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Highly transmissible cytoplasmic incompatibility by the extracellular insect symbiont Spiroplasma.

ABSTRACT: Cytoplasmic incompatibility (CI) is a form of reproductive manipulation caused by maternally inherited endosymbionts infecting arthropods, like Wolbachia, whereby matings between infected males and uninfected females produce few or no offspring. We report the discovery of a new CI symbiont, a strain of Spiroplasma causing CI in the parasitoid wasp Lariophagus distinguendus. Its extracellular occurrence enabled us to establish CI in uninfected adult insects by transferring Spiroplasma-infected hemolymph. We sequenced the CI-Spiroplasma genome and did not find any homologues of any of the cif genes discovered to cause CI in Wolbachia, suggesting independent evolution of CI. Instead, the genome contains other potential CI-causing candidate genes, such as homologues of high-mobility group (HMG) box proteins that are crucial in eukaryotic development but rare in bacterial genomes. Spiroplasma's extracellular nature and broad host range encompassing medically and agriculturally important arthropods make it a promising tool to study CI and its applications.

SUBMITTER: Pollmann M

PROVIDER: S-EPMC9118660 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Highly transmissible cytoplasmic incompatibility by the extracellular insect symbiont Spiroplasma.

Pollmann Marie M Moore Logan D LD Krimmer Elena E D'Alvise Paul P Hasselmann Martin M Perlman Steve J SJ Ballinger Matthew J MJ Steidle Johannes L M JLM Gottlieb Yuval Y

iScience 20220429 5

Cytoplasmic incompatibility (CI) is a form of reproductive manipulation caused by maternally inherited endosymbionts infecting arthropods, like Wolbachia, whereby matings between infected males and uninfected females produce few or no offspring. We report the discovery of a new CI symbiont, a strain of Spiroplasma causing CI in the parasitoid wasp Lariophagus distinguendus. Its extracellular occurrence enabled us to establish CI in uninfected adult insects by transferring <i ...[more]

PMID: 35602967

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Project description:Tsetse flies are vectors of the protozoan parasite African trypanosomes, which cause sleeping sickness disease in humans and nagana in livestock. Although there are no effective vaccines and efficacious drugs against this parasite, vector reduction methods have been successful in curbing the disease, especially for nagana. Potential vector control methods that do not involve use of chemicals is a genetic modification approach where flies engineered to be parasite resistant are allowed to replace their susceptible natural counterparts, and Sterile Insect technique (SIT) where males sterilized by chemical means are released to suppress female fecundity. The success of genetic modification approaches requires identification of strong drive systems to spread the desirable traits and the efficacy of SIT can be enhanced by identification of natural mating incompatibility. One such drive mechanism results from the cytoplasmic incompatibility (CI) phenomenon induced by the symbiont Wolbachia. CI can also be used to induce natural mating incompatibility between release males and natural populations. Although Wolbachia infections have been reported in tsetse, it has been a challenge to understand their functional biology as attempts to cure tsetse of Wolbachia infections by antibiotic treatment damages the obligate mutualistic symbiont (Wigglesworthia), without which the flies are sterile. Here, we developed aposymbiotic (symbiont-free) and fertile tsetse lines by dietary provisioning of tetracycline supplemented blood meals with yeast extract, which rescues Wigglesworthia-induced sterility. Our results reveal that Wolbachia infections confer strong CI during embryogenesis in Wolbachia-free (Gmm(Apo)) females when mated with Wolbachia-infected (Gmm(Wt)) males. These results are the first demonstration of the biological significance of Wolbachia infections in tsetse. Furthermore, when incorporated into a mathematical model, our results confirm that Wolbachia can be used successfully as a gene driver. This lays the foundation for new disease control methods including a population replacement approach with parasite resistant flies. Alternatively, the availability of males that are reproductively incompatible with natural populations can enhance the efficacy of the ongoing sterile insect technique (SIT) applications by eliminating the need for chemical irradiation.

Project description:BackgroundThe transinfection of the endosymbiotic bacterium Wolbachia provides a method to produce functionally sterile males to be used to suppress mosquito vectors. ARwP is a wPip Wolbachia infected Aedes albopictus which exhibits a bidirectional incompatibility pattern with wild-types. We coupled a modelistic approach with laboratory experiments to test ARwP as a control tool and evaluate the possible occurrence of population replacement following the release of ARwP females in a wild-type (SANG) population. Repeated male-only releases were simulated and tested in the laboratory in comparison with releases contaminated with 1% ARwP females. Model simulations also investigated how migration affects the outcome of contaminated releases. Finally, the mean level of egg fertility and the long-term evolution of populations constituted by two Wolbachia infection types were studied by testing SANG and ARwP Ae. albopictus and performing more general model simulations.ResultsThe model was parametrized with laboratory data and simulations were compared with results of biological trials. Small populations of ARwP males and females were theoretically and experimentally demonstrated to rapidly become extinct when released in larger SANG populations. Male-only releases at a 5:1 ratio with respect to the wild-type males led to a complete suppression of the SANG population in a few generations. Contaminated releases were efficient as well but led to population replacement in the long term, when the wild-type population approached eradication. Migration significantly contrasted this trend as a 5% population turnover was sufficient to avoid any risk of population replacement. At equal frequencies between ARwP and SANG individuals, the mean egg fertility of the overall population was more than halved and suppression was self-sustaining until one of the two infection types extinguished.ConclusionsIn the case of bidirectional incompatibility patterns, the repeated release of incompatible males with small percentages of contaminant females could lead to population replacement in confined environments while it could be managed to target high efficiency and sustainability in wild-type suppression when systems are open to migration. This possibility is discussed based on various contexts and taking into consideration the possibility of integration with other control methods such as SIT and the use of larvicides.

Project description:Endosymbiotic bacteria associated with eukaryotic hosts are omnipresent in nature, particularly in insects. Studying the bacterial side of host-symbiont interactions is, however, often limited by the unculturability and genetic intractability of the symbionts. Spiroplasma poulsonii is a maternally transmitted bacterial endosymbiont that is naturally associated with several Drosophila species. S. poulsonii strongly affects its host's physiology, for example by causing male killing or by protecting it against various parasites. Despite intense work on this model since the 1950s, attempts to cultivate endosymbiotic Spiroplasma in vitro have failed so far. Here, we developed a method to sustain the in vitro culture of S. poulsonii by optimizing a commercially accessible medium. We also provide a complete genome assembly, including the first sequence of a natural plasmid of an endosymbiotic Spiroplasma species. Last, by comparing the transcriptome of the in vitro culture to the transcriptome of bacteria extracted from the host, we identified genes putatively involved in host-symbiont interactions. This work provides new opportunities to study the physiology of endosymbiotic Spiroplasma and paves the way to dissect insect-endosymbiont interactions with two genetically tractable partners.IMPORTANCE The discovery of insect bacterial endosymbionts (maternally transmitted bacteria) has revolutionized the study of insects, suggesting novel strategies for their control. Most endosymbionts are strongly dependent on their host to survive, making them uncultivable in artificial systems and genetically intractable. Spiroplasma poulsonii is an endosymbiont of Drosophila that affects host metabolism, reproduction, and defense against parasites. By providing the first reliable culture medium that allows a long-lasting in vitro culture of Spiroplasma and by elucidating its complete genome, this work lays the foundation for the development of genetic engineering tools to dissect endosymbiosis with two partners amenable to molecular study. Furthermore, the optimization method that we describe can be used on other yet uncultivable symbionts, opening new technical opportunities in the field of host-microbes interactions.

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Highly transmissible cytoplasmic incompatibility by the extracellular insect symbiont Spiroplasma.

Publications

Highly transmissible cytoplasmic incompatibility by the extracellular insect symbiont <i>Spiroplasma</i>.

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