Abstract
Actually, the use of symbiotic bacteria is one of alternative solution to avoid vector resistance to pesticides. In Belgium, among 31 identified mosquito species, 10 were considered as potential vectors. Given to introduction risks of arbovirosis, the purpose of this study was to investigate the presence of symbiosis bacteria in potential mosquito vectors. Eleven species caught from 12 sites in Belgium were used: Culex pipiens s.l., Culex torrentium, Culex hortensis, Anopheles claviger, Anopheles maculipennis s.l., Anopheles plumbeus, Culiseta annulata, Ochlerotatus geniculatus, Ochlerotatus dorsalis, Aedes albopictus, and Coquillettidia richiardii. Six genera of symbiotic bacteria were screened: Wolbachia sp., Comamonas sp, Delftia sp., Pseudomonas sp., Acinetobacter sp., and Asaia sp. A total of 173 mosquito individuals (144 larvae and 29 adults) were used for the polymerase chain reaction screening. Wolbachia was not found in any Anopheles species nor Cx. torrentium. A total absence of Comamonas and Delftia was observed in all species. Acinetobacter, Pseudomonas, and Asaia were found in most of species with a high prevalence for Pseudomonas. These results were discussed to develop potential strategy and exploit the variable occurrence of symbiotic bacteria to focus on them to propose biological ways of mosquito control.
Similar content being viewed by others
References
Alauzet C et al (2010) Gluconobacter as well as Asaia species, newly emerging opportunistic human pathogens among acetic acid bacteria. J Clin Microbiol 48(11):3935–3942. doi:10.1128/jcm.00767-10
Almeida F, Moura AS, Cardoso AF, Winter CE, Bijovsky AT, Suesdek L (2011) Effects of Wolbachia on fitness of Culex quinquefasciatus (Diptera; Culicidae). Infect Genet Evol 11(8):2138–2143. doi:10.1016/j.meegid.2011.08.022
Atyame CM et al (2014) Wolbachia divergence and the evolution of cytoplasmic incompatibility in Culex pipiens. PLoS One 9(1):e87336. doi:10.1371/journal.pone.0087336
Bawin T, Seye F, Boukraa S, Zimmer J-Y, Delvigne F, Francis F (2015) La lutte contre les moustiques (Diptera: Culicidae): diversité des approches et application du contrôle biologique. Canadian Entomologist 147(4):476–500. doi:10.4039/tce.2014.56
Becker N, Petric D, Zgomba M, Boase C, Minoo M, Dahl C, Kaiser A (2010) Mosquitoes and their control, 2nd edn. Springer, Berlin Heidelberg
Bian G et al (2013) Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340(6133):748–751. doi:10.1126/science.1236192
Boukraa S et al (2013) Reintroduction of the invasive mosquito species Aedes albopictus in Belgium in July 2013. Parasite 20:54. doi:10.1051/parasite/2013054
Brammacharry U, Paily K (2012) Chitinase like activity of metabolites of Pseudomonas fluorescens Migula on immature stages of the mosquito, Culex quinquefasciatus (Diptera: Culicidae). Afr J Microbiol Res 6(11):2718–2726
Brossard M, Rutti B, Haug T, Eckert J, Crompton DWT, Wang CC, Hawdon JM, Schad GA, Bayne CJ, Harvey PH, Castro GA (1991) Parasite-host associations continued. Oxford University Press, Oxford
Bruce KD, Hiorns WD, Hobman JL, Osborn AM, Strike P, Ritchie DA (1992) Amplification of DNA from native populations of soil bacteria by using the polymerase chain reaction. Appl Environ Microbiol 58(10):3413–3416
Caragata EP, Rances E, O’Neill SL, McGraw EA (2014) Competition for amino acids between Wolbachia and the mosquito host, Aedes aegypti. Microb Ecol 67(1):205–218. doi:10.1007/s00248-013-0339-4
Chavshin AR et al (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. doi:10.1016/j.actatropica.2011.10.015
Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Terenius O (2014) Isolation and identification of culturable bacteria from wild Anopheles culicifacies, a first step in a paratransgenesis approach. Parasites Vectors 7(1):419. doi:10.1186/1756-3305-7-419
Chavshin AR, Oshaghi MA, Vatandoost H, Yakhchali B, Zarenejad F, Terenius O (2015) Malpighian tubules are important determinants of Pseudomonas transstadial transmission and longtime persistence in Anopheles stephensi. Parasit Vectors. 8(36) doi: 10.1186/s13071-015-0635-6
Chow J, Lee SM, Shen Y, Khosravi A, Mazmanian SK (2010) Host-bacterial symbiosis in health and disease. Adv Immunol 107:243–274. doi:10.1016/b978-0-12-381300-8.00008-3
Corbel V, N’Guessan R (2013) Distribution, mechanisms, impact and management of insecticide resistance in malaria vectors: a pragmatic review, Anopheles mosquitoes-New insights into malaria vectors., pp 579–633
Crotti E et al (2009) Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ Microbiol 11(12):3252–3264. doi:10.1111/j.1462-2920.2009.02048.x
Dheilly NM (2014) Holobiont–holobiont interactions: redefining host–parasite interactions. Plos Pathogens 10(7):1–4
Doughari HJ, Ndakidemi PA, Human IS, Benade S (2011) The ecology, biology and pathogenesis of Acinetobacter spp.: an overview. Microbes Environ 26(2):101–112
Favia G et al (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. doi:10.1073/pnas.0610451104
Harbach, R (2013) Mosquito taxonomic inventory http://mosquito-taxonomic-inventory.info/
Kenzaka T, Yamaguchi N, Tani K, Nasu M (1998) rRNA-targeted fluorescent in situ hybridization analysis of bacterial community structure in river water. Microbiology 144(Pt 8):2085–2093
Lindh J (2007) Identification of bacteria associated with malaria mosquitoes—their characterisation and potential use. Dissertation. Stockholm University
Lysyk TJ, Kalischuk-Tymensen L, Selinger LB, Lancaster RC, Wever L, Cheng KJ (1999) Rearing stable fly larvae (Diptera: Muscidae) on an egg yolk medium. J Med Entomol 36(3):382–388
Manguin S, Boëte C (2011) Global impact of mosquito biodiversity, human vector-borne diseases and environmental change., pp 27–50
Medlock JM, et al. (2015) An entomological review of invasive mosquitoes in Europe. Bull Entomol Res. :1–27 doi:10.1017/s0007485315000103
Minard G, Mavingui P, Moro CV (2013a) Diversity and function of bacterial microbiota in the mosquito holobiont. Parasites & Vectors 6 doi: 10.1186/1756-3305-6-146
Minard G et al (2013b) Prevalence, genomic and metabolic profiles of Acinetobacter and Asaia associated with field-caught Aedes albopictus from Madagascar. FEMS Microbiol Ecol 83(1):63–73. doi:10.1111/j.1574-6941.2012.01455.x
Moll RM, Romoser WS, Modrzakowski MC, Moncayo AC, Lerdthusnee K (2001) Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. J Med Entomol 38(1):29–32
Mweresa CK et al (2015) Understanding the long-lasting attraction of malaria mosquitoes to odor baits. PLoS One 10(3):e0121533. doi:10.1371/journal.pone.0121533
O’Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. PNAS 89(7):2699–2702
Ostfeld RS (2009) Biodiversity loss and the rise of zoonotic pathogens. Clin Microbiol Infect 15(Suppl 1):40–43. doi:10.1111/j.1469-0691.2008.02691.x
Ricci I, Damiani C, Capone A, DeFreece C, Rossi P, Favia G (2012a) Mosquito/microbiota interactions: from complex relationships to biotechnological perspectives. Curr Opin Microbiol 15(3):278–284. doi:10.1016/j.mib.2012.03.004
Ricci I, Valzano M, Ulissi U, Epis S, Cappelli A, Favia G (2012b) Symbiotic control of mosquito borne disease. Pathogens Global Health 106(7):380–385. doi:10.1179/2047773212y.0000000051
Sanguin H et al (2006) Development and validation of a prototype 16S rRNA-based taxonomic microarray for Alphaproteobacteria. Environ Microbiol 8(2):289–307. doi:10.1111/j.1462-2920.2005.00895.x
Schaffner F (2001) Les moustiques d’Europe: logiciel d’identification et d’enseignement = The mosquitoes of Europe: an identification and training programme. IRD; EID
Slenning BD (2010) Global climate change and implications for disease emergence. Vet Pathol 47(1):28–33. doi:10.1177/0300985809354465
Van den Hurk AF et al (2012) Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Negl Trop Dis 6(11):e1892. doi:10.1371/journal.pntd.0001892
Vega-Rua A et al (2013) High efficiency of temperate Aedes albopictus to transmit chikungunya and dengue viruses in the Southeast of France. PLoS One 8(3):e59716. doi:10.1371/journal.pone.0059716
Widmer F, Seidler RJ, Gillevet PM, Watrud LS, Di Giovanni GD (1998) A highly selective PCR protocol for detecting 16S rRNA genes of the genus Pseudomonas (sensu stricto) in environmental samples. Appl Environ Microbiol 64(7):2545–2553
Wilke AB, Marrelli MT (2015) Paratransgenesis: a promising new strategy for mosquito vector control. Parasit Vectors 8:342. doi:10.1186/s13071-015-0959-2
Wirth R, Friesenegger A, Fiedler S (1989) Transformation of various species of gram-negative bacteria belonging to 11 different genera by electroporation. Mol Gen Genet 216(1):175–177
Zayed ME, Bream AS (2004) Biodiversity of the microbial flora associated with two strains of Culexpipiens (Diptera: Culicidae). Commun Agric Appl Biol Sci 69(3):229–234
Zélé F, et al. (2014) Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance. Parasit Vectors 7(1) doi: 10.1186/1756-3305-7-437
Zouache K, Voronin D, Tran-Van V, Mavingui P (2009) Composition of bacterial communities associated with natural and laboratory populations of Asobara tabida infected with Wolbachia. Appl Environ Microbiol 75(11):3755–3764. doi:10.1128/aem.02964-08
Zouache K et al (2011) Bacterial diversity of field-caught mosquitoes, Aedes albopictus and Aedes aegypti, from different geographic regions of Madagascar. FEMS Microbiol Ecol 75(3):377–389. doi:10.1111/j.1574-6941.2010.01012.x
Acknowledgments
The authors thank all managers of the capture sites that allowed us unrestricted access to their sites. We also and especially thank Patrick Mavingui and the team of “Dynamics Microbial and Viral Transmission” of the University Claude Bernard 1 to kindly provide us positive controls for bacteria screening. This work was supported by “Subside Federal for Research” (grant R.DIVE.05558-J-F), University of Liege (ULg) to FNR and by the PhD scholarship of the Wallonia-Brussels International granted to SBoukraa.
Authors’ contributions
FNR conceived the study. FNR, SBoukraa, TB contributed to material collection, data analysis, interpretation and manuscript writing. FNR and SBoukraa conducted PCR studies and PCR analysis. SBoyer and FF contributed to data interpretation and manuscript writing. All authors read and approved the final version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Rights and permissions
About this article
Cite this article
Raharimalala, F.N., Boukraa, S., Bawin, T. et al. Molecular detection of six (endo-) symbiotic bacteria in Belgian mosquitoes: first step towards the selection of appropriate paratransgenesis candidates. Parasitol Res 115, 1391–1399 (2016). https://doi.org/10.1007/s00436-015-4873-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-015-4873-5