Research Article
Türkiye’de bal arısı ektoparaziti Varroa destructor’un endosimbiyotik bakterilerinin moleküler araştırması
Abstract
Varroa destructor, dünya genelinde bal arılarının (Apis mellifera L.) bir ektoparazit olarak kabul edilmekte ve arı kolonilerinin sürdürülebilirliği için ciddi bir tehdit oluşturmaktadır. Varroa akarlarının sindirim sistemi ve vücut dokularındaki bakteri topluluğu daha önceki çalışmalarda büyük ölçüde ortaya çıkarılmış olsa da, tespit edilen endosimbiyotik bakterilerin çeşitliliği ve yaygınlığı oldukça sınırlı kalmıştır. Bu çalışmada, Türkiye arıcılık kovanlarından toplanan çeşitli Varroa popülasyonlarında yaygın bulunan dört endosimbiyotik bakterinin (Wolbachia, Cardinium, Spiroplasma ve Rickettsia) varlığı araştırılmıştır. Örneklenen popülasyonların neredeyse yarısı en az bir endosimbiyotik bakteri ile enfekte bulunmuştur. Wolbachia endosimbiyotik bakterisi, altı popülasyonda tespit edilerek en yaygın cins olarak kaydedilmiş ve ardından üç popülasyonda bulunan Cardinium yer almıştır. Ayrıca, Spiroplasma ve Rickettsia endosimbiyotik bakterileri her biri bir örnekte tespit edilmiştir. Bu çalışma, Cardinium endosimbiyotik bakterisinin V. destructor’de ilk moleküler karakterizasyonunu sunmaktadır. Elde edilen 16S rDNA dizileri, NCBI veritabanında bulunan Brevipalpus papayensis'ten rapor edilen Cardinium dizisi ile %98.9'u ile benzerlik göstermektedir. Bu çalışma, Varroa akarlarında tespit edilen endosimbiyotik bakteri çeşitliliğinin genişlemesine katkı sunmaktadır. Varroa akarlarında bulunan endosimbiyotik bakterilerin çeşitliliği ve yaygınlığını anlamak, Varroa enfestasyonlarını kontrol etmek ve arı sağlığını iyileştirmek için hedefe yönelik kontrol stratejilerinin geliştirilmesine katkı sağlayacaktır.
References
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- FAOSTAT (2023) Livestock primary production. http://www.fao.org/faostat/en/#data/QL. (Accessed 15 Sep 2023)
- Traynor KS, Mondet F, de Miranda JR, Techer M, Kowallik V, Oddie MA, Chantawannakul P, McAfee A. Varroa destructor: a complex parasite, crippling honey bees worldwide. Trends Parasitol 2020;36(6):592–602
- Ramsey SD, Ochoa R, Bauchan G, Gulbronson C, Mowery JD, Cohen A, Lim D, Joklik J, Cicero JM, Ellis JD, Hawthorne D, vanEngelsdorp D Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc Natl Acad Sci USA 2019;116(5):1792–1801.
- Johnson RM, Huang ZY, Berenbaum MR. Role of detoxification in Varroa destructor (Acari: Var- roidae) tolerance of the miticide tau-fluvalinate. Int J Acarol 2010;36(1):1–6.
- Blacquière T, Altreuther G, Krieger KJ. Evaluation of the efficacy and safety of flumethrin 275 mg bee-hive strips (PolyVar Yellow®) against Varroa destructor in naturally infested honey bee colonies in a controlled study. Parasitol Res 2017;116(1):109–122
- Bogdanov S. Contaminants of bee products. Apidologie 2006;37(1):1–18.
- Koç N, İnak E, Jonckheere W, Van Leeuwen T. Genetic analysis and screening of pyrethroid resistance mutations in Varroa destructor populations from Turkey. Experimental and Applied Acarology 2021;84(2):433-444.
- Jang S, Kikuchi Y. Impact of the insect gut microbiota on ecol- ogy, evolution, and industry. Curr Opin Insect Sci 2020;41:33–39.
- Akman Gündüz E, Douglas AE. Symbiotic bacteria ena- ble insect to use a nutritionally inadequate diet. Proc Biol Sci 2009;276(1658):987–991.
- Kageyama D, Narita S, Watanabe M. Insect sex determination manipulated by their endosymbionts: incidences, mechanisms and implications. Insects 2012;3(1):161–199.
- Weiss B, Aksoy S. Microbiome influences on insect host vector competence. Trends Parasitol 2011;27(11):514–522.
- Brownlie JC, Johnson KN. Symbiont-mediated protection in insect hosts. Trends Microbiol 2009;17(8):348–354.
- Moran NA, McCutcheon JP, Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 2008;42:165– 190.
- Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C, Savakis C, Bourtzis K. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proceedings of the National Academy of Sciences 2004;101(42):15042-15045.
- Hubert J, Erban T, Kamler M et al. Bacteria detected in the honeybee parasitic mite Varroa destructor collected from beehive winter debris. J Appl Microbiol 2015;119:640–54.
- Glinski Z, Jarosz J. Serratia marcescens artificially contaminating brood and worker honey bees, contaminates the Varroa jacobsoni mite. J Apic Res 1990;29:107–111.
- Cornman RS, Schatz MC, Johnston JS et al. Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera. BMC Genomics 2010;11:1.
- Maddaloni M, Pascual DW. Isolation of oxalotrophic bacteria associated with Varroa destructor mites. Lett Appl Microbiol 2015;61:411–7.
- Pattabhiramaiah M, Brückner D, Reddy MS.. Horizontal transmission of Wolbachia in the honeybee subspecies Apis mellifera carnica and its ectoparasite Varroa destructor. International journal of environmental sciences 2011;2(2):514-523.
- Grau T, Brandt A, DeLeon S, Meixner MD, Strauß JF, Joop G, Telschow A. A comparison of Wolbachia infection frequencies in Varroa with prevalence of deformed wing virus. Journal of Insect Science 2017;17(3):72.
- Koç N, Nalbantoğlu S. Microbiome comparison of Dermanyssus gallinae populations from different farm rearing systems and the presence of common endosymbiotic bacteria at developmental stages. Parasitol Res 2023;122(1):227-235.
- Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in bioinformatics 2019;20(4):1160-1166.
- Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic acids research 2016;44(1):232-235.
- Kalyaanamoorthy S, Minh BQ, Wong TK, Von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature methods 2017;14(6):587-589.
- Sandionigi A, Vicario S, Prosdocimi EM, Galimberti A, Ferri E, Bruno A, Balech B, Mezzasalma V, Casiraghi M. Towards a better understanding of Apis mellifera and Varroa destructor microbiomes: introducing ‘phyloh’ as a novel phylogenetic diversity analysis tool. Mol Ecol Resour 2015;15:697–710.
- Hubert J, Kamler M, Nesvorna M, et al. Comparison of Varroa destructor and Worker Honeybee Microbiota Within Hives Indicates Shared Bacteria. Microb Ecol 2016;72:448-459.
- Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc R Soc B 2015;282:20150249.
- Werren J, Baldo L, Clark M. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008;6:741–751.
- Zchori-Fein E, Perlman SJ. Distribution of the bacterial sym- biont Cardinium in arthropods. Mol Ecol 2004;13:2009–2201.
- Hagimori T, Abe Y, Date S, Miura K. The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects. Curr Microbiol 2006;52:97–101.
- Cass BN, Himler AG, Bondy EC, Bergen JE, Fung SK, Kelly SE, et al. Conditional fitness benefits of the Rickettsia bacterial symbiont in an insect pest. Oecologia 2015;180:169–79.
- Liu TP, Ritter W. Morphology of some microorganisms associated with the female mite Varroa jacobsoni: a survey by electron microscopy. In: Needham GR, Page RE Jr, Delfinado-Baker M, Bowman CE (eds). Africanized honeybees and bee mites. Ellis Horwood: Chichester; 1988. p. 467-474.
- Gerth M, Wolf R, Bleidorn C. et al. Green lacewings (Neuroptera: Chrysopidae) are commonly associated with a diversity of rickettsial endosymbionts. Zoological Lett 2017;3:12.
- Jaenike J, Polak M, Fiskin A, Helou M, Minhas M. Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 2007;3:23–25.
- Schwarz RS, Teixeira EW, Tauber JP, Birke JM, Martins MF, Fonseca I, Evans JD. Honey bee colonies act as reservoirs for two Spiroplasma facultative symbionts and incur complex, multiyear infection dynamics. Microbiol Open 2014;3:341–355.
- Zheng H, Powell JE, Steele MI et al. Honeybee gut microbiota pro- motes host weight gain via bacterial metabolism and hormonal signaling. Proc Natl Acad Sci U S A 2017;201701819.
- Mouches C, Bove JM, Albisetti J. Pathogenicity of Spiroplasma apis and other spiroplasmas for honey-bees in southwestern France. Ann Microbiol (Inst Pasteur) 1984;135A:151–155.
- Gotoh T, Noda H, Ito S. Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 2007;98(1):13–20.
- Jeyaprakash A, Hoy MA. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 2000;9(4):393–405.
- Montenegro H, Souza WN, Da Silva LD, Klaczko LB. Male- killing selfish cytoplasmic element causes sex-ratio distortion in Drosophila melanogaster. Heredity 2000;85(5):465–470.
- Osaka R, Ichizono T, Kageyama D, Nomura M, Watada M. Natural variation in population densities and vertical transmission rates of a Spiroplasma endosymbiont in Drosophila hydei. Symbiosis 2013;60(2):73–78.
- Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N, Kontsedalov S, Gershon M, Gal S, Katzir N, Zchori-Fein E. Identification and localization of a Rickettsia sp. in Bemisia tabaci (Hom- optera: Aleyrodidae). Appl Environ Microbiol 2006;72(5):3646–3652.
Molecular survey of endosymbiotic bacteria in the honeybee ectoparasite Varroa destructor in Türkiye
Abstract
Varroa destructor is recognized as the predominant ectoparasite affecting Western honey bees (Apis mellifera L.) globally, representing a significant threat to the sustainability of bee colonies. The bacterial community of the digestive system and body tissues of Varroa mites has been documented in previous studies, however, the diversity and prevalence of detected endosymbiotic bacteria remain limited. In this study, the existence of four commonly found endosymbiotic bacteria including Wolbachia, Cardinium, Spiroplasma, and Rickettsia was investigated in various Varroa mite populations collected from Turkish apiaries. Almost half of the sampled population was infected with at least one endosymbiotic bacteria. Wolbachia endosymbiont was detected as the most prevalent genus, observed in six populations followed by Cardinium present in three populations. Furthermore, Spiroplasma and Rickettsia endosymbionts were each detected in one sample. To our knowledge, this study provides the first molecular characterization of Cardinium endosymbionts in V. destructor. The identity of 16S rDNA sequences of Cardinium was 98.9% of the sequence of Cardinium reported from another mite species, Brevipalpus papayensis, in the NCBI database. The study contributes new insights into the endosymbiotic bacterial community of Varroa mites. Understanding the diversity and prevalence of endosymbiotic bacteria in Varroa mites could facilitate the development of targeted management strategies to control Varroa infestations and improve honeybee health.
Ethical Statement
Not applicable.
References
- Rosenkranz P, Aumeier P, Ziegelmann B. Biology and control of Varroa destructor. J Invertebr Pathol 2010;103:96-119.
- FAOSTAT (2023) Livestock primary production. http://www.fao.org/faostat/en/#data/QL. (Accessed 15 Sep 2023)
- Traynor KS, Mondet F, de Miranda JR, Techer M, Kowallik V, Oddie MA, Chantawannakul P, McAfee A. Varroa destructor: a complex parasite, crippling honey bees worldwide. Trends Parasitol 2020;36(6):592–602
- Ramsey SD, Ochoa R, Bauchan G, Gulbronson C, Mowery JD, Cohen A, Lim D, Joklik J, Cicero JM, Ellis JD, Hawthorne D, vanEngelsdorp D Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc Natl Acad Sci USA 2019;116(5):1792–1801.
- Johnson RM, Huang ZY, Berenbaum MR. Role of detoxification in Varroa destructor (Acari: Var- roidae) tolerance of the miticide tau-fluvalinate. Int J Acarol 2010;36(1):1–6.
- Blacquière T, Altreuther G, Krieger KJ. Evaluation of the efficacy and safety of flumethrin 275 mg bee-hive strips (PolyVar Yellow®) against Varroa destructor in naturally infested honey bee colonies in a controlled study. Parasitol Res 2017;116(1):109–122
- Bogdanov S. Contaminants of bee products. Apidologie 2006;37(1):1–18.
- Koç N, İnak E, Jonckheere W, Van Leeuwen T. Genetic analysis and screening of pyrethroid resistance mutations in Varroa destructor populations from Turkey. Experimental and Applied Acarology 2021;84(2):433-444.
- Jang S, Kikuchi Y. Impact of the insect gut microbiota on ecol- ogy, evolution, and industry. Curr Opin Insect Sci 2020;41:33–39.
- Akman Gündüz E, Douglas AE. Symbiotic bacteria ena- ble insect to use a nutritionally inadequate diet. Proc Biol Sci 2009;276(1658):987–991.
- Kageyama D, Narita S, Watanabe M. Insect sex determination manipulated by their endosymbionts: incidences, mechanisms and implications. Insects 2012;3(1):161–199.
- Weiss B, Aksoy S. Microbiome influences on insect host vector competence. Trends Parasitol 2011;27(11):514–522.
- Brownlie JC, Johnson KN. Symbiont-mediated protection in insect hosts. Trends Microbiol 2009;17(8):348–354.
- Moran NA, McCutcheon JP, Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 2008;42:165– 190.
- Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C, Savakis C, Bourtzis K. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proceedings of the National Academy of Sciences 2004;101(42):15042-15045.
- Hubert J, Erban T, Kamler M et al. Bacteria detected in the honeybee parasitic mite Varroa destructor collected from beehive winter debris. J Appl Microbiol 2015;119:640–54.
- Glinski Z, Jarosz J. Serratia marcescens artificially contaminating brood and worker honey bees, contaminates the Varroa jacobsoni mite. J Apic Res 1990;29:107–111.
- Cornman RS, Schatz MC, Johnston JS et al. Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera. BMC Genomics 2010;11:1.
- Maddaloni M, Pascual DW. Isolation of oxalotrophic bacteria associated with Varroa destructor mites. Lett Appl Microbiol 2015;61:411–7.
- Pattabhiramaiah M, Brückner D, Reddy MS.. Horizontal transmission of Wolbachia in the honeybee subspecies Apis mellifera carnica and its ectoparasite Varroa destructor. International journal of environmental sciences 2011;2(2):514-523.
- Grau T, Brandt A, DeLeon S, Meixner MD, Strauß JF, Joop G, Telschow A. A comparison of Wolbachia infection frequencies in Varroa with prevalence of deformed wing virus. Journal of Insect Science 2017;17(3):72.
- Koç N, Nalbantoğlu S. Microbiome comparison of Dermanyssus gallinae populations from different farm rearing systems and the presence of common endosymbiotic bacteria at developmental stages. Parasitol Res 2023;122(1):227-235.
- Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in bioinformatics 2019;20(4):1160-1166.
- Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic acids research 2016;44(1):232-235.
- Kalyaanamoorthy S, Minh BQ, Wong TK, Von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature methods 2017;14(6):587-589.
- Sandionigi A, Vicario S, Prosdocimi EM, Galimberti A, Ferri E, Bruno A, Balech B, Mezzasalma V, Casiraghi M. Towards a better understanding of Apis mellifera and Varroa destructor microbiomes: introducing ‘phyloh’ as a novel phylogenetic diversity analysis tool. Mol Ecol Resour 2015;15:697–710.
- Hubert J, Kamler M, Nesvorna M, et al. Comparison of Varroa destructor and Worker Honeybee Microbiota Within Hives Indicates Shared Bacteria. Microb Ecol 2016;72:448-459.
- Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc R Soc B 2015;282:20150249.
- Werren J, Baldo L, Clark M. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008;6:741–751.
- Zchori-Fein E, Perlman SJ. Distribution of the bacterial sym- biont Cardinium in arthropods. Mol Ecol 2004;13:2009–2201.
- Hagimori T, Abe Y, Date S, Miura K. The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects. Curr Microbiol 2006;52:97–101.
- Cass BN, Himler AG, Bondy EC, Bergen JE, Fung SK, Kelly SE, et al. Conditional fitness benefits of the Rickettsia bacterial symbiont in an insect pest. Oecologia 2015;180:169–79.
- Liu TP, Ritter W. Morphology of some microorganisms associated with the female mite Varroa jacobsoni: a survey by electron microscopy. In: Needham GR, Page RE Jr, Delfinado-Baker M, Bowman CE (eds). Africanized honeybees and bee mites. Ellis Horwood: Chichester; 1988. p. 467-474.
- Gerth M, Wolf R, Bleidorn C. et al. Green lacewings (Neuroptera: Chrysopidae) are commonly associated with a diversity of rickettsial endosymbionts. Zoological Lett 2017;3:12.
- Jaenike J, Polak M, Fiskin A, Helou M, Minhas M. Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 2007;3:23–25.
- Schwarz RS, Teixeira EW, Tauber JP, Birke JM, Martins MF, Fonseca I, Evans JD. Honey bee colonies act as reservoirs for two Spiroplasma facultative symbionts and incur complex, multiyear infection dynamics. Microbiol Open 2014;3:341–355.
- Zheng H, Powell JE, Steele MI et al. Honeybee gut microbiota pro- motes host weight gain via bacterial metabolism and hormonal signaling. Proc Natl Acad Sci U S A 2017;201701819.
- Mouches C, Bove JM, Albisetti J. Pathogenicity of Spiroplasma apis and other spiroplasmas for honey-bees in southwestern France. Ann Microbiol (Inst Pasteur) 1984;135A:151–155.
- Gotoh T, Noda H, Ito S. Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 2007;98(1):13–20.
- Jeyaprakash A, Hoy MA. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 2000;9(4):393–405.
- Montenegro H, Souza WN, Da Silva LD, Klaczko LB. Male- killing selfish cytoplasmic element causes sex-ratio distortion in Drosophila melanogaster. Heredity 2000;85(5):465–470.
- Osaka R, Ichizono T, Kageyama D, Nomura M, Watada M. Natural variation in population densities and vertical transmission rates of a Spiroplasma endosymbiont in Drosophila hydei. Symbiosis 2013;60(2):73–78.
- Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N, Kontsedalov S, Gershon M, Gal S, Katzir N, Zchori-Fein E. Identification and localization of a Rickettsia sp. in Bemisia tabaci (Hom- optera: Aleyrodidae). Appl Environ Microbiol 2006;72(5):3646–3652.
There are 43 citations in total.
Details
| Primary Language | English |
|---|---|
| Subjects | Veterinary Parasitology |
| Journal Section | RESEARCH ARTICLE |
| Authors | |
| Early Pub Date | January 12, 2024 |
| Publication Date | January 15, 2024 |
| Submission Date | September 19, 2023 |
| Acceptance Date | December 18, 2023 |
| Published in Issue | Year 2024 Volume: 95 Issue: 1 |
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