Wolbachia Symbiont Infections Induce Strong Cytoplasmic Incompatibility in the Tsetse Fly Glossina morsitans

Stanford University, United States of America
PLoS Pathogens (Impact Factor: 7.56). 12/2011; 7(12):e1002415. DOI: 10.1371/journal.ppat.1002415
Source: PubMed


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.

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    • "In addition to its role in the Sodalis / Wolbachia couple ( dissemination of flies harboring the recom - binant Sodalis ) , Wolbachia may be used alone . The embryonic death caused by Wolbachia - induced cytoplasmic incompatibility can be applied to suppress tsetse fly populations ( Alam et al . , 2011 ; Aksoy et al . , 2013 ) . Another advantage of the Wolbachia symbiont is its capability to inhibit the development of trypanosomes in tsetse ( Table 2 ) ( Aksoy et al . , 2013 ) . One alternative to paratransgenesis could be to increase the prevalence of gut bacteria that are naturally present in tsetse flies and that are capable of re"
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    ABSTRACT: The tsetse fly vector transmits the protozoan Trypanosoma brucei, responsible for Human African Trypanosomiasis, one of the most neglected tropical diseases. Despite a recent decline in new cases, it is still crucial to develop alternative strategies to combat this disease. Here, we review the literature on the factors that influence trypanosome transmission from the fly vector to its vertebrate host (particularly humans). These factors include climate change effects to pathogen and vector development (in particular climate warming), as well as the distribution of host reservoirs. Finally, we present reports on the relationships between insect vector nutrition, immune function, microbiota and infection, to demonstrate how continuing research on the evolving ecology of these complex systems will help improve control strategies. In the future, such studies will be of increasing importance to understand how vector-borne diseases are spread in a changing world.
    The ISME Journal 12/2014; 9(7). DOI:10.1038/ismej.2014.236 · 9.30 Impact Factor
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    • "Sodalis has a broad tissular tropism and can also be found in the hemolymph, salivary glands, etc. (Cheng and Aksoy, 1999). The third symbiont, Wolbachia (O'Neill et al., 1993), belongs to the Rickettsiaceae family and causes cytoplasmic incompatibility in tsetse flies (Alam et al., 2011). S. glossinidius has been suspected of being involved in the trypanosome establishment process (Maudlin and Ellis, 1985; Welburn et al., 1993). "
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    ABSTRACT: Tsetse flies (Glossina sp.) that transmit trypanosomes causing human (and animal) African trypanosomiasis (HAT and AAT, respectively) harbor symbiotic microorganisms, including the obligate primary symbiont Wigglesworthia glossinidia. A relationship between Wigglesworthia and tsetse fly infection by trypanosomes has been suggested, as removal of the symbiont results in a higher susceptibility to midgut infection in adult flies. To investigate this relationship and to decipher the role of W. glossinidia in the fly's susceptibility to trypanosome infection, we challenged flies with trypanosomes and subsequently analyzed and compared the transcriptomes of W. glossinidia from susceptible and refractory tsetse flies at three time points (3, 10, and 20 days). More than 200 W. glossinidia genes were found to be differentially expressed between susceptible and refractory flies. The high specificity of these differentially expressed genes makes it possible to distinguish Wigglesworthia inhabiting these two distinct groups of flies. Furthermore, gene expression patterns were observed to evolve during the infection time course, such that very few differentially expressed genes were found in common in Wigglesworthia from the 3-, 10- and 20-day post-feeding fly samples. The overall results clearly demonstrate that the taking up of trypanosomes by flies, regardless of whether flies proceed with the developmental program of Trypanosoma brucei gambiense, strongly alters gene expression in Wigglesworthia. These results therefore provide a novel framework for studies that aim to decrease or even abolish tsetse fly vector competence.
    Frontiers in Microbiology 11/2014; DOI:10.3389/fmicb.2014.00620 · 3.99 Impact Factor
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    • "S. glossinidius, originally classified as a rickettsia-like organism [3], has no clear role within the tsetse but is thought to play a part in susceptibility to trypanosome infection [4–6]. Wolbachia has recently been shown to be involved in cytoplasmic incompatibility in tsetse [7]. "
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    ABSTRACT: Background Tsetse flies are the biological vectors of African trypanosomes, the causative agents of sleeping sickness in humans and nagana in animals. The tsetse endosymbiont Sodalis glossinidius has been suggested to play a role in tsetse susceptibility to infection. Here we investigate the prevalence of African trypanosomes within tsetse from the Luambe National Park, Zambia and if there is an association between S. glossinidius and presence of trypanosomes within the tsetse examined. Methods Tsetse representing three species (Glossina brevipalpis, Glossina morsitans morsitans and Glossina pallidipes), were sampled from Luambe National Park, Zambia. Following DNA extraction, PCR was used to examine the tsetse for presence of trypanosomes and the secondary endosymbiont S. glossinidius. Results S. glossinidius infection rates varied significantly between tsetse species, with G. brevipalpis (93.7%) showing the highest levels of infection followed by G. m. morsitans (17.5%) and G. pallidipes (1.4%). ITS-PCR detected a wide variety of trypanosomes within the tsetse that were analysed. Significant differences were found in terms of trypanosome presence between the three tsetse species. A high proportion of G. m. morsitans were shown to carry T. brucei s.l. DNA (73.7%) and of these around 50% were positive for Trypanosoma brucei rhodesiense. T. vivax, T. godfreyi, T. simiae, T. simiae Tsavo and T. congolense were also detected. No association was found between the occurrence of S. glossinidius and the presence of trypanosome DNA in any of the three tsetse species tested. Conclusion The current work shows that T. b. rhodesiense was circulating in Luambe National Park, representing a risk for people living in the park or surrounding area and for tourists visiting the park. The differences in trypanosome DNA presence observed between the different tsetse species tested may indicate host feeding preferences, as the PCR will not discriminate between a fly with an active/resident infection compared to a refractory fly that has fed on an infected animal. This makes it difficult to establish if S. glossinidius may play a role in the susceptibility of tsetse flies to trypanosome infection.
    Parasites & Vectors 08/2014; 7(1):378. DOI:10.1186/1756-3305-7-378 · 3.43 Impact Factor
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