Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection

Xi, Zhiyong; Dean, Jeffry L.; Khoo, Cynthia; Dobson, Stephen L.

doi:10.1016/j.ibmb.2005.03.015

Cited by 119 publications

(109 citation statements)

References 45 publications

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“…Finally, Rickettsia was found to be concentrated at the posterior pole of the oocyte during mid to late and late oogenesis, as well as at the posterior pole of the egg during early embryogenesis. The same pattern has been observed for Wolbachia in many insect host species (13,22,63,70,91,98). As the posterior pole is the site where the germ cells form during embryogenesis, concentration of symbionts at this site has been thought to be a mechanism for increasing the probability that bacteria are integrated into the germ cells and then transmitted to host progeny (31,63,77).…”

Section: Downloaded Fromsupporting

confidence: 53%

Rickettsia Symbionts Cause Parthenogenetic Reproduction in the Parasitoid Wasp Pnigalio soemius (Hymenoptera: Eulophidae)

Giorgini¹,

Bernardo²,

Monti³

et al. 2010

Appl Environ Microbiol

126

121

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Bacteria in the genus Rickettsia are intracellular symbionts of disparate groups of organisms. Some Rickettsia strains infect vertebrate animals and plants, where they cause diseases, but most strains are vertically inherited symbionts of invertebrates. In insects Rickettsia symbionts are known to have diverse effects on hosts ranging from influencing host fitness to manipulating reproduction. Here we provide evidence that a Rickettsia symbiont causes thelytokous parthenogenesis (in which mothers produce only daughters from unfertilized eggs) in a parasitoid wasp, Pnigalio soemius (Hymenoptera: Eulophidae). Feeding antibiotics to thelytokous female wasps resulted in production of progeny that were almost all males. Cloning and sequencing of a fragment of the 16S rRNA gene amplified with universal primers, diagnostic PCR screening of symbiont lineages associated with manipulation of reproduction, and fluorescence in situ hybridization (FISH) revealed that Rickettsia is always associated with thelytokous P. soemius and that no other bacteria that manipulate reproduction are present. Molecular analyses and FISH showed that Rickettsia is distributed in the reproductive tissues and is transovarially transmitted from mothers to offspring. Comparison of antibiotic-treated females and untreated females showed that infection had no cost. Phylogenetic analyses of 16S rRNA and gltA gene sequences placed the symbiont of P. soemius in the bellii group and indicated that there have been two separate origins of the parthenogenesis-inducing phenotype in the genus Rickettsia. A possible route for evolution of induction of parthenogenesis in the two distantly related Rickettsia lineages is discussed.The genus Rickettsia contains a group of obligate intracellular symbionts of eukaryotic cells and belongs to the family Rickettsiaceae in the order Rickettsiales of the Alphaproteobacteria (58, 90). Many species have medical importance as they are pathogens of humans and other vertebrates; pathogenic Rickettsia species infect their hosts through blood-feeding arthropods, including lice, fleas, ticks, and mites (51, 80). In addition to Rickettsia species that cause infectious diseases in vertebrates, symbiotic species have been found in disparate groups of organisms, including arthropods, annelids, amoebae, hydrozoa, and plants (53). Rickettsia appears to be especially common in arthropods, having been found in a wide range of taxa in the classes Entognatha

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Section: Downloaded Fromsupporting

confidence: 53%

Rickettsia Symbionts Cause Parthenogenetic Reproduction in the Parasitoid Wasp Pnigalio soemius (Hymenoptera: Eulophidae)

Giorgini¹,

Bernardo²,

Monti³

et al. 2010

Appl Environ Microbiol

126

121

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“…This positions Wolbachia at the site of the future germline prior to cellularization, promoting subsequent envelopment of Wolbachia by the germline cells. Posterior Wolbachia localization in late oogenesis has also been observed in several mosquito and hymenopteran host species (18,40,136,140,156,160), suggesting that posterior localization is successful as a Wolbachia transmission strategy.…”

Section: How Wolbachia Localization Relates To Transmissionmentioning

confidence: 88%

The Genetics and Cell Biology of Wolbachia-Host Interactions

et al. 2008

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Wolbachia are gram-negative bacteria that are widespread in nature, carried by the majority of insect species as well as some mites, crustaceans, and filarial nematodes. Wolbachia can range from parasitic to symbiotic, depending upon the interaction with the host species. The success of Wolbachia is attributed to efficient maternal transmission and manipulations of host reproduction that favor infected females, such as sperm-egg cytoplasmic incompatibility (CI). Much remains unknown about the mechanistic basis for Wolbachia-host interactions. Here we summarize the current understanding of Wolbachia interaction with insect hosts, with a focus on Drosophila. The areas of discussion include Wolbachia transmission in oogenesis, Wolbachia distribution in spermatogenesis, induction and rescue of the CI phenotype, Wolbachia genomics, and Wolbachia-membrane interactions. 683

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“…Embryos were collected, prepared, and microinjected as previously described (29,30). Injection was performed using an IM 300 microinjector (Narishige Scientific, Tokyo, Japan).…”

Section: Methodsmentioning

confidence: 99%

Artificial Triple Wolbachia Infection in Aedes albopictus Yields a New Pattern of Unidirectional Cytoplasmic Incompatibility

Gavotte

Mercer

et al. 2010

Appl Environ Microbiol

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Obligately intracellular Wolbachia bacteria infect numerous invertebrates and often manipulate host reproduction to facilitate the spread of infection. An example of reproductive manipulation is Wolbachia-induced cytoplasmic incompatibility (CI), which occurs commonly in insects. This CI has been the focus both of basic scientific studies of naturally occurring invasion events and of applied investigations on the use of Wolbachia as a vehicle to drive desired genotypes into insect populations ("gene drive" or "population replacement" strategies). The latter application requires an ability to generate artificial infections that cause a pattern of unidirectional incompatibility with the targeted host population. A suggested target of population replacement strategies is the mosquito Aedes albopictus (Asian tiger mosquito), an important invasive pest and disease vector. Aedes albopictus individuals are naturally "superinfected" with two Wolbachia types: wAlbA and wAlbB. Thus, generating a strain that is unidirectionally incompatible with field populations requires the introduction of an additional infection into the preexisting superinfection. Although prior reports demonstrate an ability to transfer Wolbachia infections to A. albopictus artificially, including both intra-and interspecific Wolbachia transfers, previous efforts have not generated a strain capable of invading natural populations. Here we describe the generation of a stable triple infection by introducing Wolbachia wRi from Drosophila simulans into a naturally superinfected A. albopictus strain. The triple-infected strain displays a pattern of unidirectional incompatibility with the naturally infected strain. This unidirectional CI, combined with a high fidelity of maternal inheritance and low fecundity effects, suggests that the artificial cytotype could serve as an appropriate vehicle for gene drive.

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Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection

Cited by 119 publications

References 45 publications

Rickettsia Symbionts Cause Parthenogenetic Reproduction in the Parasitoid Wasp Pnigalio soemius (Hymenoptera: Eulophidae)

Rickettsia Symbionts Cause Parthenogenetic Reproduction in the Parasitoid Wasp Pnigalio soemius (Hymenoptera: Eulophidae)

The Genetics and Cell Biology of Wolbachia-Host Interactions

Artificial Triple Wolbachia Infection in Aedes albopictus Yields a New Pattern of Unidirectional Cytoplasmic Incompatibility

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