Isolation and identification of microbiota of Culex quinquefasciatus for their application as paratransgenic tools in vector control
Abstract
Background and Objectives: Although the study on the bacteria residing in the mid-gut, salivary gland, and reproductive organs of insect vectors have drawn appeal to the host-pathogen interactions, we know comparatively less about microbiota that naturally exist in different mosquito organs within Iran.
Materials and Methods: In the current investigation, PCR assay by using 16S rRNA gene amplification and DNA sequencing, in addition to the traditional culture-based approach utilized for the detection of cultivable bacterial assemblages in mid-gut and reproductive tracts of Culex quinquefasciatus.
Results: The identified bacteria isolated from different tissues of 45 individuals were consisted of Achromobacter, Aeromonas, Arthrobacter, Asaia, Enterobacter, Gluconobacter, Klebsiella, Lysinibacillus, Micrococcus, Psuedomonas and Serratia. The results showed that Proteobacteria was the most prevalent phylum in both genders' mid-gut and reproductive tracts, and Asaia was the most common bacteria that originated in adult females and males’ tissues.
Conclusion: These outcomes recommend that the discovered microbiome may span through Cx. quinquefasciatus populations. This data can be utilized to interfere with the transmission of pathogens and design new strategies for the control of mosquito-borne diseases.
1. Amraoui F, Krida G, Bouattour A, Rhim A, Daaboub J, Harrat Z, et al. Culex pipiens, an experimental efficient vector of West Nile and Rift Valley fever viruses in the Maghreb region. PLoS One 2012; 7(5): e36757.
2. Hamer GL, Kitron UD, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, et al. Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile virus to humans. J Med Entomol 2008; 45: 125-128.
3. Turell MJ. Members of the Culex pipiens complex as vectors of viruses. J Am Mosq Control Assoc 2012; 28(4 Suppl): 123-126.
4. Diaz LA, Flores FS, Beranek M, Rivarola ME, Almirón WR, Contigiani MS. Transmission of endemic St Louis encephalitis virus strains by local Culex quinquefasciatus populations in Cordoba, Argentina. Trans R Soc Trop Med Hyg 2013; 107: 332-334.
5. Samy AM, Elaagip AH, Kenawy MA, Ayres CF, Peterson AT, Soliman DE. Climate change influences on the global potential distribution of the mosquito Culex quinquefasciatus, vector of West Nile virus and lymphatic filariasis. PloS One 2016; 11(10): e0163863.
6. Bakhshi H, Mousson L, Vazeille M, Zakeri S, Raz A, De Lamballerie X, et al. High transmission potential of West Nile Virus Lineage 1 for Cx. pipiens s.l. of Iran. Viruses 2020; 12: 397.
7. Bakhshi H, Beck C, Lecollinet S, Monier M, Mousson L, Zakeri S, et al. Serological evidence of West Nile virus infection among birds and horses in some geographical locations of Iran. Vet Med Sci 2021; 7: 204-209.
8. Liu Z, Zhou T, Lai Z, Zhang Z, Jia Z, Zhou G, et al. Competence of Aedes aegypti, Ae. albopictus, and Culex quinquefasciatus mosquitoes as Zika virus vectors, China. Emerg Infect Dis 2017; 23: 1085-1091.
9. Pruck-Ngern M, Pattaradilokrat S, Chumpolbanchorn K, Pimnon S, Narkpinit S, Harnyuttanakorn P, et al. Effects of artesunate treatment on Plasmodium gallinaceum transmission in the vectors Aedes aegypti and Culex quinquefasciatus. Vet Parasitol 2015; 207: 161-165.
10. Nourani L, Zakeri S, Dinparast Djadid N. Dynamics of prevalence and distribution pattern of avian Plasmodium species and its vectors in diverse zoogeographical areas-A review. Infect Genet Evol 2020; 81: 104244.
11. Weiss B, Aksoy S. Microbiome influences on insect host vector competence. Trends Parasitol 2011; 27: 514-522.
12. Weiss BL, Wang J, Aksoy S. Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biol 2011; 9(5): e1000619.
13. Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 2004; 49: 71-92.
14. Scolari F, Casiraghi M, Bonizzoni M. Aedes spp. and their microbiota: a review. Front Microbiol 2019; 10: 2036.
15. McCarroll L, Paton MG, Karunaratne SH, Jayasuryia HT, Kalpage KS, Hemingway J. Insecticides and mosquito-borne disease. Nature 2000; 407: 961-962.
16. Wilke ABB, Marrelli MT. Paratransgenesis: a promising new strategy for mosquito vector control. Parasit Vectors 2015; 8: 342.
17. Raharimalala FN, Boukraa S, Bawin T, Boyer S, Francis F. Molecular detection of six (endo-) symbiotic bacteria in Belgian mosquitoes: first step towards the selection of appropriate paratransgenesis candidates. Parasitol Res 2016; 115: 1391-1399.
18. Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M. Fighting malaria with engineered symbiotic bacteria from vector mosquitoes. Proc Natl Acad Sci U S A 2012; 109: 12734-12739.
19. Welch M, Govindarajan S, Ness JE, Villalobos A, Gurney A, Minshull J, et al. Design parameters to control synthetic gene expression in Escherichia coli. PLoS One 2009; 4(9): e7002.
20. Pidiyar V, Kaznowski A, Narayan NB, Patole M, Shouche YS. Aeromonas culicicola sp. nov., from the midgut of Culex quinquefasciatus. Int J Syst Evol Microbiol 2002; 52: 1723-1728.
21. Pidiyar VJ, Jangid K, Patole MS, Shouche YS. Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus mosquito midgut based on 16S ribosomal RNA gene analysis. Am J Trop Med Hyg 2004; 70: 597-603.
22. Chandel K, Mendki MJ, Parikh RY, Kulkarni G, Tikar SN, Sukumaran D, et al. Midgut microbial community of Culex quinquefasciatus mosquito populations from India. PloS One 2013; 8(11): e80453.
23. Chandel K, Parikh RY, Mendki MJ, Shouche YS, Veer V. Isolation and characterization of Vagococcus sp from midgut of Culex quinquefasciatus (Say) mosquito. J Vector Borne Dis 2015; 52: 52-57.
24. Mancini MV, Damiani C, Accoti A, Tallarita M, Nunzi E, Cappelli A, et al. Estimating bacteria diversity in different organs of nine species of mosquito by next generation sequencing. BMC Microbiol 2018; 18: 126.
25. Juma EO, Allan BF, Kim C-H, Stone C, Dunlap C, Muturi EJ. Effect of life stage and pesticide exposure on the gut microbiota of Aedes albopictus and Culex pipiens L. Sci Rep 2020; 10: 9489.
26. Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA, et al. 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 2012; 121: 129-134.
27. Dinparast Djadid N, Jazayeri H, Raz A, Favia G, Ricci I, Zakeri S. Identification of the midgut microbiota of An. stephensi and An. maculipennis for their application as a paratransgenic tool against malaria. PloS One 2011; 6(12): e28484.
28. Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Terenius O. Isolation and identification of culturable bacteria from wild Anopheles culicifacies, a first step in a paratransgenesis approach. Parasit
Vectors 2014; 7: 419.
29. Dehghan H, Sadraei J, Moosa-Kazemi SH, Abolghasemi E, Solimani H, Jaffari Nodoshan A, et al. A pictorial key for Culex pipiens complex (Diptera: Culicidae) in Iran. J Arthropod Borne Dis 2016; 10: 291-302.
30. Favia G, Ricci I, Damiani C, Raddadi N, Crotti E, Marzorati M, et al. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci U S A 2007; 104: 9047-9051.
31. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30: 2725-2729.
32. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19: 1572-1574.
33. Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 2020; 37: 291-294.
34. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009; 25: 1451-1452.
35. Minard G, Mavingui P, Moro CV. Diversity and function of bacterial microbiota in the mosquito holobiont. Parasit Vectors 2013; 6: 146.
36. Farajollahi A, Fonseca DM, Kramer LD, Marm Kilpatrick A. “Bird biting” mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect Genet Evol 2011; 11: 1577-1585.
37. Coon KL, Brown MR, Strand MR. Gut bacteria differentially affect egg production in the anautogenous mosquito Aedes aegypti and facultatively autogenous mosquito Aedes atropalpus (Diptera: Culicidae). Parasit Vectors 2016; 9: 375.
38. Muturi EJ, Kim C-H, Bara J, Bach EM, Siddappaji MH. Culex pipiens and Culex restuans mosquitoes harbor distinct microbiota dominated by few bacterial taxa. Parasit Vectors 2016; 9: 18.
39. Suo P, Wang K, Yu H, Fu X, An L, Bhowmick B, et al. Seasonal variation of midgut bacterial diversity in Culex quinquefasciatus populations in Haikou City, Hainan Province, China. Biology (Basel) 2022; 11: 1166.
40. Telang A, Skinner J, Nemitz RZ, McClure AM. Metagenome and culture-based methods reveal Candidate bacterial mutualists in the Southern House Mosquito (Diptera: Culicidae). J Med Entomol 2018; 55: 1170-1181.
41. Adly E, Hegazy AA, Kamal M, Abu-Hussien SH. Midguts of Culex pipiens L. (Diptera: Culicidae) as a potential source of raw milk contamination with pathogens. Sci Rep 2022; 12: 13183.
42. Gazzoni Araujo Gonçalves G, Feitosa APS, Portela-Júnior NC, De Oliveira CMF, De Lima Filho JL, Brayner FA, et al. Use of MALDI-TOF MS to identify the culturable midgut microbiota of laboratory and wild mosquitoes. Acta Trop 2019; 200: 105174.
43. Ramos-Nino ME, Fitzpatrick DM, Eckstrom KM, Tighe S, Hattaway LM, Hsueh AN, et al. Metagenomic analysis of Aedes aegypti and Culex quinquefasciatus mosquitoes from Grenada, West Indies. PLoS One 2020; 15(4): e0231047.
44. Tandina F, Almeras L, Koné AK, Doumbo OK, Raoult D, Parola P. Use of MALDI-TOF MS and culturomics to identify mosquitoes and their midgut microbiota. Parasit Vectors 2016; 9: 495.
45. Chandler JA, Liu RM, Bennett SN. RNA shotgun metagenomic sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Front Microbiol 2015; 6: 185.
46. Novakova E, Woodhams DC, Rodríguez-Ruano SM, Brucker RM, Leff JW, Maharaj A, et al. Mosquito microbiome dynamics, a background for prevalence and seasonality of West Nile virus. Front Microbiol 2017; 8: 526.
47. Osei-Poku J, Mbogo CM, Palmer WJ, Jiggins FM. Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Mol Ecol 2012; 21: 5138-5150.
48. Ricci I, Damiani C, Capone A, DeFreece C, Rossi P, Favia G. Mosquito/microbiota interactions: from complex relationships to biotechnological perspectives. Curr Opin Microbiol 2012; 15: 278-284.
49. Duguma D, Hall MW, Rugman-Jones P, Stouthamer R, Terenius O, Neufeld JD, et al. Developmental succession of the microbiome of Culex mosquitoes. BMC Microbiol 2015; 15: 140.
50. Duguma D, Hall MW, Smartt CT, Neufeld JD. Temporal variations of microbiota associated with the immature stages of two Florida Culex mosquito vectors. Microb Ecol 2017; 74: 979-989.
51. Duguma D, Hall MW, Smartt CT, Neufeld JD. Effects of organic amendments on microbiota associated with the Culex nigripalpus mosquito vector of the Saint Louis Encephalitis and West Nile viruses. mSphere 2017; 2(1): e00387-16.
52. De Freece C, Damiani C, Valzano M, D'amelio S, Cappelli A, Ricci I, et al. Detection and isolation of the α‐proteobacterium Asaia in Culex mosquitoes. Med Vet Entomol 2014; 28: 438-442.
53. Coon KL, Vogel KJ, Brown MR, Strand MR. Mosquitoes rely on their gut microbiota for development. Mol Ecol 2014; 23: 2727-2739.
2. Hamer GL, Kitron UD, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, et al. Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile virus to humans. J Med Entomol 2008; 45: 125-128.
3. Turell MJ. Members of the Culex pipiens complex as vectors of viruses. J Am Mosq Control Assoc 2012; 28(4 Suppl): 123-126.
4. Diaz LA, Flores FS, Beranek M, Rivarola ME, Almirón WR, Contigiani MS. Transmission of endemic St Louis encephalitis virus strains by local Culex quinquefasciatus populations in Cordoba, Argentina. Trans R Soc Trop Med Hyg 2013; 107: 332-334.
5. Samy AM, Elaagip AH, Kenawy MA, Ayres CF, Peterson AT, Soliman DE. Climate change influences on the global potential distribution of the mosquito Culex quinquefasciatus, vector of West Nile virus and lymphatic filariasis. PloS One 2016; 11(10): e0163863.
6. Bakhshi H, Mousson L, Vazeille M, Zakeri S, Raz A, De Lamballerie X, et al. High transmission potential of West Nile Virus Lineage 1 for Cx. pipiens s.l. of Iran. Viruses 2020; 12: 397.
7. Bakhshi H, Beck C, Lecollinet S, Monier M, Mousson L, Zakeri S, et al. Serological evidence of West Nile virus infection among birds and horses in some geographical locations of Iran. Vet Med Sci 2021; 7: 204-209.
8. Liu Z, Zhou T, Lai Z, Zhang Z, Jia Z, Zhou G, et al. Competence of Aedes aegypti, Ae. albopictus, and Culex quinquefasciatus mosquitoes as Zika virus vectors, China. Emerg Infect Dis 2017; 23: 1085-1091.
9. Pruck-Ngern M, Pattaradilokrat S, Chumpolbanchorn K, Pimnon S, Narkpinit S, Harnyuttanakorn P, et al. Effects of artesunate treatment on Plasmodium gallinaceum transmission in the vectors Aedes aegypti and Culex quinquefasciatus. Vet Parasitol 2015; 207: 161-165.
10. Nourani L, Zakeri S, Dinparast Djadid N. Dynamics of prevalence and distribution pattern of avian Plasmodium species and its vectors in diverse zoogeographical areas-A review. Infect Genet Evol 2020; 81: 104244.
11. Weiss B, Aksoy S. Microbiome influences on insect host vector competence. Trends Parasitol 2011; 27: 514-522.
12. Weiss BL, Wang J, Aksoy S. Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biol 2011; 9(5): e1000619.
13. Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 2004; 49: 71-92.
14. Scolari F, Casiraghi M, Bonizzoni M. Aedes spp. and their microbiota: a review. Front Microbiol 2019; 10: 2036.
15. McCarroll L, Paton MG, Karunaratne SH, Jayasuryia HT, Kalpage KS, Hemingway J. Insecticides and mosquito-borne disease. Nature 2000; 407: 961-962.
16. Wilke ABB, Marrelli MT. Paratransgenesis: a promising new strategy for mosquito vector control. Parasit Vectors 2015; 8: 342.
17. Raharimalala FN, Boukraa S, Bawin T, Boyer S, Francis F. Molecular detection of six (endo-) symbiotic bacteria in Belgian mosquitoes: first step towards the selection of appropriate paratransgenesis candidates. Parasitol Res 2016; 115: 1391-1399.
18. Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M. Fighting malaria with engineered symbiotic bacteria from vector mosquitoes. Proc Natl Acad Sci U S A 2012; 109: 12734-12739.
19. Welch M, Govindarajan S, Ness JE, Villalobos A, Gurney A, Minshull J, et al. Design parameters to control synthetic gene expression in Escherichia coli. PLoS One 2009; 4(9): e7002.
20. Pidiyar V, Kaznowski A, Narayan NB, Patole M, Shouche YS. Aeromonas culicicola sp. nov., from the midgut of Culex quinquefasciatus. Int J Syst Evol Microbiol 2002; 52: 1723-1728.
21. Pidiyar VJ, Jangid K, Patole MS, Shouche YS. Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus mosquito midgut based on 16S ribosomal RNA gene analysis. Am J Trop Med Hyg 2004; 70: 597-603.
22. Chandel K, Mendki MJ, Parikh RY, Kulkarni G, Tikar SN, Sukumaran D, et al. Midgut microbial community of Culex quinquefasciatus mosquito populations from India. PloS One 2013; 8(11): e80453.
23. Chandel K, Parikh RY, Mendki MJ, Shouche YS, Veer V. Isolation and characterization of Vagococcus sp from midgut of Culex quinquefasciatus (Say) mosquito. J Vector Borne Dis 2015; 52: 52-57.
24. Mancini MV, Damiani C, Accoti A, Tallarita M, Nunzi E, Cappelli A, et al. Estimating bacteria diversity in different organs of nine species of mosquito by next generation sequencing. BMC Microbiol 2018; 18: 126.
25. Juma EO, Allan BF, Kim C-H, Stone C, Dunlap C, Muturi EJ. Effect of life stage and pesticide exposure on the gut microbiota of Aedes albopictus and Culex pipiens L. Sci Rep 2020; 10: 9489.
26. Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA, et al. 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 2012; 121: 129-134.
27. Dinparast Djadid N, Jazayeri H, Raz A, Favia G, Ricci I, Zakeri S. Identification of the midgut microbiota of An. stephensi and An. maculipennis for their application as a paratransgenic tool against malaria. PloS One 2011; 6(12): e28484.
28. Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Terenius O. Isolation and identification of culturable bacteria from wild Anopheles culicifacies, a first step in a paratransgenesis approach. Parasit
Vectors 2014; 7: 419.
29. Dehghan H, Sadraei J, Moosa-Kazemi SH, Abolghasemi E, Solimani H, Jaffari Nodoshan A, et al. A pictorial key for Culex pipiens complex (Diptera: Culicidae) in Iran. J Arthropod Borne Dis 2016; 10: 291-302.
30. Favia G, Ricci I, Damiani C, Raddadi N, Crotti E, Marzorati M, et al. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci U S A 2007; 104: 9047-9051.
31. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30: 2725-2729.
32. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19: 1572-1574.
33. Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 2020; 37: 291-294.
34. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009; 25: 1451-1452.
35. Minard G, Mavingui P, Moro CV. Diversity and function of bacterial microbiota in the mosquito holobiont. Parasit Vectors 2013; 6: 146.
36. Farajollahi A, Fonseca DM, Kramer LD, Marm Kilpatrick A. “Bird biting” mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect Genet Evol 2011; 11: 1577-1585.
37. Coon KL, Brown MR, Strand MR. Gut bacteria differentially affect egg production in the anautogenous mosquito Aedes aegypti and facultatively autogenous mosquito Aedes atropalpus (Diptera: Culicidae). Parasit Vectors 2016; 9: 375.
38. Muturi EJ, Kim C-H, Bara J, Bach EM, Siddappaji MH. Culex pipiens and Culex restuans mosquitoes harbor distinct microbiota dominated by few bacterial taxa. Parasit Vectors 2016; 9: 18.
39. Suo P, Wang K, Yu H, Fu X, An L, Bhowmick B, et al. Seasonal variation of midgut bacterial diversity in Culex quinquefasciatus populations in Haikou City, Hainan Province, China. Biology (Basel) 2022; 11: 1166.
40. Telang A, Skinner J, Nemitz RZ, McClure AM. Metagenome and culture-based methods reveal Candidate bacterial mutualists in the Southern House Mosquito (Diptera: Culicidae). J Med Entomol 2018; 55: 1170-1181.
41. Adly E, Hegazy AA, Kamal M, Abu-Hussien SH. Midguts of Culex pipiens L. (Diptera: Culicidae) as a potential source of raw milk contamination with pathogens. Sci Rep 2022; 12: 13183.
42. Gazzoni Araujo Gonçalves G, Feitosa APS, Portela-Júnior NC, De Oliveira CMF, De Lima Filho JL, Brayner FA, et al. Use of MALDI-TOF MS to identify the culturable midgut microbiota of laboratory and wild mosquitoes. Acta Trop 2019; 200: 105174.
43. Ramos-Nino ME, Fitzpatrick DM, Eckstrom KM, Tighe S, Hattaway LM, Hsueh AN, et al. Metagenomic analysis of Aedes aegypti and Culex quinquefasciatus mosquitoes from Grenada, West Indies. PLoS One 2020; 15(4): e0231047.
44. Tandina F, Almeras L, Koné AK, Doumbo OK, Raoult D, Parola P. Use of MALDI-TOF MS and culturomics to identify mosquitoes and their midgut microbiota. Parasit Vectors 2016; 9: 495.
45. Chandler JA, Liu RM, Bennett SN. RNA shotgun metagenomic sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Front Microbiol 2015; 6: 185.
46. Novakova E, Woodhams DC, Rodríguez-Ruano SM, Brucker RM, Leff JW, Maharaj A, et al. Mosquito microbiome dynamics, a background for prevalence and seasonality of West Nile virus. Front Microbiol 2017; 8: 526.
47. Osei-Poku J, Mbogo CM, Palmer WJ, Jiggins FM. Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Mol Ecol 2012; 21: 5138-5150.
48. Ricci I, Damiani C, Capone A, DeFreece C, Rossi P, Favia G. Mosquito/microbiota interactions: from complex relationships to biotechnological perspectives. Curr Opin Microbiol 2012; 15: 278-284.
49. Duguma D, Hall MW, Rugman-Jones P, Stouthamer R, Terenius O, Neufeld JD, et al. Developmental succession of the microbiome of Culex mosquitoes. BMC Microbiol 2015; 15: 140.
50. Duguma D, Hall MW, Smartt CT, Neufeld JD. Temporal variations of microbiota associated with the immature stages of two Florida Culex mosquito vectors. Microb Ecol 2017; 74: 979-989.
51. Duguma D, Hall MW, Smartt CT, Neufeld JD. Effects of organic amendments on microbiota associated with the Culex nigripalpus mosquito vector of the Saint Louis Encephalitis and West Nile viruses. mSphere 2017; 2(1): e00387-16.
52. De Freece C, Damiani C, Valzano M, D'amelio S, Cappelli A, Ricci I, et al. Detection and isolation of the α‐proteobacterium Asaia in Culex mosquitoes. Med Vet Entomol 2014; 28: 438-442.
53. Coon KL, Vogel KJ, Brown MR, Strand MR. Mosquitoes rely on their gut microbiota for development. Mol Ecol 2014; 23: 2727-2739.
| Files | ||
| Issue | Vol 15 No 2 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i2.12478 | |
| Keywords | ||
| Vector-borne diseases; Culex; Polymerase chain reaction; Bacteria | ||
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How to Cite
1.
Nourani L, Raz A, Dinparast Djadid N. Isolation and identification of microbiota of Culex quinquefasciatus for their application as paratransgenic tools in vector control. Iran J Microbiol. 2023;15(2):258-266.
