Published May 10, 2024 | Version v1
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Bacterial community associated with Culex quinquefasciatus Say, 1823 (Diptera: Culicidae) from an urban area in the Amazon, Brazil

  • 1. Universidade de São Paulo, Faculdade de Saúde Pública, Departamento de Epidemiologia, São Paulo, SP, Brasil.

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Oliveira, Tatiane Marques Porangaba de, Sallum, Maria Anice Mureb, Silva, Herculano da (2024): Bacterial community associated with Culex quinquefasciatus Say, 1823 (Diptera: Culicidae) from an urban area in the Amazon, Brazil. Revista Brasileira de Entomologia (e20230079) 68 (1): 1-8, DOI: 10.1590/1806-9665-RBENT-2023-0079, URL: http://dx.doi.org/10.1590/1806-9665-rbent-2023-0079

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References

  • Akorli, E.A., Ubiaru, P.C., Pradhan, S., Akorli, J., Ranford-Cartwright, L., 2022. Bio-products from Serratia marcescens isolated from Ghanaian Anopheles gambiae reduce Plasmodium falciparum burden in vector mosquitoes. Front. Trop. Dis. 3, 979615. http:// dx.doi.org/10.3389/fitd.2022.979615.
  • Andersen, K.S., Kirkegaard, R.H., Karst, S.M., Albertsen, M., 2018.Ampvis2: an R package to analyse and visualise 16S rRNA amplicon data. bioRxiv. 1-2. http://dx.doi.org/10.1101/299537.
  • Ant, T.H., Herd, C., Louis, F., Failloux, A.B., Sinkins, S.P., 2020. Wolbachia transinfections in Culex quinquefasciatus generate cytoplasmic incompatibility.Insect Mol.Biol.29 (1), 1-8.http://dx.doi.org/10.1111/ imb.12604.
  • Arai, H., Lin, S.R., Nakai, M., Kunimi, Y., Inoue, M.N., 2020. Closely related male-killing and nonmale-killing Wolbachia strains in the oriental tea tortrix Homona magnanima. Microb. Ecol. 79 (4), 1011-1020. http://dx.doi.org/10.1007/s00248-019-01469-6.
  • Ayres, C.F.J., Guedes, D.R.D., Paiva, M.H.S., Morais-Sobral, M.C., Krokovsky, L., Machado, L.C., Melo-Santos, M.A.V., Crespo, M., Oliveira, C.M.F., Ribeiro, R.S., Cardoso, O.A., Menezes, A.L.B., Laperriere-Jr, R.C., Luna, C.F., Oliveira, A.L.S., Leal, W.S., Wallau, G.L., 2019.Zika virus detection, isolation and genome sequencing through Culicidae sampling during the epidemic in Vitoria, Espirito Santo, Brazil. Parasit. Vectors 12 (1), 220. http://dx.doi.org/10.1186/s13071-019-3461-4.
  • Baimai, V., Ahantarig, A., Trinachartvanit, W., 2021. Novel supergroup U Wolbachia in bat mites of Thailand. Southeast Asian J.Trop.52, 48-55.
  • Baldo, L., Lo, N., Werren, J.H., 2005. Mosaic nature of the Wolbachia surface protein. J. Bacteriol. 187 (15), 5406-5418. http://dx.doi. org/10.1128/JB.187.15.5406-5418.2005.
  • Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Abnet, C.C., Al- Ghalith, G.A., Alexander, H., Alm, E.J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J.E., Bittinger, K., Brejnrod, A., Brislawn, C.J., Brown, C.T., Callahan, B.J., Caraballo-Rodriguez, A.M., Chase, J., Cope, E.K., Da Silva, R., Diener, C., Dorrestein, P.C., Douglas, G.M., Durall, D.M., Duvallet, C., Edwardson, C.F., Ernst, M., Estaki, M., Fouquier,J., Gauglitz, J.M., Gibbons, S.M., Gibson, D.L., Gonzalez, A., Gorlick, K., Guo, J., Hillmann, B., Holmes, S., Holste, H., Huttenhower, C., Huttley, G. A., Janssen, S., Jarmusch, A.K., Jiang, L., Kaehler, B.D., Kang, K.B., Keefe, C.R., Keim, P., Kelley, S.T., Knights, D., Koester, I., Kosciolek, T., Kreps, J., Langille, M. G. I., Lee, J., Ley, R., Liu, Y. X., Loftfield, E., Lozupone, C., Maher, M., Marotz, C., Martin, B.D., McDonald, D., McIver, L.J., Melnik, A.V., Metcalf, J.L., Morgan, S.C., Morton, J.T., Naimey, A.T., Navas-Molina, J.A., Nothias, L.F., Orchanian, S.B., Pearson, T., Peoples, S.L., Petras, D., Preuss, M.L., Pruesse, E., Rasmussen, L.B., Rivers, A., Robeson 2nd, M. S., Rosenthal, P., Segata, N., Shaffer, M., Shiffer, A., Sinha, R., Song, S. J., Spear, J.R., Swafford, A.D., Thompson, L.R., Torres, P.J., Trinh, P., Tripathi, A., Turnbaugh, P.J., Ul-Hasan, S., van der Hooft, J.J.J., Vargas, F., Vazquez-Baeza, Y., Vogtmann, E., von Hippel, M., Walters, W., Wan, Y., Wang, M., Warren, J., Weber, K.C., Williamson, C.H.D., Willis, A.D., Xu, Z.Z., Zaneveld, J.R., Zhang, Y., Zhu, Q., Knight, R., Caporaso, J.G., 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol.37 (8), 852-857.http://dx.doi.org/10.1038/s41587- 019-0209-9.
  • Bongio, N.J., Lampe, D.J., 2015. Inhibition of Plasmodium berghei development in mosquitoes by effector proteins secreted from Asaia sp. bacteria using a novel native secretion signal. PLoS One 10 (12), e0143541.http://dx.doi.org/10.1371/journal.pone.0143541.
  • Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., Fierer, N., Knight, R., 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA 108 (Suppl. 1), 4516-4522. http://dx.doi. org/10.1073/pnas.1000080107.
  • Carvajal, T.M., Capistrano, J.D.R., Hashimoto, K., Go, K.J.D., Cruz, M.A.I.J., Martinez, M.J.L.B., Tiopianco, V.S. P., Amalin, D.M., Watanabe, K., 2018. Detection and distribution of Wolbachia endobacteria in Culex quinquefasciatus populations (Diptera: Culicidae) from Metropolitan Manila, Philippines. J. Vector Borne Dis. 55 (4), 265- 270. http://dx.doi.org/10.4103/0972-9062.256561.
  • Chavshin, A.R., Oshaghi, M.A., Vatandoost, H., Pourmand, M.R., Raeisi, A., Enayati, A.A., Mardani, N., Ghoorchian, S., 2012. Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: a step toward finding suitable paratransgenesis candidates. Acta Trop. 121 (2), 129-134. http:// dx.doi.org/10.1016/j.actatropica.2011.10.015.
  • Chen, K., Ponnusamy, L., Mouhamadou, C.S., Fodjo, B.K., Sadia, G.C., Affoue, F.P.K., Deguenon, J.M., Roe, R.M., 2022. Internal and external microbiota of home-caught Anopheles coluzzii (Diptera: Culicidae) from Cote d'Ivoire, Africa: mosquitoes are filthy. PLoS One 17 (12), e0278912. http://dx.doi.org/10.1371/journal.pone.0278912.
  • Consoli, R.A.G.B., Oliveira, R.L., 1994. Principais mosquitos de importancia sanitaria no Brasil. Editora FIOCRUZ, Rio de Janeiro, 228 p. http:// dx.doi.org/10.7476/9788575412909.
  • De Freece, C., Damiani, C., Valzano, M., D'Amelio, S., Cappelli, A., Ricci, I., Favia, G., 2014. Detection and isolation of the α -proteobacterium Asaia in Culex mosquitoes. Med. Vet. Entomol. 28 (4), 438-442. http://dx.doi.org/10.1111/mve.12045.
  • Dennison, N.J., Jupatanakul, N., Dimopoulos, G., 2014. The mosquito microbiota influences vector competence for human pathogens. Curr. Opin. Insect Sci. 3, 6-13. http://dx.doi.org/10.1016/j.cois.2014.07.004.
  • Favia, G., Ricci, I., Damiani, C., Raddadi, N., Crotti, E., Marzorati, M., Rizzi, A., Urso, R., Brusetti, L., Borin, S., Mora, D., Scuppa, P., Pasqualini, L., Clementi, E., Genchi, M., Corona, S., Negri, I., Grandi, G., Alma, A., Kramer, L., Esposito, F., Bandi, C., Sacchi, L., Daffonchio, D., 2007. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc. Natl. Acad. Sci. USA 104 (21), 9047-9051.http://dx.doi.org/10.1073/pnas.0610451104.
  • Forattini, O.P., 2002. Especie de Culex (Culex) In: Forattini OP, editor. Culicidologia Medica. Editora Universidade de Sao Paulo, Sao Paulo, pp. 693-722.
  • Fraser, J.E., O'Donnell, T.B., Duyvestyn, J.M., O'Neill, S.L., Simmons, C.P., Flores, H.A., 2020. Novel phenotype of Wolbachia strain wPip in Aedes aegypti challenges assumptions on mechanisms of Wolbachiamediated dengue virus inhibition. PLoS Pathog. 16 (7), e1008410. http://dx.doi.org/10.1371/journal.ppat.1008410.
  • Gao, H., Cui, C., Wang, L., Jacobs-Lorena, M., Wang, S., 2020. Mosquito microbiota and implications for disease control. Trends Parasitol. 36 (2), 98-111. http://dx.doi.org/10.1016/j.pt.2019.12.001.
  • Goncalves, G.G.A., Feitosa, A.P.S., Portela-Junior, N.C., Oliveira, C.M.F., Lima Filho, J.L.L., Brayner, F.A., Alves, L.C., 2019. Use of MALDI-TOF MS to identify the culturable midgut microbiota of laboratory and wild mosquitoes. Acta Trop.200, 105174.http://dx.doi.org/10.1016/j. actatropica.2019.105174.
  • Guedes, D.R., Paiva, M.H., Donato, M.M., Barbosa, P.P., Krokovsky, L., Rocha, S.W.D.S., Saraiva, K., Crespo, M.M., Rezende, T.M., Wallau, G.L., Barbosa, R.M., Oliveira, C.M., Melo-Santos, M.A., Pena, L., Cordeiro, M.T., Franca, R.F.O., Oliveira, A.L., Peixoto, C.A., Leal, W.S., Ayres, C.F., 2017. Zika virus replication in the mosquito Culex quinquefasciatus in Brazil.Emerg. Microbes Infect. 6 (8), e69.http:// dx.doi.org/10.1038/emi.2017.59.
  • Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A., Werren, J.H., 2008.How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol. Lett. 281 (2), 215-220. http://dx.doi.org/10.1111/j.1574-6968.2008.01110.x.
  • Huang, W., Rodrigues, J., Bilgo, E., Tormo, J.R., Challenger, J.D., De Cozar-Gallardo, C., Perez-Victoria, I., Reyes, F., Castaneda-Casado, P., Gnambani, E.J., Hien, D.F.S., Konkobo, M., Urones, B., Coppens, I., Mendoza-Losana, A., Ballell, L., Diabate, A., Churcher, T.S., Jacobs-Lorena, M., 2023. Delftia tsuruhatensis TC1 symbiont suppresses malaria transmission by anopheline mosquitoes. Science 381 (6657), 533-540. http://dx.doi.org/10.1126/science.adf8141.
  • Jeyaprakash, A., Hoy, M.A., 2000. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol. Biol. 9 (4), 393-405. http://dx.doi. org/10.1046/j.1365-2583.2000.00203.x.
  • Jupatanakul, N., Pengon, J., Selisana, S.M.G., Choksawangkarn, W., Jaito, N., Saeung, A., Bunyong, R., Posayapisit, N., Thammatinna, K., Kalpongnukul, N., Aupalee, K., Pisitkun, T., Kamchonwongpaisan, S., 2020. Serratia marcescens secretes proteases and chitinases with larvicidal activity against Anopheles dirus. Acta Trop. 212, 105686. http://dx.doi.org/10.1016/j.actatropica.2020.105686.
  • Lo, N., Paraskevopoulos, C., Bourtzis, K., O'Neill, S.L., Werren, J.H., Bordenstein, S.R., Bandi, C., 2007.Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int. J. Syst. Evol. Microbiol. 57 (Pt 3), 654-657. http://dx.doi.org/10.1099/ijs.0.64515-0.
  • Lopes, R.P., Lima, J.B.P., Martins, A.J., 2019. Insecticide resistance in Culex quinquefasciatus Say, 1823 in Brazil: a review. Parasit. Vectors 12 (1), 591. http://dx.doi.org/10.1186/s13071-019-3850-8.
  • Lourenco-de-Oliveira, R., Marques, J.T., Sreenu, V.B., Atyame Nten, C., Aguiar, E.R.G.R., Varjak, M., Kohl, A., Failloux, A.B., 2018. Culex quinquefasciatus mosquitoes do not support replication of Zika virus. J. Gen. Virol. 99 (2), 258-264.http://dx.doi.org/10.1099/jgv.0.000949.
  • Mago c, T., Salzberg, S.L., 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinform.27 (21), 2957-2963. http://dx.doi.org/10.1093/bioinformatics/btr507.
  • Mancini, M.V., Spaccapelo, R., Damiani, C., Accoti, A., Tallarita, M., Petraglia, E., Rossi, P., Cappelli, A., Capone, A., Peruzzi, G., Valzano, M., Picciolini, M., Diabate, A., Facchinelli, L., Ricci, I., Favia, G., 2016. Paratransgenesis to control malaria vectors: a semi-field pilot study. Parasit. Vectors 9 (1), 140. http://dx.doi.org/10.1186/ s13071-016-1427-3.
  • Minard, G., Tran, F.H., Raharimalala, F.N., Hellard, E., Ravelonandro, P., Mavingui, P., Valiente Moro, C., 2013. Prevalence, genomic and metabolic profiles of Acinetobacter and Asaia associated with field-caught Aedes albopictus from Madagascar. FEMS Microbiol. Ecol. 83 (1), 63-73. http://dx.doi.org/10.1111/j.1574-6941.2012.01455.x.
  • Ministerio da Saude. Secretaria de Vigilancia em Saude. Secretaria de Vigilancia em Saude. Departamento de Vigilancia Epidemiologica, 2011.Guia de vigilancia do Culex quinquefasciatus. 3ª ed. Ministerio da Saude, Brasilia, 76 p. (Serie A. Normas e manuais tecnicos).
  • Morais, S.A., Almeida, F.D., Suesdek, L., Marrelli, M.T., 2012.Low genetic diversity in Wolbachia-Infected Culex quinquefasciatus (Diptera: Culicidae) from Brazil and Argentina. Rev. Inst. Med. Trop. 54 (6), 325-329. https://doi.org/10.1590/s0036-46652012000600007.
  • Murray, K.O., Mertens, E., Despres, P., 2010. West Nile virus and its emergence in the United States of America. Vet. Res. 41 (6), 67. http://dx.doi.org/10.1051/vetres/2010039.
  • Nourani, L., Raz, A., Djadid, N.D., 2023. Isolation and identification of microbiota of Culex quinquefasciatus for their application as paratransgenic tools in vector control. Iran. J. Microbiol. 15 (2), 258-266. http://dx.doi.org/10.18502/ijm.v15i2.12478.
  • Pelloquin, B., Kristan, M., Edi, C., Meiwald, A., Clark, E., Jeffries, C.L., Walker, T., Dada, N., Messenger, L.A., 2021. Overabundance of Asaia and Serratia bacteria is associated with deltamethrin insecticide susceptibility in Anopheles coluzzii from Agboville, Cote d'Ivoire. Microbiol. Spectr. 9 (2), e0015721. http://dx.doi.org/10.1128/ Spectrum.00157-21.
  • Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glockner, F.O., 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res.41 (D1), D590-D596.http://dx.doi.org/10.1093/nar/gks1219.
  • Ramos-Nino, M.E., Fitzpatrick, D.M., Eckstrom, K.M., Tighe, S., Hattaway, L.M., Hsueh, A.N., Stone, D.M., Dragon, J.A., Cheetham, S., 2020. Metagenomic analysis of Aedes aegypti and Culex quinquefasciatus mosquitoes from Grenada, West Indies. PLoS One 15 (4), e0231047. http://dx.doi.org/10.1371/journal.pone.0231047.
  • Ratcliffe, N.A., Furtado Pacheco, J.P., Dyson, P., Castro, H.C., Gonzalez, M.S., Azambuja, P., Mello, C.B., 2022. Overview of paratransgenesis as a strategy to control pathogen transmission by insect vectors. Parasit. Vectors 15 (1), 112. http://dx.doi.org/10.1186/s13071-021-05132-3.
  • Reis, L.A.M.,Silva,E.V.P.D., Dias, D.D., Freitas, M.N.O., Caldeira, R.D., Araujo, P.A.D.S., Silva, F.S.D., Rosa Junior, J.W., Brandao, R.C.F., Nascimento, B.L.S.D., Martins, L.C., Nunes Neto, J.P., 2023. Vector competence of Culex quinquefasciatus from Brazil for West Nile Virus. Trop. Med. Infect. Dis.8 (4), 217.http://dx.doi.org/10.3390/tropicalmed8040217.
  • Robeson 2nd, M.S., O'Rourke, D.R., Kaehler, B.D., Ziemski, M., Dillon, M.R., Foster, J.T., Bokulich, N.A., 2021. RESCRIPt: reproducible sequence taxonomy reference database management. PLOS Comput. Biol. 17 (11), e1009581.http://dx.doi.org/10.1371/journal.pcbi.1009581.
  • Rousset, F., Bouchon, D., Pintureau, B., Juchault, P., Solignac, M., 1992. Wolbachia endosymbionts responsible for variousalterations of sexuality in arthropods. Proc. Biol. Sci. 250 (1328), 91-98. http:// dx.doi.org/10.1098/rspb.1992.0135.
  • Santos, N.A.C.D., Carvalho, V.R., Souza-Neto, J.A., Alonso, D.P., Ribolla, P.E.M., Medeiros, J.F., Araujo, M.D.S., 2023. Bacterial microbiota from lab-reared and field-captured anopheles darlingi midgut and salivary gland. Microorganisms 11 (5), 1145. http://dx.doi. org/10.3390/microorganisms11051145.
  • Savage, H.M., Smith, G.C., Moore, C.G., Mitchell, C.J., Townsend, M., Marfin, A.A., 1993. Entomologic investigations of an epidemic of St. Louis encephalitis in Pine Bluff, Arkansas, 1991. Am. J. Trop. Med. Hyg. 49 (1), 38-45. http://dx.doi.org/10.4269/ajtmh.1993.49.38.
  • Serra, O.P., Cardoso, B.F., Ribeiro, A.L., Santos, F.A., Slhessarenko, R.D., 2016. Mayaro virus and dengue virus 1 and 4 natural infection in culicids from Cuiaba,state of Mato Grosso, Brazil.Mem. Inst.Oswaldo Cruz 111 (1), 20-29. http://dx.doi.org/10.1590/0074-02760150270.
  • Shih, C.M., Ophine, L., Chao, L.L., 2021. Molecular detection and genetic identification of wolbachia endosymbiont in wild-caught Culex quinquefasciatus (Diptera: Culicidae) mosquitoes from Sumatera Utara, Indonesia. Microb. Ecol. 81 (4), 1064-1074. http://dx.doi. org/10.1007/s00248-020-01655-x.
  • Silva-do-Nascimento, T.F., Sanchez-Ribas, J., Oliveira, T.M.P., Bourke, B.P., Oliveira-Ferreira, J., Rosa-Freitas, M.G., Lourenco-de-Oliveira, R., Marinho-E-Silva, M., Neves, M.S.A.S., Conn, J.E., Sallum, M.A.M., 2021. Molecular analysis reveals a high diversity of anopheline mosquitoes in yanomami lands and the Pantanal Region of Brazil. Genes 12 (12), 1995. http://dx.doi.org/10.3390/genes12121995.
  • Sinkins, S.P., 2004. Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochem. Mol. Biol. 34 (7), 723-729. http:// dx.doi.org/10.1016/j.ibmb.2004.03.025.
  • Stouthamer, R., Breeuwer, J.A.J., Luck, R.F., Werren, J.H., 1993. Molecular identification of microorganisms associatedwith parthenogenesis. Nature 361 (6407), 66-68. http://dx.doi.org/10.1038/361066a0.
  • Tamura, K., Stecher, G., Kumar, S., 2021.MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol. Biol. Evol. 38 (7), 3022-3027. http://dx.doi.org/10.1093/molbev/msab120.
  • Tuanudom, R., Yurayart, N., Rodkhum, C., Tiawsirisup, S., 2021. Diversity of midgut microbiota in laboratory-colonized and field-collected Aedes albopictus (Diptera:Culicidae): A preliminary study. Heliyon 7 (10), e08259. http://dx.doi.org/10.1016/j.heliyon.2021.e08259.
  • Wang, Y.T., Shen, R.X., Xing, D., Zhao, C.P., Gao, H.T., Wu, J.H., Zhang, N., Zhang, H.D., Chen, Y., Zhao, T.Y., Li, C.X., 2021. Metagenome Sequencing Reveals the Midgut Microbiota Makeup of Culex pipiens quinquefasciatus and Its Possible Relationship With Insecticide Resistance.Front. Microbiol. 12, 625539. http://dx.doi.org/10.3389/ fmicb.2021.625539.
  • Wilke, A.B.B., Marrelli, M.T., 2015. Paratransgenesis: a promising new strategy for mosquito vector control. Parasit. Vectors 8 (1), 342. http://dx.doi.org/10.1186/s13071-015-0959-2.
  • Wilke, A.B.B., Benelli, G., Beier, J.C., 2021. Anthropogenic changes and associated impacts on vector-borne diseases. Trends Parasitol. 37 (12), 1027-1030. http://dx.doi.org/10.1016/j.pt.2021.09.013.
  • Wong, M.L., Liew, J.W.K., Wong, W.K., Pramasivan, S., Mohamed Hassan, N., Wan Sulaiman, W.Y., Jeyaprakasam, N.K., Leong, C.S., Low, V.L., Vythilingam, I., 2020. Natural Wolbachia infection in field-collected Anopheles and other mosquito species from Malaysia. Parasit. Vectors 13 (1), 414.http://dx.doi.org/10.1186/s13071-020-04277-x.
  • WMP: World Mosquito Program, 2022. Annual Review. Available in https://www.worldmosquitoprogram.org/en/wmp-annualreview-2022 (accessed 18 July 2023).
  • Zheng, X., Zhang, D., Li, Y., Yang, C., Wu, Y., Liang, X., Liang, Y., Pan, X., Hu, L., Sun, Q., Wang, X., Wei, Y., Zhu, J., Qian, W., Yan, Z., Parker, A.G., Gilles, J.R.L., Bourtzis, K., Bouyer, J., Tang, M., Zheng, B., Yu, J., Liu, J., Zhuang, J., Hu, Z., Zhang, M., Gong, J.T., Hong, X.Y., Zhang, Z., Lin, L., Liu, Q., Hu, Z., Wu, Z., Baton, L.A., Hoffmann, A.A., Xi, Z., 2019. Incompatible and sterile insect techniques combined eliminate mosquitoes. Nature 572 (7767), 56-61. http://dx.doi.org/10.1038/ s41586-019-1407-9.
  • Zhou, W., Rousset,F., O'Neil, S., 1998.Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. Biol. Sci. 265 (1395), 509-515. http://dx.doi.org/10.1098/rspb.1998.0324.