wolbachia of arthropods and filarial nematodes: biology and applications. Chula Med J, 54, 605-621.
  • Sunish IP, Rajendran R, Paramasivan R, Dhananjeyan KJ, Tyagi BK (2011): Wolbachia endobacteria in a natural population of Culex quinquefasciatus from filariasis endemic villages of South India and its phylogenetic implication. Trop Biomed, 28, 569-576.
  • Vandekerckhove TT, Watteyne S, Willems A, Swings JG, Mertens J, Gillis M (1999): Phylogenetic analysis of the 16S rDNA of the cytoplasmic bacterium Wolbachia from then ovel host Folsomia candida (Hexapoda, Collembola) and its implications for Wolbachial taxonomy. FEMS Microbiol Lett, 180, 279-286.
  • Werren JH (1997): Biology of Wolbachia. Annu Rev Entomol, 42, 587-609.
  • Werren JH, Windsor DM (2000): Wolbachia infection frequencies in insects:evidence of a global equilibrium? Proc R Soc Lond B, 267, 1277-1285.
  • Werren JH, Zhang W, Guo LR. (1995): Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc R Soc Lond B, 261, 55-63.
  • White BJ, Andrew DR, Mans NZ, Ohajuruka OA, Garvin MC (2006): West Nile virus in mosquitoes of northern Ohio, 2003. Am J Trop Med Hyg, 75, 346-349.
  • Xi Z, Khoo CC, Dobson SL (2005): Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science, 310, 326-328.
  • Yen JH, Barr AR (1971): New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature, 232, 657-658.
  • Yildirim A, Inci A, Duzlu O, Biskin Z, Ica A, Sahin I (2011): Aedes vexans and Culex pipiens as the potential vectors of Dirofilaria immitis in Central Turkey. Vet Parasitol 178,143-147.
  • Zhou W, Rousset F, O’Neill SL (1998): Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc R Soc Lond Ser B, 265, 509-515. Geliş tarihi: 14.02.2013 / Kabul tarihi: 27.03.2013 Address for correspondence: Doç. Dr. Alparslan Yıldırım Department of Parasitology, Faculty of Veterinary Medicine, Erciyes University, 38090 Melikgazi, Kayseri, Turkey e-mail: yildirima@erciyes.edu.tr
There are 43 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Other ID JA36BP93KG
Journal Section Research Article
Authors

Alparslan Yıldırım

Abdullah Incı

Onder Duzlu

Zuhal Onder

Arif Cıloglu

Publication Date September 1, 2013
Published in Issue Year 2013Volume: 60 Issue: 3

Cite

APA Yıldırım, A., Incı, A., Duzlu, O., Onder, Z., et al. (2013). Detection and molecular characterization of the Wolbachia Endobacteria in the Culex pipiens (Diptera: Culicidae) specimens collected from Kayseri province of Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 60(3), 189-194. https://doi.org/10.1501/Vetfak_0000002577
AMA Yıldırım A, Incı A, Duzlu O, Onder Z, Cıloglu A. Detection and molecular characterization of the Wolbachia Endobacteria in the Culex pipiens (Diptera: Culicidae) specimens collected from Kayseri province of Turkey. Ankara Univ Vet Fak Derg. September 2013;60(3):189-194. doi:10.1501/Vetfak_0000002577
Chicago Yıldırım, Alparslan, Abdullah Incı, Onder Duzlu, Zuhal Onder, and Arif Cıloglu. “Detection and Molecular Characterization of the Wolbachia Endobacteria in the Culex Pipiens (Diptera: Culicidae) Specimens Collected from Kayseri Province of Turkey”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 60, no. 3 (September 2013): 189-94. https://doi.org/10.1501/Vetfak_0000002577.
EndNote Yıldırım A, Incı A, Duzlu O, Onder Z, Cıloglu A (September 1, 2013) Detection and molecular characterization of the Wolbachia Endobacteria in the Culex pipiens (Diptera: Culicidae) specimens collected from Kayseri province of Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi 60 3 189–194.
IEEE A. Yıldırım, A. Incı, O. Duzlu, Z. Onder, and A. Cıloglu, “Detection and molecular characterization of the Wolbachia Endobacteria in the Culex pipiens (Diptera: Culicidae) specimens collected from Kayseri province of Turkey”, Ankara Univ Vet Fak Derg, vol. 60, no. 3, pp. 189–194, 2013, doi: 10.1501/Vetfak_0000002577.
ISNAD Yıldırım, Alparslan et al. “Detection and Molecular Characterization of the Wolbachia Endobacteria in the Culex Pipiens (Diptera: Culicidae) Specimens Collected from Kayseri Province of Turkey”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 60/3 (September 2013), 189-194. https://doi.org/10.1501/Vetfak_0000002577.
JAMA Yıldırım A, Incı A, Duzlu O, Onder Z, Cıloglu A. Detection and molecular characterization of the Wolbachia Endobacteria in the Culex pipiens (Diptera: Culicidae) specimens collected from Kayseri province of Turkey. Ankara Univ Vet Fak Derg. 2013;60:189–194.
MLA Yıldırım, Alparslan et al. “Detection and Molecular Characterization of the Wolbachia Endobacteria in the Culex Pipiens (Diptera: Culicidae) Specimens Collected from Kayseri Province of Turkey”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 60, no. 3, 2013, pp. 189-94, doi:10.1501/Vetfak_0000002577.
Vancouver Yıldırım A, Incı A, Duzlu O, Onder Z, Cıloglu A. Detection and molecular characterization of the Wolbachia Endobacteria in the Culex pipiens (Diptera: Culicidae) specimens collected from Kayseri province of Turkey. Ankara Univ Vet Fak Derg. 2013;60(3):189-94.

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