Wolbachia genetic similarity in different insect host species: Drosophila melanogaster and Yogyakarta’s (Indonesia) Aedes aegypti as a novel host




Abstract. Rovik A, Daniwijaya EW, Supriyati E, Rahayu A, Kumalawati DA, Saraswati U, Handayaningsih AE, Rachman MP, Oktriani R, Kurniasari I, Candrasari DS, Nurhayati I, Sholeh R, Arianto B, Tantowijoyo W, Ahmad RA, Utarini A, Arguni E. 2022. Wolbachia genetic similarity in different insect host species: Drosophila melanogaster and Yogyakarta’s (Indonesia) Aedes aegypti as a novel host. Biodiversitas 23: 2321-2328. Wolbachia naturally presents in a large number of insects and other arthropod species. The Wolbachia strain wMel from Drosophila melanogaster has been stably transinfected into Aedes aegypti where it stops the mosquito host from being infected with medically important arbovirus like dengue. Consequently, Ae. aegypti infected with wMel have been released in Indonesia as a public health intervention against dengue. This study genetically compared wMel from Yogya field-caught D. melanogaster and the wMel in stably transfected Ae. aegypti used for field releases in Yogyakarta, Indonesia. The genetic similarity between wMel Wolbachia was evaluated by sequencing of Wolbachia surface protein (wsp) gene and some polymorphic genomic regions of insertion sites (IS) and variable number tandem repeats (VNTR) loci. The sequence of the Wolbachia surface protein (wsp) gene was 100% identical between hosts. There is no insertion sequence among specimens. The insertion sequence IS-WD1310 was identical between wMel from both hosts and among other strains, as well as the IS-WD516/7. The VNTR-141 period was identical within wMel from both hosts and among other strains, the VNTR-105 as well. Wolbachia Yogya field-caught D. melanogaster and Wolbachia strain wMel present in Ae. aegypti used for bio-control of dengue were genetically identical. These findings provide beneficial understanding to answer the public attention on safety issues, especially on the genetic similarity between Wolbachia strain in the natural and transfected hosts of this novel technology for dengue control.


Afizah NA, Roziah A, Nazni WA, Lee HL. 2015. Detection of Wolbachia from field-collected Aedes albopictus Skuse in Malaysia. Indian Journal of Medical Research 142: 205-10. DOI: 10.4103/0971-5916.164259
Aliota MT, Peinado SA, Velez ID, Osorio JE. 2016. The wMel strain of Wolbachia reduces transmission of zika virus by Aedes aegypti. Scientific Reports 6: 28792. DOI: 10.1038/srep28792
Ant TH, Herd CS, Geoghegan V, Hoffmann AA, Sinkins SP. 2018. The Wolbachia strain wAu provides highly efficient virus transmission blocking in Aedes aegypti. PLoS Pathogens; 14(1): e1006815. DOI: 10.1371/journal.ppat.1006815
Bian G. Xu Y, Lu P, Xie Y, Xi Z. 2010. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathogens 6(4): e1000833. DOI: 10.1371/journal.ppat.1000833
Bian G, Joshi D, Dong Y, Lu P, Zhou G, Xi Z, et al. 2013. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340: 748-51. DOI: 10.1126/science.1236192
Bing X-L, Xia W-Q, Gui J-D, Yan G-H, Wang X-W, Liu SS. 2014. Diversity and evolution of the Wolbachia endosymbionts of Bemisia (Hemiptera: Aleyrodidae) whiteflies. Ecology and Evolution 4(13): 2714-37. DOI: 10.1002/ece3.1126
Blagrove MSC, Arias-Goeta C, Failloux A-B, Sinkin PS. 2012. Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus. PNAS 109: 255-60. DOI: 10.1073/pnas.1112021108
Blagrove MSC, Arias-Goeta C, Di-Genua C, Failloux A-B, Sinkin PS. 2013. A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits the Chikungunya virus. PLoS Neglected Tropical Diseases 7(3): e2152. DOI: 10.1371/journal.pntd.0002152
Calvitti M, Moretti R, Lampazzi E, Bellini R, Dobson SL. 2010. Characterization of a new Aedes albopictus (Diptera: Culicidae)-Wolbachia pipientis (Rickettsiales: Rickettsiaceae) symbiotic association generated by the artificial transfer of the wPip strain from Culex pipiens (Diptera: Culicidae). Journal of Medical Entomology 47(2): 179-87. DOI: 10.1603/me09140
Chrostek E, Teixeira, L. 2015. Mutualism breakdown by amplification of Wolbachia genes. PLoS Biology 13(2): e1002065. DOI: 10.1371/journal.pbio.1002065
Dedeine F, Ahrens M, Calcaterra L, Shoemaker DD. 2005. Social parasitism in fire ants (Solenopsis spp.): a potential mechanism for the interspecies transfer of Wolbachia. Molecular Ecology 14: 1543-48. DOI: 10.1111/j.1365-294X.2005.02499.x
Dobson SL, Marsland EJ, Veneti Z, Bourtzis K, O’Neill SL. 2002. Characterization of Wolbachia host cell range via the in vitro establishment of infections. Applied and Environmental Microbiology 68: 656-60. DOI: 10.1128/AEM.68.2.656-660.2002
Dutra HL, Rocha MN, Dias FB, Mansur SB, Caragata EP, Moreira LA. 2016. Wolbachia blocks currently circulating zika virus isolates in Brazilian Aedes aegypti mosquitoes. Cell Host Microbes 19: 771-4. DOI: 10.1016/j.chom.2016.04.021
Dyson EA, Kamath MK, Hurst GDD. 2002. Wolbachia infection associated with all-female broods in Hypolimnas bolina (Lepidoptera: Nymphalidae): evidence for horizontal transmission of a butterfly male killer. Heredity 88: 166-71. DOI: 10.1038/sj.hdy.6800021
Ferguson NM. Kien DTH, Clapham H, Aguas R, Trung VT, Chau TNB, et al. 2015. Modeling the impact on virus transmission of Wolbachia-mediated blocking of dengue virus infection of Aedes aegypti. Science 7(279): 279ra37. DOI: 10.1126/scitranslmed.3010370
Flores HA, Taneja de Bruyne J, O’Donnell TB, Tuyet Nhu V, Thi Giang N, Thi Xuan, et al. 2020. Multiple Wolbachia strains provide comparative levels of protection against dengue virus infection in Aedes aegypti. PLoS Pathogens 16(4): e1008433. DOI: 10.1371/journal.ppat.1008433
Fraser JE, De Bruyne JT, Iturbe-Ormaetxe I, Stepnell J, Burns RL, Flores HA, et al. 2017. Novel Wolbachia-transinfected Aedes aegypti mosquitoes possess diverse fitness and vector competence phenotypes. PLoS Pathogens 13(12): e1006751. DOI: 10.1371/journal.ppat.1006751
Frentiu FD, Zakir T, Walker T, Popovici J, Pyke AT, van den Hurk A, et al. 2014. Limited dengue virus replication in field-collected Aedes aegypti mosquitoes infected with Wolbachia. PLoS Neglected Tropical Disease 8(2): e2688. DOI: 10.1371/journal.pntd.0002688
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 Microbiology Letters 281: 215-20. DOI: 10.1111/j.1574-6968.2008.01110.x
Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, et al. 2011. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476: 454-7. DOI: 10.1038/nature10356
Hosokawa T, Koga R, Kikuchi Y, Meng X-Y, Fukatsu T. 2010. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proceeding of National Academy of Science USA 107: 769-74. DOI: 10.1073/pnas.0911476107
Hurst GD, Jiggins FM, Pomiankowski A. 2002. Which way to manipulate host reproduction? Wolbachia that cause cytoplasmic incompatibility is easily invaded by sex ratio-distorting mutants. American Naturalist 160(3): 360-73. DOI: 10.1086/341524
Ilinsky YY, Zakharov IK. 2011. Cytoplasmic incompatibility in Drosophila melanogaster is caused by different Wolbachia genotypes. Russian J Genetics Applied Research 1(5): 458-62. DOI: 10.17816/ecogen7211-18
Indriani C, Tantowijoyo W, Rancès E, Andari B, Prabowo E, Yusdi D, et al. 2020. Reduced dengue incidence following deployments of Wolbachia-infected Aedes aegypti in Yogyakarta, Indonesia: a quasi-experimental trial using controlled interrupted time series analysis. Gates Open Research 4: 50. DOI: 10.12688/gatesopenres.13122.1
Jin C, Ren X, Rasgon JL. 2009. The virulent Wolbachia strain wMelPop efficiently establishes somatic infections in the malaria vector Anopheles gambiae. Applied and Environmental Microbiology 75(10): 3373-6. DOI: 10.1128/AEM.00207-09
Kambris Z, Blagborough AM, Pinto SB, Blagrove MSC, Godfray HCJ, et al. 2010. Wolbachia stimulates immune gene expression and inhibits Plasmodium development in Anopheles gambiae. PLoS Pathogens 6(10): e1001143. DOI: 10.1371/journal.ppat.1001143
Kumalawati DA, Supriyati E, Rachman MP, Oktriani R, Kurniasari I, Candrasari DS, et al. 2020. Wolbachia infection prevalence as a common insect’s endosymbiont in the rural area of Yogyakarta, Indonesia. Biodiversitas 21(12): 5608-14. DOI: 10.13057/biodiv/d211216
McMeniman CJ, Lane AM, Fong AWC, Voronin DA, Iturbe-Ormaetxe I, Yamada R, et al. 2008. Host adaptation of a Wolbachia strain after long-term serial passage in mosquito cell lines. Applied and Environmental Microbiology 74(22): 6963-9. DOI: 10.1128/AEM.01038-08
McMeniman CJ, Lane RV, Cass BN, Fong AWC, Sidhu M, Wang YF, et al. 2009. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323(5910): 141-4. DOI: 10.1126/science.1165326
Moreira L, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, et al. 2009. A Wolbachia symbiont in Aedes aegypti infection with Dengue, Chikungunya, and Plasmodium. Cell 139: 1268-78. DOI: 10.1016/j.cell.2009.11.042
Morrow JL, Frommer M, Shearman DCA, Riegler M. 2014. Tropical tephritid fruit fly community with a high incidence of shared Wolbachia strains as a platform for horizontal transmission of symbionts. Environmental Microbiology 16(12): 3622-37. DOI: 10.1111/1462-2920.12382
Nazni WA, Hoffmann AA, Afizah AN, Cheong YL, Mancini MV, Golding N, et al. 2019. Establishment of Wolbachia strain wAlbB in Malaysian populations of Aedes aegypti for Dengue control. Current Biology 29: 4241-8. DOI: 10.1016/j.cub.2019.11.007
Rasgon JL, Scott TW. 2004. An initial survey for Wolbachia (Rickettsiales: Rickettsiaceae) infections in selected California mosquitoes (Diptera: Culicidae). Journal of Medical Entomology 41(2): 255-7. DOI: 10.1603/0022-2585-41.2.255
Riegler M, Sidhu M, Miller WJ, O’Neill SL. 2005. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Current Biology 15: 1428-33. DOI: 10.1016/j.cub.2005.06.069
Riegler M, Iturbe-Ormaetxe I, Woolfit M, Miller WJ, O'Neill SL. 2012. Tandem repeat markers as novel diagnostic tools for high-resolution fingerprinting of Wolbachia. BMC Microbiology 12(Suppl. 1): S12. DOI: 10.1186/1471-2180-12-S1-S12
Ryan PA, Turley AP, Wilson G, Hurst TP, Retzki K, Brown-Kenyon J, et al. 2019. Establishment of wMel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia. Gates Open Research 3: 1547. DOI: 10.12688/gatesopenres.13061.2
Schneider DI, Riegler M, Arthofer W, Mercot H, Stauffer C, Miller WJ. 2013. Uncovering Wolbachia diversity upon artificial host transfer. PLoS ONE 8(12): e82402. DOI: 10.1371/journal.pone.0082402
Starr DJ, Cline TW. 2002. A host-parasite interaction rescues Drosophila oogenesis defects. Nature 418(6893): 76-9. DOI: 10.1038/nature00843
Stevens L, Giordano R, Fialho RF. 2001. Male-killing, nematode infections, bacteriophage infection, and virulence of cytoplasmic bacteria in the genus Wolbachia. Annual Review of Ecology and Systematics 32(1): 519-45. DOI: 10.1146/annurev.ecolsys.32.081501.114132
Tantowijoyo W, Andari B, Arguni E, Budiwati N, Nurhayati I, Fitriana I, et al. 2020. Stable establishment of wMel Wolbachia in Aedes aegypti populations in Yogyakarta, Indonesia. PLoS Neglected Tropical Disease 4(4): e0008157. DOI: 10.1371/journal.pntd.0008157
Tram U, Ferree PM, Sullivan W. 2003. Identification of Wolbachia–host interacting factors through cytological analysis. Microbes Infection 5: 999-1011. DOI: 10.1016/s1286-4579(03)00192-8
Tsai K-H, Lien J-C, Huang C-G, Wu W-J, Chen W-J. 2004. Molecular (sub)-grouping of endosymbiont Wolbachia infection among mosquitoes of Taiwan. Journal of Medical Entomology 41(4): 0677-83. DOI: 10.1603/0022-2585-41.4.677
Utarini A, Indriani C, Ahmad RA, Tantowijoyo W, Arguni E, Ansari MR, et al. 2021. Efficacy of Wolbachia-infected mosquito deployments for the control of dengue. New England Journal of Medicine 384: 2177-86. DOI: 10.1056/NEJMoa2030243
Van den Hurk AF, Hall-Mendellin S, Pyke AT, Frentiu FD, McElroy K, Day A, et al. 2012. Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Neglected Tropical Disease 6(11): e1892. DOI: 10.1371/journal.pntd.0001892
Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, et al. 2011. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476(7361): 450-3. DOI: 10.1038/nature10355
Werren JH, Baldo L, Clark ME. 2008. Wolbachia: master manipulators of invertebrate biology. Nature Review of Microbiology 6(10): 741-51. DOI: 10.1038/nrmicro1969
Woolfit M, Iturbe-Ormaetxe I, Brownlie JC, Walker T, Riegler M, Seleznev A, et al. 2013. Genomic evolution of the pathogenic Wolbachia strain, wMelPop. Genome Biology Evolution 5(11): 2189-204. DOI: 10.1093/gbe/evt169
Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC, et al. 2004. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. Public Library of Science and Biology 2(3): 327-41. DOI: 10.1371/journal.pbio.0020069
Xi Z, Khoo CC, Dobson SL. 2005. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310(5746): 326-8. DOI: 10.1126/science.1117607
Zhao G-Z, Zhu T-R, Zeng Y, Zhu D-H. 2021. Wolbachia infection in six species of gall wasps and their parasitoids. Journal of Asia-Pacific Entomology 2: 21-5. DOI: 10.1016/j.aspen.2020.11.004
Zhou W, Rousset F, O’Neill SL. 1998. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceeding of Royal Society of London Biology 265: 509-15. DOI: 10.1098/rspb.1998.0324
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. DOI: 10.1371/JOURNAL.PONE.0038544

Most read articles by the same author(s)