Abstract
Symbiotic bacteria have been proposed as tools for control of insect-borne diseases. Primary requirements for such symbionts are dominance, prevalence and stability within the insect body. Most of the bacterial symbionts described to date in Anopheles mosquitoes, the vector of malaria in humans, have lacked these features. We describe an a-Proteobacterium of the genus Asaia, which stably associates with several Anopheles species and dominates within the body of An. Stephensi. Asaia exhibits all the required ecological characteristics making it the best candidate, available to date, for the development of a paratransgenic approach for manipulation of mosquito vector competence. Key features of Asaia are: (i) dominance within the mosquito-associated microflora, as shown by clone prevalence in 16S rRNA gene libraries and quantitative real time Polymerase Chain Reaction (qRT-PCR); (ii) cultivability in cell-free media; (iii) ease of transformation with foreign DNA and iv) wide distribution in the larvae and adult mosquito body, as revealed by transmission electron microscopy, and in situ-hybridization experiments. Using a green fluorescent protein (GFP)-tagged Asaia strain, it has been possible to show that it effectively colonizes all mosquito body organs necessary for malaria parasite development and transmission, including female gut and salivary glands. Asaia was also found to massively colonize the larval gut and the male reproductive system of adult mosquitoes. Moreover, mating experiments showed an additional key feature necessary for symbiotic control, the high transmission potential of the symbiont to progeny by multiple mechanisms. Asaia is capable of horizontal infection through an oral route during feeding both in preadult and adult stages and through a venereal pattern during mating in adults. Furthermore, Asaia is vertically transmitted from mother to progeny indicating that it could quickly spread in natural mosquito populations.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Ishikawa H. Insect in symbiosis: An introduction. In: Bourtzis K, Miller TA, eds. Insect Symbiosis Boca Raton: Crc Press Llc, 2003:33487.
Dillon RJ, Dillon VM. The gut bacteria of insects: Nonpathogenic interactions. Annu Rev Entomol 2004; 49:71–92.
Gil R, Latorre A, Moya A. Bacterial endosymbionts of insects: Insights from comparative genomics. Environ Microbiol 2004; 6:1109–22.
Hoffmeister M, Martin W. Interspecific evolution: Microbial symbiosis, endosymbiosis and gene transfer. Environ Microbiol 2003; 5:641–49.
Riehle MA, Jacobs-Lorena M. Using bacteria to express and display anti-parasite molecules in mosquitoes: Current and future strategies. Insect Biochem Mol Biol 2005; 35:699–707.
Zientz E, Silva FJ, Gross R. Genome interdependence in insect-bacterium symbioses. Genome Biol 2001; 2:1032. 1–32.6.
Douglas AE. Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 1998; 43:17–37.
Sinkins SP. Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochem Mol Biol 2004; 34:723–29.
Gotoh T, Noda H, Ito S. Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 2007; 98:13–20.
Marzorati M, Alma A, Sacchi L et al. A novel Bacteroidetes symbiont is localized in Scaphoideus titanus, the insect vector of Flavescence doree in Vitis vinifera. Appl Environ Microbiol 2006; 72:1467–75.
Aksoy S. Control of tsetse flies and trypanosomes using molecular genetics. Vet Parasitol 2003; 115:125–45.
Durvasula RV, Sundaram RK, Cordon-Rosales C et al. Rhodnius prolixus and its symbiont, Rhodococcus rhodnii: A model for paratrangenic control of disease transmission. In: Bourtzis K, Miller TA, eds. Insect Symbiosis. Boca Raton: Crc Press Llc, 2003:33487.
Chang TL, Chang CH, Simpson DA et al. Inhibition of HIV infectivity by a natural human isolate of Lactobacillus jensenii engineered to express functional two-domain CD4. Proc Natl Acad Sci USA 2003; 100:11672–77.
Bextine B, Lauzon C, Potter S et al. Delivery of a genetically marked Alcaligenes sp. to the glassy-winged sharpshooter for use in a paratransgenic control strategy. Curr Microbiol 2004; 48:327–31.
Zabalou M, Riegler M, Theodorakopoulou M et al. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc Natl Acad Sci USA 2004; 101:15042–45.
Schnepf E, Crickmore N, Van Rie J et al. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 1998; 62:775–806.
Zchori-Fein E, Gottlieb Y, Kelly SE et al. A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc Natl Acad Sci USA 2001; 98:12555–60.
Beard CB, Dotson EM, Pennington PM et al. Bacterial symbiosis and paratransgenic control of vector-borne Chagas disease. Int J Parasitol 2001; 31:621–27.
Baldridge GD, Burkhardt NY, Simser JA et al. Sequence and expression analysis of the ompA gene of Rickettsia peacockii, an endosymbiont of the Rocky Mountain wood tick, Dermacentor andersoni. Appl Environ Microbiol 2004; 70:6628–36.
World Health Organization. World malaria report 2005. Geneva, Switzerland: World Health Organization, Online http://www.rbm.who.int/wmr2005.
Atkinson PW, Michel K. What’s buzzing? Mosquito genomics and transgenic mosquitoes. Genesis 2002; 32:42–48.
Grossman GL, Rafferty CS, Clayton JR et al. Germline transformation of the malaria vector, Anopheles gambiae, with the piggyBac transposable element. Insect Mol Biol 2001; 10:597–604.
Catteruccia F, Nolan T, Loukeris TG et al. Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 2000; 405:959–62.
Ito J, Ghosh A, Moreira AL et al. Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 2002; 417:452–55.
Catteruccia F, Godfray HC, Crisanti A. Impact of genetic manipulation on the fitness of Anopheles stephensi mosquitoes. Science 2003; 299:1225–27.
Marrelli MT, Li C, Rasgon JL et al. Transgenic malaria-resistant mosquitoes have a fitness advantage when feeding on Plasmodium-infected blood. Proc Natl Acad Sci USA 2007; 104:5580–83.
Riehle MA, Moreira CK, Lampe D et al. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Int J Parasitol 2007; 37:595–603.
Khampang P, Chungjatupornchai W, Luxananil P et al. Efficient expression of mosquito-larvicidal proteins in a gram-negative bacterium capable of recolonization in the guts of Anopheles dirus larva. Appl Microbiol Biotechnol 1999; 51:79–84.
Lindh JM, Terenius O, Faye I. 16S rRNA gene-based identification of midgut bacteria from field-caught Anopheles gambiae sensu lato and A. funestus mosquitoes reveals new species related to known insect symbionts. Appl Environ Microbiol 2005; 71:7217–23.
Hoy MA. Transgenic insects for pest management programs: Status and prospects. Environ Biosafety Res 2003; 2:61–64.
Favia G, Ricci I, Damiani C et al. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci USA 2007; 104:9047–51.
Yamada Y, Katsura K, Kawasaki H et al. Asaia bogorensis gen. nov., sp. nov., an unusual acetic acid bacterium in the alpha-Proteobacteria. Int J Syst Evol Microbiol 2000; 50:823–29.
Katsura K, Kawasaki H, Potacharoen W et al. Asaia siamensis sp. nov., an acetic acid bacterium in the alpha-proteobacteria. Int J Syst Evol Microbiol 2001; 51:559–63.
Dong Y, Taylor HE, Dimopoulos G. AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 2006; 4:e229.
Cheng Q, Aksoy S. Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol Biol 1999; 8:125–32.
Tamas I, Andersson SGE. Comparative genomics in insect endosymbionts. In: Bourtzis K, Miller TA, eds. Insect Symbiosis. Boca Raton: Crc Press Llc, 2003:33487.
Ochman H, Moran NA. Genes lost and genes found: Evolution of bacterial pathogenesis and symbiosis. Science 2001; 292:1096–99.
Mostafa HE, Heller KJ, Geis A. Cloning of Escherichia coli lacZ and lacY genes and their expression in Gluconobacter oxydans and Acetobacter liquefaciens. Appl Environ Microbiol 2002; 68:2619–23.
Moran NA, Dunbar HE. Sexual acquisition of beneficial symbionts in aphids. Proc Natl Acad Sci USA 2006; 103:12803–06.
Nalepa CA, Bignell DE, Bandi C. Detritivory, coprophagy and the evolution of digestive mutualisms in Dictyoptera. Insect Socieaux 2001; 48:194–201.
Ricci I, Cancrini G, Gabrielli S et al. Searching for Wolbachia (Rickettsiales: Rickettsiaceae) in mosquitoes (Diptera: Culicidae): Large polymerase chain reaction survey and new identifications. J Med Entomol 2002; 39:562–67.
Yoshida S, Ioka D, Matsuoka H et al. Bacteria expressing single-chain immunotoxin inhibit malaria parasite development in mosquitoes. Mol Biochem Parasitol 2001; 113:89–96.
Ghosh AK, Ribolla PE, Jacobs-Lorena M. Targeting Plasmodium ligands on mosquito salivary glands and midgut with a phage display peptide library. Proc Natl Acad Sci USA 2001; 98:13278–81.
Zieler H, Keister DB, Dvorak JA et al. A snake venom phospholipase A(2) blocks malaria parasite development in the mosquito midgut by inhibiting ookinete association with the midgut surface. J Exp Biol 2001; 204:4157–67.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2008 Landes Bioscience and Springer Science+Business Media
About this chapter
Cite this chapter
Favia, G. et al. (2008). Bacteria of the Genus Asaia: A Potential Paratransgenic Weapon Against Malaria. In: Aksoy, S. (eds) Transgenesis and the Management of Vector-Borne Disease. Advances in Experimental Medicine and Biology, vol 627. Springer, New York, NY. https://doi.org/10.1007/978-0-387-78225-6_4
Download citation
DOI: https://doi.org/10.1007/978-0-387-78225-6_4
Publisher Name: Springer, New York, NY
Print ISBN: 978-0-387-78224-9
Online ISBN: 978-0-387-78225-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)