Combining paratransgenesis with SIT: impact of ionizing radiation on the DNA copy number of Sodalis glossinidius in tsetse flies

Abstract

BackgroundTsetse flies (Diptera: Glossinidae) are the cyclical vectors of the causative agents of African Trypanosomosis, which has been identified as a neglected tropical disease in both humans and animals in many regions of sub-Saharan Africa. The sterile insect technique (SIT) has shown to be a powerful method to manage tsetse fly populations when used in the frame of an area-wide integrated pest management (AW-IPM) program. To date, the release of sterile males to manage tsetse fly populations has only been implemented in areas to reduce transmission of animal African Trypanosomosis (AAT). The implementation of the SIT in areas with Human African Trypanosomosis (HAT) would require additional measures to eliminate the potential risk associated with the release of sterile males that require blood meals to survive and hence, might contribute to disease transmission. Paratransgenesis offers the potential to develop tsetse flies that are refractory to trypanosome infection by modifying their associated bacteria (Sodalis glossinidius) here after referred to as Sodalis. Here we assessed the feasibility of combining the paratransgenesis approach with SIT by analyzing the impact of ionizing radiation on the copy number of Sodalis and the vectorial capacity of sterilized tsetse males.ResultsAdult Glossina morsitans morsitans that emerged from puparia irradiated on day 22 post larviposition did not show a significant decline in Sodalis copy number as compared with non-irradiated flies. Conversely, the Sodalis copy number was significantly reduced in adults that emerged from puparia irradiated on day 29 post larviposition and in adults irradiated on day 7 post emergence. Moreover, irradiating 22-day old puparia reduced the copy number of Wolbachia and Wigglesworthia in emerged adults as compared with non-irradiated controls, but the radiation treatment had no significant impact on the vectorial competence of the flies.ConclusionAlthough the radiation treatment significantly reduced the copy number of some tsetse fly symbionts, the copy number of Sodalis recovered with time in flies irradiated as 22-day old puparia. This recovery offers the opportunity to combine a paratransgenesis approach – using modified Sodalis to produce males refractory to trypanosome infection – with the release of sterile males to minimize the risk of disease transmission, especially in HAT endemic areas. Moreover, irradiation did not increase the vector competence of the flies for trypanosomes.Electronic supplementary materialThe online version of this article (10.1186/s12866-018-1283-8) contains supplementary material, which is available to authorized users.

Increased biting rate and decreasedWolbachiadensity in irradiatedAedesmosquitoes

“…nevertheless, the density of Wolbachia is markedly affected by radiation doses applied to other insect species to achieve sterilization [28]. The results presented in this study highlighted an overall decrease in the density of Wolbachia in irradiated females, and this decrease was negatively correlated to the age of the pupae at the time of the radiation treatment and positively correlated to female aging.…”

Quorum sensing sets the stage for the establishment and vertical transmission of Sodalis praecaptivus in tsetse flies

“…This difference may be explained by the fact that female tsetse harbor significantly higher densities of S . glossinidius [ 37 ], perhaps yielding sufficient ( S . glossinidius -derived) OHHL to suppress killing by the ΔypeI mutant strain.…”

“…However, this effect was not observed in male flies, with members of both the -Sg and +Sg groups showing a similar mean longevity ( Fig 3B, 19.9 ± 3.4 d versus 22.3 ± 6.0 d for +Sg males and -Sg males; respectively, Mann-Whitney U test, p = 0.6825). This difference may be explained by the fact that female tsetse harbor significantly higher densities of S. glossinidius [37], perhaps yielding sufficient (S. glossinidius-derived) OHHL to suppress killing by the ΔypeI mutant strain. Further, it is possible that the difference in survival observed between the sexes may be a function of the different lifespans of males and females [38], where the significantly shorter life span of males limits our ability to detect a rescue effect.…”

The Insect Pest Control Laboratory of the Joint FAO/IAEA Programme: Ten Years (2010–2020) of Research and Development, Achievements and Challenges in Support of the Sterile Insect Technique

“…No significant impact of irradiation treatment was found on Wigglesworthia and Wolbachia densities. In addition, the vectorial capacity of the sterile males for trypanosome was not affected by an irradiation treatment [ 131 ].…”