Symbiosis of intracellular bacteria Wolbachia with insects: a hundred years of study summarized

   Wolbachia pipientis is an α-proteobacterium, which is a widespread intracellular symbiont in a number of Arthropoda and some Nematoda species. With insects, W. pipientis forms a symbiont-host system characterized by very close interactions between its components. The mutual effects of Wolbachia on the host and the host on Wolbachia are important biotic factors for both components of this symbiotic system. Wolbachia is able to affect both host reproduction and somatic organ function. Due to its prevalence among insects and a wide variety of both negative (cytoplasmic incompatibility and androcide are among the most well-known examples) and positive (increasing resistance to biotic and abiotic factors, providing vitamins and metabolites) effects on the host organism, Wolbachia is of great interest for both entomologists and microbiologists. The diversity of host phenotypes induced by Wolbachia provides a broad choice of evolutionary strategies (such as reproductive parasitism or mutually beneficial symbiont-host relationships) that it utilizes. The influence of Wolbachia is to be considered in the design of any experiment conducted on insects. The application of sequencing technologies has led to new approaches being created to study the existing relationships within the Wolbachia-insect system, but interpretation of the data obtained is challenging. Nevertheless, the prospects for the use of the whole-genome analysis data to study Wolbachia-host coevolution are beyond doubt. Ongoing projects to introduce Wolbachia strains, which provide antiviral host defense, into insect populations to control the spread of RNA-viruses are actively pursued, which could result in saving many human lives.

   The aim of this brief review is to summarize the data collected by scientists over the past hundred years of Wolbachia studies and the current understanding of its genetic diversity and mechanisms of interaction with the host, including those based on transcriptome analysis.

1. Adonyeva N.V., Efimov V.M., Gruntenko N.E. The effect of genotype combinations of Wolbachia and its Drosophila melanogaster host on fertility, developmental rate and heat stress resistance of flies. Insects. 2023;14(12):928. doi: 10.3390/insects14120928

2. Augustinos A.A., Santos-Garcia D., Dionyssopoulou E., Moreira M., Papapanagiotou A., Scarvelakis M., Doudoumis V., Ramos S., Aguiar A.F., Borges P.A.V., Khadem M., Latorre A., Tsiamis G., Bourtzis K. Detection and characterization of Wolbachia infections in natural populations of Aphids: is the hidden diversity fully unraveled? PLoS One. 2011;6(12):e28695. doi: 10.1371/journal.pone.0028695

3. Backert S., Meyer T.F. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol. 2006;9(2):207-217. doi: 10.1016/j.mib.2006.02.008

4. Baldo L., Bordenstein S.R., Wernegreen J.J., Werren J.H. Widespread recombination throughout Wolbachia genomes. Mol Biol Evol. 2006a;23:437-449. doi: 10.1093/molbev/msj049

5. Baldo L., Hotopp J.C.D., Jolley K.A., Bordenstein S.R., Biber S.A., Choudhury R.R., Hayashi C., Maiden M.C.J., Tettelin H., Werren J.H. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol. 2006b;72(11):7098-7110. doi: 10.1128/AEM.00731-06

6. Beckmann J.F., Ronau J.A., Hochstrasser M. A Wolbachia deubiquity-lating enzyme induces cytoplasmic incompatibility. Nat Microbiol. 2017;2:17007. doi: 10.1038/nmicrobiol.2017.7

7. Brownlie J.C., Cass B.N., Riegler M., Witsenburg J.J., Iturbe-Ormaetxe I., McGraw E.A., O’Neill S.L. Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipi­entis, during periods of nutritional stress. PLoS Pathog. 2009;5(4): e1000368. doi: 10.1371/journal.ppat.1000368

8. Burdina E.V., Gruntenko N.E. Physiological aspects of Wolbachia pipi­entis–Drosophila melanogaster relationship. J Evol Biochem Phys. 2022;58(2):303-317. doi: 10.1134/s0022093022020016

9. Burdina E.V., Bykov R.A., Menshanov P.N., Ilinsky Y.Y., Gruntenko N. Unique Wolbachia strain wMelPlus increases heat stress resistance in Drosophila melanogaster. Arch Insect Biochem Physiol. 2021; 106(4):e21776. doi: 10.1002/arch.21776

10. Bykov R.A., Yudina M.A., Gruntenko N.E., Zakharov I.K., Voloshina M.A., Melashchenko E.S., Danilova M.V., Mazunin I.O., Ilinsky Y.Y. Prevalence and genetic diversity of Wolbachia endosymbiont and mtDNA in Palearctic populations of Drosophila melanogaster. BMC Evol Biol. 2019;19(Suppl. 1):48. doi: 10.1186/s12862-019-1372-9

11. Chen H., Ronau J.A., Beckmann J.F., Hochstrasser M. A Wolbachia nuclease and its binding partner provide a distinct mechanism for cytoplasmic incompatibility. Proc Natl Acad Sci USA. 2019;116(44): 22314-22321. doi: 10.1073/pnas.1914571116

12. Cho K.O., Kim G.W., Lee O.K. Wolbachia bacteria reside in host Golgirelated vesicles whose position is regulated by polarity proteins. PLoS One. 2011;6(7):e22703. doi: 10.1371/journal.pone.0022703

13. Chrostek E., Teixeira L. Mutualism breakdown by amplification of Wolbachia genes. PLoS Biol. 2015;13(2):e1002065. doi: 10.1371/journal.pbio.1002065

14. Chrostek E., Teixeira L. Within host selection for faster replicating bacterial symbionts. PLoS One. 2018;13(1):e0191530. doi: 10.1371/journal.pone.0191530

15. Chrostek E., Marialva M.S.P., Esteves S.S., Weinert L.A., Martinez J., Jiggins F.M., Teixeira L. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: A phenotypic and phylogenomic analysis. PLoS Genet. 2013;9(12):e1003896. doi: 10.1371/journal.pgen.1003896

16. Creasey E.A., Isberg R.R. Maintenance of vacuole integrity by bacterial pathogens. Curr Opin Microbiol. 2014;17(1):46-52. doi: 10.1016/j.mib.2013.11.005

17. Currin-Ross D., Husdell L., Pierens G.K., Mok N.E., O’Neill S.L., Schirra H.J., Brownlie J.C. The metabolic response to infection with Wolbachia implicates the insulin/insulin-like-growth factor and hypoxia signaling pathways in Drosophila melanogaster. Front Ecol Evol. 2021;9:623561. doi: 10.3389/fevo.2021.623561

18. da Rocha Fernandes M., Martins R., Pessoa Costa E., Pacidônio E.C., Araujo de Abreu L., da Silva Vaz I. Jr., Moreira L.A., da Fonseca R.N., Logullo C. The modulation of the symbiont/host interaction between Wolbachia pipientis and Aedes fluviatilis embryos by glycogen metabolism. PLoS One. 2014;9(6):e98966. doi: 10.1371/journal.pone.0098966

19. De Felipe K.S., Pampou S., Jovanovic O.S., Pericone C.D., Ye S.F., Kalachikov S., Shuman H.A. Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J Bacteriol. 2005;187(22):7716-7726. doi: 10.1128/JB.187.22.7716-7726.2005

20. Dean M.D. A Wolbachia-associated fitness benefit depends on genetic background in Drosophila simulans. Proc Biol Sci. 2006;273(1592): 1415-1420. doi: 10.1098/rspb.2005.3453

21. Detcharoen M., Schilling M.P., Arthofer W., Schlick-Steiner B.C., Steiner F.M. Differential gene expression in Drosophila melanogaster and D. nigrosparsa infected with the same Wolbachia strain. Sci Rep. 2021;11(1):11336. doi: 10.1038/s41598-021-90857-5

22. Duarte E.H., Carvalho A., López-Madrigal S., Costa J., Teixeira L. Forward genetics in Wolbachia: regulation of Wolbachia proliferation by the amplification and deletion of an addictive genomic island. PLoS Genet. 2021;17(6):e1009612. doi: 10.1371/journal.pgen.1009612

23. Ferree P.M., Frydman H.M., Li J.M., Cao J., Wieschaus E., Sullivan W. Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog. 2005;1(2):0111-0124. doi: 10.1371/journal.ppat.0010014

24. Frantz S.I., Small C.M., Cresko W.A., Singh N.D. Ovarian transcriptional response to Wolbachia infection in D. melanogaster in the context of between-genotype variation in gene expression. G3. 2023;13(5):jkad047. doi: 10.1093/g3journal/jkad047

25. Fronzes R., Christie P.J., Waksman G. The structural biology of type IV secretion systems. Nat Rev Microbiol. 2009;7(10):703-714. doi: 10.1038/nrmicro2218

26. Fry A.J., Rand D.M. Wolbachia interactions that determine Drosophila melanogaster survival. Evolution. 2002;56(10):1976-1981. doi: 10.1111/j.0014-3820.2002.tb00123.x

27. Fry A.J., Palmer M.R., Rand D.M. Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity. 2004;93(4):379-389. doi: 10.1038/sj.hdy.6800514

28. Gill A.C., Darby A.C., Makepeace B.L. Iron necessity: the secret of Wolbachia’s success? PLoS Negl Trop Dis. 2014;8(10):e3224. doi: 10.1371/journal.pntd.0003224

29. Gruntenko N.E., Ilinsky Y.Y., Adonyeva N.V., Burdina E.V., Bykov R.A., Menshanov P.N., Rauschenbach I.Y. Various Wolba­chia genotypes differently influence host Drosophila dopamine metabolism and survival under heat stress conditions. BMC Evol Biol. 2017;17:252. doi: 10.1186/s12862-017-1104-y

30. Gruntenko N.E., Karpova E.K., Adonyeva N.V., Andreenkova O.V., Burdina E.V., Ilinsky Y.Y., Bykov R.A., Menshanov P.N., Rauschenbach I.Y. Drosophila female fertility and juvenile hormone metabolism depends on the type of Wolbachia infection. J Exp Biol. 2019;222(Pt. 4):jeb195347. doi: 10.1242/jeb.195347

31. Gruntenko N.E., Deryuzhenko M.A., Andreenkova O.V., Shishkina O.D., Bobrovskikh M.A., Shatskaya N.V., Vasiliev G.V. Drosophila melanogaster transcriptome response to different Wolbachia strains. Int J Mol Sci. 2023;24(24):17411. doi: 10.3390/ijms242417411

32. Gu X., Ross P.A., Rodriguez-Andres J., Robinson K.L., Yang Q., Lau M.J., Hoffmann A.A. A wMel Wolbachia variant in Aedes aegypti from field-collected Drosophila melanogaster with increased phenotypic stability under heat stress. Environ Microbiol. 2022;24(4):2119-2135. doi: 10.1111/1462-2920.15966

33. Hargitai D., Kenéz L., Al-Lami M., Szenczi G., Lőrincz P., Juhász G. Autophagy controls Wolbachia infection upon bacterial damage and in aging Drosophila. Front Cell Dev Biol. 2022;10:976882. doi: 10.3389/fcell.2022.976882

34. He Z., Zheng Y., Yu W.J., Fang Y., Mao B., Wang Y.F. How do Wol­bachia modify the Drosophila ovary? New evidences support the “titration-restitution” model for the mechanisms of Wolbachia-induced CI. BMC Genomics. 2019;20(1):608. doi: 10.1186/s12864-019-5977-6

35. Hedges L.M., Brownlie J.C., O’Neill S.L., Johnson K.N. Wolbachia and virus protection in insects. Science. 2008;322(5902):702. doi: 10.1126/science.1162418

36. Hertig M., Wolbach S.B. Studies on rickettsia-like micro-organisms in insects. J Med Res. 1924;44(3):329-374.7

37. Hilgenboecker K., Hammerstein P., Schlattmann P., Telschow A., Werren J.H. How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol Lett. 2008;281(2): 215-220. doi: 10.1111/j.1574-6968.2008.01110.x

38. Hoffmann A.A. Partial cytoplasmic incompatibility between two Australian populations of Drosophila melanogaster. Entomol Exp Appl. 1988;48(1):61-67. doi: 10.1111/j.1570-7458.1988.tb02299.x

39. Hoffmann A.A., Montgomery B.L., Popovici J., Iturbe-Ormaetxe I., Johnson P.H., Muzzi F., Greenfield M., Durkan M., Leong Y.S., Dong Y., Cook H., Axford J., Callahan A.G., Kenny N., Omodei C., McGraw E.A., Ryan P.A., Ritchie S.A., Turelli M., O’Neill S.L. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature. 2011;476(7361):454-459. doi: 10.1038/nature10356

40. Ikeya T., Broughton S., Alic N., Grandison R., Partridge L. The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc Biol Sci. 2009;276(1674):3799-3807. doi: 10.1098/rspb.2009.0778

41. Ilinsky Y. Coevolution of Drosophila melanogaster mtDNA and Wol­bachia genotypes. PLoS One. 2013;8(1):e54373. doi: 10.1371/journal.pone.0054373

42. Ilinsky Y.Y., Zakharov I.K. Cytoplasmic incompatibility in Drosophila melanogaster is caused by different Wolbachia genotypes. Russ J Genet Appl Res. 2011;1(5):458-462. doi: 10.1134/S2079059711020031

43. Ilinsky Y., Demenkova M., Bykov R., Bugrov A. Narrow genetic diversity of Wolbachia symbionts in acrididae grasshopper hosts (Insecta, Orthoptera). Int J Mol Sci. 2022;23(2):853. doi: 10.3390/ijms23020853

44. Jiménez N.E., Gerdtzen Z.P., Olivera-Nappa Á., Salgado J.C., Conca C. A systems biology approach for studying Wolbachia metabolism reveals points of interaction with its host in the context of arboviral infection. PLoS Negl Trop Dis. 2019;13(8):e0007678. doi: 10.1371/journal.pntd.0007678

45. Kamtchum-Tatuene J., Makepeace B.L., Benjamin L., Baylis M., Solomon T. The potential role of Wolbachia in controlling the transmission of emerging human arboviral infections. Curr Opin Infect Dis. 2017;30(1):108-116. doi: 10.1097/QCO.0000000000000342

46. Karpova E.K., Bobrovskikh M.A., Deryuzhenko M.A., Shishkina O.D., Gruntenko N.E. Wolbachia effect on Drosophila melanogaster lipid and carbohydrate metabolism. Insects. 2023;14(4):357. doi: 10.3390/insects14040357

47. Kaur R., Shropshire J.D., Cross K.L., Leigh B., Mansueto A.J., Stewart V., Bordenstein S.R., Bordenstein S.R. Living in the endosymbiotic world of Wolbachia: a centennial review. Cell Host Microbe. 2021;29(6):879-893. doi: 10.1016/j.chom.2021.03.006

48. Korenskaia A.E., Shishkina O.D., Klimenko A.I., Andreenkova O.V., Bobrovskikh M.A., Shatskaya N.V., Vasiliev G.V., Gruntenko N.E. New Wolbachia pipientis genotype increasing heat stress resistance of Drosophila melanogaster host is characterized by a large chromosomal inversion. Int J Mol Sci. 2022;23(24):16212. doi: 10.3390/ijms232416212

49. Kremer N., Voronin D., Charif D., Mavingui P., Mollereau B., Vavre F. Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog. 2009;5(10):e1000630. doi: 10.1371/journal.ppat.1000630

50. Kumar Y., Valdivia R.H. Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe. 2009;5(6):593-601. doi: 10.1016/j.chom.2009.05.014

51. Lassy C.W., Karr T.L. Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mech Dev. 1996;57(1):47-58. doi: 10.1016/0925-4773(96)00527-8

52. Laven H. Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature. 1967;216:383-384. doi: 10.1038/216383a0

53. LePage D., Bordenstein S.R. Wolbachia: can we save lives with a great pandemic? Trends Parasitol. 2013;29(8):385-393. doi: 10.1016/j.pt.2013.06.003

54. LePage D.P., Metcalf J.A., Bordenstein S.R., On J., Perlmutter J.I., Shropshire J.D., Layton E.M., Funkhouser-Jones L.J., Beckmann J.F., Bordenstein S.R. Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature. 2017;543(7644):243-247. doi: 10.1038/nature21391

55. Lindsey A.R.I. Sensing, signaling, and secretion : a review and analysis of systems for regulating host interaction in Wolbachia. Genes (Ba­sel). 2020;11(7):813. doi: 10.3390/genes11070813

56. Lindsey A.R.I., Bhattacharya T., Hardy R.W., Newton I.L.G. Wolbachia and virus alter the host transcriptome at the interface of nucleotide metabolism pathways. mBio. 2021;12(1):e03472-20. doi: 10.1128/mBio.03472-20

57. Lo N., Evans T.A. Phylogenetic diversity of the intracellular symbiont Wolbachia in termites. Mol Phylogenet Evol. 2007;44(1):461-466. doi: 10.1016/j.ympev.2006.10.028

58. Lo N., Paraskevopoulos C., Bourtzis K., O’Neill S.L., Werren J.H., Bordenstein S.R., Bandi C. Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int J Syst Evol Microbiol. 2007;57(3): 654-657. doi: 10.1099/ijs.0.64515-0

59. Luck A.N., Slatko B.E., Foster J.M. Removing the needle from the haystack: enrichment of Wolbachia endosymbiont transcripts from host nematode RNA by Cappable-seq™. PLoS One. 2017;12(3): e0173186. doi: 10.1371/journal.pone.0173186

60. Maistrenko O.M., Serga S.V., Vaiserman A.M., Kozeretska I.A. Longevity-modulating effects of symbiosis: insights from Drosophila–Wolbachia interaction. Biogerontology. 2016;17(5-6):785-803. doi: 10.1007/s10522-016-9653-9

61. Mateos M., Silva N.O., Ramirez P., Higareda-Alvear V.M., Aramayo R., Erickson J.W. Effect of heritable symbionts on maternally-derived embryo transcripts. Sci Rep. 2019;9(1):8847. doi: 10.1038/s41598-019-45371-0

62. Min K.-T., Benzer S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci USA. 1997;94(20):10792-10796. doi: 10.1073/pnas.94.20.10792

63. Moreira L.A., Iturbe-Ormaetxe I., Jeffery J.A., Lu G., Pyke A.T., Hedges L.M., Rocha B.C., Hall-Mendelin S., Day A., Riegler M., Hugo L.E., Johnson K.N., Kay B.H., McGraw E.A., van den Hurk A.F., Ryan P.A., O’Neill S.L. A Wolbachia symbiont in Aedes aegypti limits infection with Dengue, Chikungunya, and Plasmo­dium. Cell. 2009;139(7):1268-1278. doi: 10.1016/j.cell.2009.11.042

64. Moriyama M., Nikoh N., Hosokawa T., Fukatsu T. Riboflavin provisioning underlies Wolbachia’s fitness contribution to its insect host. mBio. 2015;6(6):e01732-15. doi: 10.1128/mBio.01732-15

65. Newton I.L.G., Rice D.W. The Jekyll and Hyde symbiont: could Wolbachia be a nutritional mutualist? J Bacteriol. 2020;202(4): e00589-19. doi: 10.1128/JB.00589-19

66. Nikoh N., Hosokawa T., Moriyama M., Oshima K., Hattori M., Fukatsu T. Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc Natl Acad Sci USA. 2014;111(28):10257-10262. doi: 10.1073/pnas.1409284111

67. Nunes M.D.S., Nolte V., Schlötterer C. Nonrandom Wolbachia infection status of Drosophila melanogaster strains with different mtDNA haplotypes. Mol Biol Evol. 2008;25(11):2493-2498. doi: 10.1093/molbev/msn199

68. O’Neill S.L., Pettigrew M.M., Sinkins S.P., Braig H.R., Andrea dis T.G., Tesh R.B. In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect Mol Biol. 1997;6(1):33-39. doi: 10.1046/j.1365-2583.1997.00157.x

69. Ote M., Ueyama M., Yamamoto D. Wolbachia protein TomO targets nanos mRNA and restores germ stem cells in Drosophila sex­lethal mutants. Curr Biol. 2016;26(17):2223-2232. doi: 10.1016/j.cub.2016.06.054

70. Pichon S., Bouchon D., Cordaux R., Chen L., Garrett R.A., Grève P. Conservation of the Type IV secretion system throughout Wolbachia evolution. Biochem Biophys Res Commun. 2009;385(4):557-562. doi: 10.1016/j.bbrc.2009.05.118

71. Pietri J.E., DeBruhl H., Sullivan W. The rich somatic life of Wolbachia. Microbiologyopen. 2016;5(6):923-936. doi: 10.1002/mbo3.390

72. Poinsot D., Charlat S., Merçot H. On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. BioEssays. 2003;25(3):259-265. doi: 10.1002/bies.10234

73. Porter J., Sullivan W. The cellular lives of Wolbachia. Nat Rev Microbiol. 2023;21(11):750-766. doi: 10.1038/s41579-023-00918-x

74. Rice D.W., Sheehan K.B., Newton I.L.G. Large-scale identification of Wolbachia pipientis effectors. Genome Biol Evol. 2017;9(7):1925-1937. doi: 10.1093/gbe/evx139

75. Riegler M., Sidhu M., Miller W.J., O’Neill S.L. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol. 2005;15(15):1428-1433. doi: 10.1016/j.cub.2005.06.069

76. Rohrscheib C.E., Bondy E., Josh P., Riegler M., Eyles D., van Swinderen B., Weible M.W., Brownlie J.C. Wolbachia influences the production of octopamine and affects Drosophila male aggression. Appl Environ Microbiol. 2015;81(14):4573-4580. doi: 10.1128/AEM.00573-15

77. Ros V.I.D., Fleming V.M., Feil E.J., Breeuwer J.A.J. How diverse is the genus Wolbachia? Multiple-gene sequencing reveals a putatively new Wolbachia supergroup recovered from spider mites (Acari: Tetranychidae). Appl Environ Microbiol. 2009;75(4):1036-1043. doi: 10.1128/AEM.01109-08

78. Ryan S.L., Saul G.B. 2^nd. Post-fertilization effect of incompatibility factors in Mormoniella. Mol Gen Genet. 1968;103(1):29-36. doi: 10.1007/BF00271154

79. Sheehan K.B., Martin M., Lesser C.F., Isberg R.R., Newton I.L.G. Identification and characterization of a candidate Wolbachia pipientis type IV effector that interacts with the actin cytoskeleton. mBio. 2016;7(4):e00622-16. doi: 10.1128/mBio.00622-16

80. Teixeira L., Ferreira Á., Ashburner M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 2008;6(12):2753-2763. doi: 10.1371/journal.pbio.1000002

81. Truitt A.M., Kapun M., Kaur R., Miller W.J. Wolbachia modifies thermal preference in Drosophila melanogaster. Environ Microbiol. 2019;21(9):3259-3268. doi: 10.1111/1462-2920.14347

82. Werren J.H. Biology of Wolbachia. Annu Rev Entomol. 1997;42:587-609. doi: 10.1146/annurev.ento.42.1.587

83. White P.M., Pietri J.E., Debec A., Russell S., Patel B., Sullivan W. Mechanisms of horizontal cell-to-cell transfer of Wolbachia spp. in Drosophila melanogaster. Appl Environ Microbiol. 2017;83(7): e03425-16. doi: 10.1128/AEM.03425-16

84. Wu M., Sun L.V., Vamathevan J., Riegler M., Deboy R., Brownlie J.C., McGraw E.A., Martin W., Esser C., Ahmadinejad N., Wiegand C., Madupu R., Beanan M.J., Brinkac L.M., Daugherty S.C., Durkin A.S., Kolonay J.F., Nelson W.C., Mohamoud Y., Lee P., Berry K., Young M.B., Utterback T., Weidman J., Nierman W.C., Paulsen I.T., Nelson K.E., Tettelin H., O’Neill S.L., Eisen J.A. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2004;2(3):E69. doi: 10.1371/journal.pbio.0020069

85. Yu X.-J., Walker D.H. The Order Rickettsiales. In: The Prokaryotes. Springer, 2006;493-528. doi: 10.1007/0-387-30745-1_20

86. Zhang H., Id Z.C., Qiao J., Zhong Z., Pan C. Metabolomics provide new insights into mechanisms of Wolbachia-induced paternal defects in Drosophila melanogaster. PLoS Pathog. 2021;17(8):e1009859. doi: 10.1371/journal.ppat.1009859

87. Zhou W., Rousset F., O’Neil S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci. 1998;265(1395):509-515. doi: 10.1098/rspb.1998.0324

88. Zug R., Hammerstein P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40 % of terrestrial arthropod species are infected. PLoS One. 2012;7(6):e38544. doi: 10.1371/journal.pone.0038544

89. Zug R., Hammerstein P. Wolbachia and the insect immune system: what reactive oxygen species can tell us about the mechanisms of Wolbachia-host interactions. Front Microbiol. 2015;6:1201. doi: 10.3389/fmicb.2015.01201