Endosymbiont Bacteria in Acari

Year 2023, Volume: 10 Issue: 2, 445 - 455, 30.11.2023

Gizem Berber Sibel Yorulmaz

https://doi.org/10.35193/bseufbd.1212415

Abstract

Acari are a large and important phylum within the arthropoda. Ticks, spiders, and especially agricultural beneficial and harmful mite species are included in this group. All of these living groups play significant roles in nature. Endosymbiotic bacteria interact with living things in Acari. Endosymbiont bacteria cause various reproductive manipulations such as parthenogenesis, male killing, feminization, cytoplasmic incompatibility (CI) in arthropods. They also play a role in processes such as nutritional support, defense against natural enemies, and detoxification. Due to these effects on their hosts, the determination of endosymbiotic bacteria relationships, especially in medicinal and agricultural pest species, is important in terms of both biodiversity and determination of alternative control strategies against pests. The relationships between living things in Acari and endosymbiotic bacteria are mentioned in this review.

Keywords

Acari, Cytoplasmic Incompatibility, Endosymbiotic Bacteria

Acari’de Endosimbiyont Bakteriler

Abstract

Acari, arthropoda şubesi içerisinde sayıca fazla ve önemli bir grubu oluşturmaktadır. Bu grup içerisinde keneler, örümcekler ve özellikle tarımsal yararlı ile zararlı akar türleri bulunmaktadır. Tüm bu canlı grupları doğada önemli faaliyetlere sahiptir. Acari içerisinde yer alan canlılar endosimbiyotik bakteriler ile ilişki içerisindedir. Endosimbiyont bakteriler, eklembacaklılarda partenogenez, erkek öldürücülük, feminizasyon, sitoplazmik uyumsuzluk (CI) gibi çeşitli üreme manipülasyonlarına neden olmaktadırlar. Ayrıca besin desteği, doğal düşmanlara karşı savunma ve detoksifikasyon gibi süreçlerde rol almaktadırlar. Konukçularındaki bu etkileri nedeniyle özellikle de tıbbi ve tarımsal zararlı türlerde endosimbiyotik bakteri ilişkilerinin belirlenmesi hem biyolojik çeşitlilik hem de zararlılara karşı alternatif mücadele stratejilerinin belirlenmesi açısından önemlidir.Bu derlemede Acari içerisinde yer alan canlılar ile endosimbiyotik bakteriler arasındaki ilişkilerinden söz edilmiştir.

Keywords

Acari, endosimbiyont bakteri, sitoplazmik uyumsuzluk

References

• Zhang, Z.-Q. (2013). 'Phylum Athropoda. In: Zhang, Z.-Q. (Ed.) Animal Biodiversity: An Outline of Higher-level Classification and Survey of Taxonomic Richness (Addenda 2013)'. Zootaxa. 3703 (1), 17.
• Krantz, G.W. & Walter, D.E., Eds. (2009). A manual of acarology. 3rd ed Texas Tech University Press, Lubbock, Tex.
• Helle, W. & Sabelis, M.W. (1985). Spider mites: their biology, natural enemies and control. in: pp. 141–160.
• Gerson, U., Smiley, R.L., &Ochoa, R., (2003). Mites (acari) for pest control. 2nd ed. Blackwell Science, Oxford ; Malden, MA.
• Palyvos, N.E., Emmanouel, N.G., & Saitanis, C.J. (2008). Mites associated with stored products in Greece. Experimental and Applied Acarology. 44 (3), 213–226.
• Sapp, J. (1994). Evolution by Association: A History of Symbiosis. Oxford University Press, .
• Kumar, N., Anjana, N., & Anjana, G. (2022). Endosymbionts: A New Frontier in Insect Pest Management. in: Applied Entomology and Zoology, pp. 43–57.
• Brelsfoard, C. & Dobson, S. (2009). Wolbachia-based strategies to control insect pests and disease vectors. Asia Pac. J. Mol. Biol. Biotechnol. 17.
• Zug, R. & Hammerstein, P. (2012). Still a Host of Hosts for Wolbachia: Analysis of Recent Data Suggests That 40% of Terrestrial Arthropod Species Are Infected. PLoS ONE. 7 (6), e38544.
• Moran, N.A., McCutcheon, J.P., & Nakabachi, A. (2008). Genomics and Evolution of Heritable Bacterial Symbionts. Annual Review of Genetics. 42 (1), 165–190.
• Buchner, P. (1965) Endosymbiosis of animals with plant microorganisms.
• Hoy, M.A. & Jeyaprakash, A. (2008). Symbionts, including pathogens, of the predatory mite Metaseiulus occidentalis: current and future analysis methods. Experimental and Applied Acarology. 46 (1–4), 329–347.
• Schütte, C. & Dicke, M. (2009). Verified and potential pathogens of predatory mites (Acari: Phytoseiidae). in: J. Bruin, L.P.S. van der Geest (Eds.), Diseases of Mites and Ticks, Springer Netherlands, Dordrechtpp. 307–328.
• Werren, J.H. & O’Neill, S.L. (1997). The evolution of heritable symbionts.Influential passengers: inherited microorganisms and arthropod reproduction.1–41.
• Bandi, C., Dunn, A.M., Hurst, G.D.D., & Rigaud, T. (2001). Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends in Parasitology. 17 (2), 88–94.
• Ahmed, M.Z., Breinholt, J.W., & Kawahara, A.Y. (2016). Evidence for common horizontal transmission of Wolbachia among butterflies and moths. BMC Evolutionary Biology. 16 (1), 118.
• Brown, A.N. & Lloyd, V.K. (2015). Evidence for horizontal transfer of Wolbachia by a Drosophila mite. Experimental and Applied Acarology. 66 (3), 301–311.
• Kremer, N. & Huigens, M.E. (2011). Vertical and horizontal transmission drive bacterial invasion: NEWS AND VIEWS: PERSPECTIVE. Molecular Ecology. 20 (17), 3496–3498.
• Caspi-Fluger, A., Inbar, M., Mozes-Daube, N., Katzir, N., Portnoy, V., Belausov, E., et al. (2012). Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proceedings of the Royal Society B: Biological Sciences. 279 (1734), 1791–1796.
• Sintupachee, S., Milne, J.R., Poonchaisri, S., Baimai, V., & Kittayapong, P. (2006). Closely Related Wolbachia Strains within the Pumpkin Arthropod Community and the Potential for Horizontal Transmission via the Plant. Microbial Ecology. 51 (3), 294–301.
• Cordaux, R., Bouchon, D., & Grève, P. (2011). The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends in Genetics. 27 (8), 332–341.
• Dykstra, H.R., Weldon, S.R., Martinez, A.J., White, J.A., Hopper, K.R., Heimpel, G.E., et al. (2014). Factors Limiting the Spread of the Protective Symbiont Hamiltonella defensa in Aphis craccivora Aphids. Applied and Environmental Microbiology. 80 (18), 5818–5827.
• Rao, Q., Wang, S., Su, Y.-L., Bing, X.-L., Liu, S.-S., & Wang, X.-W. (2012). Draft Genome Sequence of “Candidatus Hamiltonella defensa,” an Endosymbiont of the Whitefly Bemisia tabaci. Journal of Bacteriology. 194 (13), 3558–3558.
• Majerus, T.M. & Majerus, M.E. (2010). Discovery and identification of a male-killing agent in the Japanese ladybird Propylea japonica (Coleoptera: Coccinellidae). BMC Evolutionary Biology. 10 (1).
• Duron, O., Bouchon, D., Boutin, S., Bellamy, L., Zhou, L., Engelstädter, J., et al. (2008). The diversity of reproductive parasites among arthropods: Wolbachiado not walk alone. BMC Biology. 6 (1).
• Duron, O., Binetruy, F., Noël, V., Cremaschi, J., McCoy, K.D., Arnathau, C., et al. (2017). Evolutionary changes in symbiont community structure in ticks. Molecular Ecology. 26 (11), 2905–2921.
• Weinert, L.A., Araujo-Jnr, E.V., Ahmed, M.Z., & Welch, J.J. (2015). The incidence of bacterial endosymbionts in terrestrial arthropods. Proceedings of the Royal Society B: Biological Sciences. 282 (1807), 20150249.
• Zhang, Y.-K., Chen, Y.-T., Yang, K., & Hong, X.-Y. (2016). A review of prevalence and phylogeny of the bacterial symbiont Cardinium in mites (subclass: Acari). Systematic and Applied Acarology. 21 (7), 978–990.
• Breeuwer, J.A.J. (1997). Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity. 79 (1), 41–47.
• Gotoh, T., Noda, H., & Hong, X.-Y. (2003). Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity. 91 (3), 208–216.
• Ros, V.I.D. & Breeuwer, J. a. J. (2009). The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity. 102 (4), 413–422.
• Zhang, Y., Sun, B., & Hong, X. (2014). Infection and reproductive effects of Wolbachia in the hawthorn spider mite, Amphitetranychus viennensis (Acarina: Tetranychidae). Acta Entomologica Sinica. 57 (8), 914–920.
• Zhao, J., Neher, D.A., Fu, S., Li, Z., & Wang, K. (2013). Non-target effects of herbicides on soil nematode assemblages. Pest Management Science. 69 (6), 679–684.
• Zhu, L.-Y., Zhang, K.-J., Zhang, Y.-K., Ge, C., Gotoh, T., & Hong, X.-Y. (2012). Wolbachia Strengthens Cardinium-Induced Cytoplasmic Incompatibility in the Spider Mite Tetranychus piercei McGregor. Current Microbiology. 65 (5), 516–523.
• Asimakis, E.D., Doudoumis, V., Hadapad, A.B., Hire, R.S., Batargias, C., Niu, C., et al. (2019). Detection and characterization of bacterial endosymbionts in Southeast Asian tephritid fruit fly populations. BMC Microbiology. 19 (S1),.
• Bourtzis, K. & Miller, T.A., Eds. (2003). Insect symbiosis. CRC Press, Boca Raton, Fla.
• Hancock, P.A., Sinkins, S.P., & Godfray, H.C.J. (2011). Strategies for Introducing Wolbachia to Reduce Transmission of Mosquito-Borne Diseases. PLoS Neglected Tropical Diseases. 5 (4), e1024.
• Madhav, M., Baker, D., Morgan, J.A.T., Asgari, S., & James, P. (2020). Wolbachia: A tool for livestock ectoparasite control. Veterinary Parasitology. 288, 109297.
• İpekdal, K. & Kaya, T. (2020). Screening stored wheat beetles for reproductive parasitic endosymbionts in central Turkey. Journal of Stored Products Research. 89, 101732.
• Xu, X., Ridland, P.M., Umina, P.A., Gill, A., Ross, P.A., Pirtle, E., et al. (2021). High Incidence of Related Wolbachia across Unrelated Leaf-Mining Diptera. Insects. 12 (9), 788.
• Kaya, T.&İpekdal, K. (2017). Türkiye’de Yayılış Gösteren Akdeniz Meyve Sineğinde, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), Cardinium Bakterisinin Taranması ve Tanımlanması. undefined. 1–77.
• Feldhaar, H. (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology. 36 (5), 533–543.
• Oliver, K.M., Smith, A.H., & Russell, J.A. (2014). Defensive symbiosis in the real world – advancing ecological studies of heritable, protective bacteria in aphids and beyond. Functional Ecology. 28 (2), 341–355.
• Correa, C.C. & Ballard, J.W.O. (2016). Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator. Frontiers in Ecology and Evolution. 3.
• Li, Y., Liu, X., & Guo, H. (2018). Variations in Endosymbiont Infection Between Buprofezin-Resistant and Susceptible Strains of Laodelphax striatellus (Fallén). Current Microbiology. 75 (6), 709–715.
• Weeks, A.R. & Stouthamer, R. (2004). Increased fecundity associated with infection by a Cytophaga –like intracellular bacterium in the predatory mite, Metaseiulus occidentalis. Proceedings of the Royal Society of London. Series B: Biological Sciences. 271 (suppl_4),.
• van der Kooi, C.J., Matthey-Doret, C., & Schwander, T. (2017). Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods. Evolution Letters. 1 (6), 304–316.
• Ma, W.-J. & Schwander, T. (2017). Patterns and mechanisms in instances of endosymbiont-induced parthenogenesis. Journal of Evolutionary Biology. 30 (5), 868–888.
• Tomassone, L., Portillo, A., Nováková, M., de Sousa, R., & Oteo, J.A. (2018). Neglected aspects of tick-borne rickettsioses. Parasites & Vectors. 11 (1), 263.
• Yang, K., Xie, K., Zhu, Y.-X., Huo, S.-M., Hoffmann, A., & Hong, X.-Y. (2020). Wolbachia dominate Spiroplasma in the co-infected spider mite Tetranychus truncatus. Insect Molecular Biology. 29 (1), 19–37.
• Zhao, D.-X., Zhang, X.-F., & Hong, X.-Y. (2013). Host-Symbiont Interactions in Spider Mite Tetranychus truncates Doubly Infected WithWolbachia and Cardinium. Environmental Entomology. 42 (3), 445–452.
• Duron, O. & Hurst, G.D. (2013). Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. BMC Biology. 11 (1), 45.
• Engelstädter, J. & Hurst, G.D. (2009). What use are male hosts? The dynamics of maternally inherited bacteria showing sexual transmission or male killing. The American Naturalist. 173 (5), E159–E170.
• Jeyaprakash, A. & Hoy, M.A. (2000). Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Molecular Biology. 9 (4), 393–405.
• Zchori-Fein, E. & Perlman, S.J. (2004). Distribution of the bacterial symbiont Cardinium in arthropods. Molecular Ecology. 13 (7), 2009–2016.
• Hurst, G.D.D., Johnson, A.P., Schulenburg, J.H.G. v d, & Fuyama, Y. (2000). Male-Killing Wolbachia in Drosophila: A Temperature-Sensitive Trait With a Threshold Bacterial Density. Genetics. 156 (2), 699–709.
• Fialho, R.F. & Stevens, L. (2000). Male-killing Wolbachia in a flour beetle. Proceedings of the Royal Society of London. Series B: Biological Sciences. 267 (1451), 1469–1473.
• Zeh, D.W., Zeh, J.A., & Bonilla, M.M. (2005). Wolbachia, sex ratio bias and apparent male killing in the harlequin beetle riding pseudoscorpion. Heredity. 95 (1), 41–49.
• Hurst, L.D. (1991). The incidences and evolution of cytoplasmic male killers. Proceedings of the Royal Society of London. Series B: Biological Sciences. 244 (1310), 91–99.
• McGraw, E.A. & O’Neill, S.L. (1999). Evolution of Wolbachia pipientis transmission dynamics in insects. Trends in Microbiology. 7 (7), 297–302.
• Markov, A.V. & Zakharov, I.A. (2005). Sexual Reproduction of Insects Is Regulated by Cytoplasmic Bacteria. Russian Journal of Developmental Biology. 36 (4), 230–239.
• Werren, J.H., Baldo, L., & Clark, M.E. (2008). Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology. 6 (10), 741–751.
• Werren, J.H. & Beukeboom, L.W. (1998). SEX DETERMINATION, SEX RATIOS, AND GENETIC CONFLICT. Annual Review of Ecology and Systematics. 29 (1), 233–261.
• Moret, Y., Juchault, P., & Rigaud, T. (2001). Wolbachia endosymbiont responsible for cytoplasmic incompatibility in a terrestrial crustacean: effects in natural and foreign hosts. Heredity. 86 (3), 325–332.
• Serbus, L.R., Casper-Lindley, C., Landmann, F., & Sullivan, W. (2008). The Genetics and Cell Biology of Wolbachia -Host Interactions. Annual Review of Genetics. 42 (1), 683–707.
• Takano, S., Tuda, M., Takasu, K., Furuya, N., Imamura, Y., Kim, S., et al. (2017). Unique clade of alphaproteobacterial endosymbionts induces complete cytoplasmic incompatibility in the coconut beetle. Proceedings of the National Academy of Sciences. 114 (23), 6110–6115.
• Penz, T., Schmitz-Esser, S., Kelly, S.E., Cass, B.N., Müller, A., Woyke, T., et al. (2012). Comparative Genomics Suggests an Independent Origin of Cytoplasmic Incompatibility in Cardinium hertigii. PLoS Genetics. 8 (10), e1003012. Doran, T. & Moore, R. (2001). Application of the reproductive parasite Wolbachia to the biological control of flystrike. In Proceedings of the FLICS Conference, Launcestan (pp. 4-6).
• Werren, J.H. (1997). BIOLOGY OF WOLBACHIA. Annual Review of Entomology. 42 (1), 587–609.
• Charlat, S. & Merçot, H. (2000). News and Comment Trends. Trends in Ecology and Evoluation 15 (11): 438. 440.
• Saridaki, A. & Bourtzis, K. (2010). Wolbachia: more than just a bug in insects genitals. Current Opinion in Microbiology. 13 (1), 67–72.
• Weeks, A.R., Marec, F., & Breeuwer, J.A.J. (2001). A Mite Species That Consists Entirely of Haploid Females. Science. 292 (5526), 2479–2482.
• Zchori-Fein, E., Faktor, O., Zeidan, M., Gottlieb, Y., Czosnek, H., & Rosen, D. (1995). Parthenogenesis-inducing microorganisms in Aphytis (Hymenoptera: Aphelinidae). Insect Molecular Biology. 4 (3), 173–178.
• Huigens, M.E. & Stouthamer, R. (2003). Parthenogenesis Associated with Wolbachia.Insect symbiosis, in: p. 247.
• Stouthamer, R. (1997). Wolbachia-induced parthenogenesis. Influential Passengers. Edited by: ONeill SL, Werren JH.
• Charlat, S., Hurst, G.D.D., & Merçot, H. (2003). Evolutionary consequences of Wolbachia infections. Trends in Genetics. 19 (4), 217–223.
• Scola, B., Bandi, C., & Raoult, D. (2005). Wolbachia Hertig 1936, 472 AL. in: D.J. Brenner, N.R. Krieg, G.M. Garrity, J.T. Staley, D.R. Boone, P. Vos, et al. (Eds.), Bergey’s Manual® of Systematic Bacteriology, Springer-Verlag, New Yorkpp. 138–143.
• Dewayne Shoemaker, 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. Series B: Biological Sciences. 269 (1506), 2257–2267.
• Lachowska, D., Kajtoch, Ł., & Knutelski, S. (2010). Occurrence of Wolbachia in central European weevils: correlations with host systematics, ecology, and biology. Entomologia Experimentalis et Applicata. 135 (1), 105–118.
• Enigl, M. & Schausberger, P. (2007). Incidence of the endosymbionts Wolbachia, Cardinium and Spiroplasma in phytoseiid mites and associated prey. Experimental and Applied Acarology. 42 75–85.
• Ros, V.I.D., Fleming, V.M., Feil, E.J., & Breeuwer, J.A.J. (2009). How Diverse Is the Genus Wolbachia ? Multiple-Gene Sequencing Reveals a Putatively New Wolbachia Supergroup Recovered from Spider Mites (Acari: Tetranychidae). Applied and Environmental Microbiology. 75 (4), 1036–1043.
• Gotoh, T., Sugasawa, J., Noda, H., & Kitashima, Y. (2007). Wolbachia-induced cytoplasmic incompatibility in Japanese populations of Tetranychus urticae (Acari: Tetranychidae). Experimental and Applied Acarology. 42 (1), 1–16.
• Liu, Y., Miao, H., & Hong, X.-Y. (2006). Distribution of the endosymbiotic bacterium Cardinium in Chinese populations of the carmine spider mite Tetranychus cinnabarinus (Acari: Tetranychidae). Journal of Applied Entomology. 130 (9–10), 523–529.
• Ros, V.I., Fleming, V.M., Feil, E.J., & Breeuwer, J.A. (2012). Diversity and recombination in Wolbachia and Cardinium from Bryobiaspider mites. BMC Microbiology. 12 (1), 1–15.
• Suh, E., Sim, C., Park, J.-J., & Cho, K. (2015). Inter-population variation for Wolbachia induced reproductive incompatibility in the haplodiploid mite Tetranychus urticae. Experimental and Applied Acarology. 65 (1), 55–71.
• Xie, R.-R., Chen, X.-L., & Hong, X.-Y. (2011). Variable fitness and reproductive effects of Wolbachia infection in populations of the two-spotted spider mite Tetranychus urticae Koch in China. Applied Entomology and Zoology. 46 (1), 95–102.
• Zhang, Y.-K., Chen, Y.-T., Yang, K., Qiao, G.-X., & Hong, X.-Y. (2016). Screening of spider mites (Acari: Tetranychidae) for reproductive endosymbionts reveals links between co-infection and evolutionary history. Scientific Reports. 6 (1), 1–9.
• Zhu, Y.-X., Song, Y.-L., Zhang, Y.-K., Hoffmann, A.A., Zhou, J.-C., Sun, J.-T., et al. (2018). Incidence of Facultative Bacterial Endosymbionts in Spider Mites Associated with Local Environments and Host Plants. Applied and Environmental Microbiology. 84 (6), e02546-17.
• Bjørnson, S. (2008). Natural enemies of the convergent lady beetle, Hippodamia convergens Guérin-Méneville: their inadvertent importation and potential significance for augmentative biological control. Biological Control. 44 (3), 305–311.
• Van der Geest, L.P., Elliot, S.L., Breeuwer, J.A.J., & Beerling, E.A.M. (2000). Diseases of mites. Experimental & Applied Acarology. 24, 497–560.
• Johanowicz, D.L. & Hoy, M.A. (1998). The Manipulation of Arthropod Reproduction by Wolbachia Endosymbionts. The Florida Entomologist. 81 (3), 310.
• Erban, T., Klimov, P.B., Smrz, J., Phillips, T.W., Nesvorna, M., Kopecky, J., et al. (2016). Populations of Stored Product Mite Tyrophagus putrescentiae Differ in Their Bacterial Communities. Frontiers in Microbiology. 7, 1046.
• Chao, L.-L., Castillo, C.T., & Shih, C.-M. (2021). Molecular detection and genetic identification of Wolbachia endosymbiont in Rhipicephalus sanguineus (Acari: Ixodidae) ticks of Taiwan. Experimental and Applied Acarology. 83 (1), 115–130.
• Konecka, E., Olszanowski, Z., & Koczura, R. (2019). Wolbachia of phylogenetic supergroup E identified in oribatid mite Gustavia microcephala (Acari: Oribatida). Molecular Phylogenetics and Evolution. 135 230–235. Kurtti, T.J., Munderloh, U.G., Andreadis, T.G., Magnarelli, L.A., & Mather, T.N. (1996). Tick Cell Culture Isolation of an Intracellular Prokaryote from the TickIxodes scapularis. Journal of Invertebrate Pathology. 67 (3), 318–321.
• Nakamura, Y., Kawai, S., Yukuhiro, F., Ito, S., Gotoh, T., Kisimoto, R., et al. (2009). Prevalence of Cardinium Bacteria in Planthoppers and Spider Mites and Taxonomic Revision of “Candidatus Cardinium hertigii” Based on Detection of a New Cardinium Group from Biting Midges. Applied and Environmental Microbiology. 75 (21), 6757–6763.
• Weeks, A.R., Velten, R., & Stouthamer, R. (2003). Incidence of a new sexratiodistorting endosymbiotic bacterium among arthropods. Proceedings of the Royal Society of London. Series B: Biological Sciences. 270(1526), 1857-1865.
• Groot, T.V.M. & Breeuwer, J.A.J. (2006). Cardinium symbionts induce haploid thelytoky in most clones of three closely related Brevipalpus species. Experimental & Applied Acarology. 39 (3), 257–271.
• Chigira, A. & Miura, K. (2005). Detection of ‘Candidatus Cardinium’ Bacteria from the Haploid Host Brevipalpus Californicus (Acari: Tenuipalpidae) and Effect on the Host. Experimental & Applied Acarology. 37 (1), 107–116.
• Wu, K. & Hoy, M.A. (2012). Cardinium is associated with reproductive incompatibility in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae). Journal of Invertebrate Pathology. 110 (3), 359–365.
• Konecka, E. & Olszanowski, Z. (2019). A new Cardinium group of bacteria found in Achipteria coleoptrata (Acari: Oribatida). Molecular Phylogenetics and Evolution. 131, 64–71.
• Gasparich, G.E., Whitcomb, R.F., Dodge, D., French, F.E., Glass, J., and Williamson, D.L. (2004). The genus Spiroplasma and its non-helical descendants: phylogenetic classification, correlation with phenotype and roots of the Mycoplasma mycoides clade. International Journal of Systematic and Evolutionary Microbiology. 54 (3), 893–918.
• Bolaños, L., Servín-Garcidueñas, L., & Martínez-Romero, E. (2015). Arthropod-Spiroplasma relationship in the genomic era. FEMS Microbiology Ecology. 91.
• Frago, E., Mala, M., Weldegergis, B.T., Yang, C., McLean, A., Godfray, H.C.J., et al. (2017). Symbionts protect aphids from parasitic wasps by attenuating herbivore-induced plant volatiles. Nature Communications. 8 (1), 1860.
• Guidolin, A.S. and Cônsoli, F.L. (2018). Diversity of the most commonly reported facultative symbionts in two closely-related aphids with different host ranges. Neotropical Entomology. 47, 440–446.
• Heyworth, E.R. & Ferrari, J. (2015). A facultative endosymbiont in aphids can provide diverse ecological benefits. Journal of Evolutionary Biology. 28 (10), 1753–1760.
• Staudacher, H., Schimmel, B.C.J., Lamers, M.M., Wybouw, N., Groot, A.T., & Kant, M.R. (2017). Independent Effects of a Herbivore’s Bacterial Symbionts on Its Performance and Induced Plant Defences. International Journal of Molecular Sciences. 18 (1), 182.
• Gols, R., Schütte, C., Stouthamer, R., & Dicke, M. (2007). PCR-based identification of the pathogenic bacterium, Acaricomes phytoseiuli, in the biological control agent Phytoseiulus persimilis (Acari: Phytoseiidae). Biological Control. 42 (3), 316–325.
• Pekas, A., Palevsky, E., Sumner, J.C., Perotti, M.A., Nesvorna, M., & Hubert, J. (2017). Comparison of bacterial microbiota of the predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae) and its factitious prey Tyrophagus putrescentiae (Acari: Acaridae). Scientific Reports. 7 (1), 2.
• Bonnet, S.I., Binetruy, F., Hernández-Jarguín, A.M., & Duron, O. (2017). The tick microbiome: why non-pathogenic microorganisms matter in tick biology and pathogen transmission. Frontiers in Cellular and Infection Microbiology. 7, 236.
• TULLY, J.G., WHITCOMB, R.F., ROSE, D.L., & BOVÉ, J.M. (1982). Spiroplasma mirum, a new species from the rabbit tick (Haemaphysalis leporispalustris). International Journal of Systematic and Evolutionary Microbiology. 32 (1), 92–100.
• Tully, J.G., Rose, D.L., Yunker, C.E., Cory, J., Whitcomb, R.F., & Williamson, D.L. (1981). Helical mycoplasmas (spiroplasmas) from Ixodes ticks. Science. 212 (4498), 1043–1045.
• Bell-Sakyi, L., Palomar, A.M., & Kazimirova, M. (2015). Isolation and propagation of a Spiroplasma sp. from Slovakian Ixodes ricinus ticks in Ixodes spp. cell lines. Ticks and Tick-Borne Diseases. 6 (5), 601–606.
• Henning, K., Greiner-Fischer, S., Hotzel, H., Ebsen, M., & Theegarten, D. (2006). Isolation of Spiroplasma sp. from an Ixodes tick. International Journal of Medical Microbiology. 296, 157–161.
• Hornok, S., Meli, M.L., Perreten, A., Farkas, R., Willi, B., Beugnet, F., et al. (2010). Molecular investigation of hard ticks (Acari: Ixodidae) and fleas (Siphonaptera: Pulicidae) as potential vectors of rickettsial and mycoplasmal agents. Veterinary Microbiology. 140 (1), 98–104.
• Qiu, Y., Nakao, R., Ohnuma, A., Kawamori, F., & Sugimoto, C. (2014). Microbial population analysis of the salivary glands of ticks; a possible strategy for the surveillance of bacterial pathogens. PloS One. 9 (8), e103961.
• Taroura, S., Shimada, Y., Sakata, Y., Miyama, T., Hiraoka, H., Watanabe, M., et al. (2005). Detection of DNA of “Candidatus Mycoplasma haemominutum” and Spiroplasma sp. in Unfed Ticks Collected from Vegetation in Japan. Journal of Veterinary Medical Science. 67 (12), 1277–1279.
• Van Oosten, A.R., Duron, O., & Heylen, D.J.A. (2018). Sex ratios of the tick Ixodes arboricola are strongly female-biased, but there are no indications of sex-distorting bacteria. Ticks and Tick-Borne Diseases. 9 (2), 307–313.
• Jaenike, J., Polak, M., Fiskin, A., Helou, M., & Minhas, M. (2007). Interspecific transmission of endosymbiotic Spiroplasma by mites. Biology Letters. 3 (1), 23–25.
• Hubert, J., Erban, T., Kamler, M., Kopecky, J., Nesvorna, M., Hejdankova, S., et al. (2015). Bacteria detected in the honeybee parasitic mite Varroa destructor collected from beehive winter debris. Journal of Applied Microbiology. 119 (3), 640–654.
• Sutcu, M. & Somer, A. (2015). Riketsiyal Enfeksiyonlar. in: pp. 457–465.
• Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X.-Y., & Fukatsu, T. (2010). Wolbachia as a bacteriocyte-associated nutritional mutualist. Proceedings of the National Academy of Sciences. 107 (2), 769–774.
• Liu, X.-D. & Guo, H.-F. (2019). Importance of endosymbionts Wolbachia and Rickettsia in insect resistance development. Current Opinion in Insect Science. 33, 84–90.
• Perlman, S. J., Hunter, M. S., & Zchori-Fein, E. (2006) The emerging diversity of Rickettsia. Proceedings of the Royal Society B: Biological Sciences, 273(1598), 2097-2106.
• Stevens, L., Giordano, R., & Fialho, R.F. (2001). Male-killing, nematode infections, bacteriophage infection, and virulence of cytoplasmic bacteria in the genus Wolbachia. Annual Review of Ecology and Systematics. 32 (1), 519–545.
• Stouthamer, R., Breeuwer, J.A.J., & Hurst, G.D.D. (1999). Wolbachia Pipientis: Microbial Manipulator of Arthropod Reproduction. Annual Review of Microbiology. 53 (1), 71–102.
• Zélé, F., Santos, I., Olivieri, I., Weill, M., Duron, O., & Magalhães, S. (2018). Endosymbiont diversity and prevalence in herbivorous spider mite populations in South-Western Europe. FEMS Microbiology Ecology. 94 (4), fiy015.
• Raoult, D. & Roux, V. (1997). Rickettsioses as paradigms of new or emerging infectious diseases. Clinical Microbiology Reviews. 10 (4), 694–719.
• Azad, A.F. & Beard, C.B. (1998). Rickettsial pathogens and their arthropod vectors. Emerging Infectious Diseases. 4 (2), 179.