Interactions Between Tsetse Endosymbionts and Glossina pallidipes Salivary Gland Hypertrophy Virus in Glossina Hosts.

Güler Demirbas-Uzel,Vangelis Doudoumis,Kostas Bourtzis,George Tsiamis,Andrew G Parker,Adly M M Abd-Alla,Antonios A Augustinos

doi:10.3389/fmicb.2021.653880

Güler Demirbas-Uzel, Vangelis Doudoumis + Show 5 more

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https://doi.org/10.3389/fmicb.2021.653880

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Abstract

Tsetse flies are the sole cyclic vector for trypanosomosis, the causative agent for human African trypanosomosis or sleeping sickness and African animal trypanosomosis or nagana. Tsetse population control is the most efficient strategy for animal trypanosomosis control. Among all tsetse control methods, the Sterile Insect Technique (SIT) is one of the most powerful control tactics to suppress or eradicate tsetse flies. However, one of the challenges for the implementation of SIT is the mass production of target species. Tsetse flies have a highly regulated and defined microbial fauna composed of three bacterial symbionts (Wigglesworthia, Sodalis and Wolbachia) and a pathogenic Glossina pallidipes Salivary Gland Hypertrophy Virus (GpSGHV) which causes reproduction alterations such as testicular degeneration and ovarian abnormalities with reduced fertility and fecundity. Interactions between symbionts and GpSGHV might affect the performance of the insect host. In the present study, we assessed the possible impact of GpSGHV on the prevalence of tsetse endosymbionts under laboratory conditions to decipher the bidirectional interactions on six Glossina laboratory species. The results indicate that tsetse symbiont densities increased over time in tsetse colonies with no clear impact of the GpSGHV infection on symbionts density. However, a positive correlation between the GpSGHV and Sodalis density was observed in Glossina fuscipes species. In contrast, a negative correlation between the GpSGHV density and symbionts density was observed in the other taxa. It is worth noting that the lowest Wigglesworthia density was observed in G. pallidipes, the species which suffers most from GpSGHV infection. In conclusion, the interactions between GpSGHV infection and tsetse symbiont infections seems complicated and affected by the host and the infection density of the GpSGHV and tsetse symbionts.

Highlights

Tsetse flies (Diptera: Glossinidae) are medically and agriculturally important vectors of trypanosomes, the causative agents of human African trypanosomosis or sleeping sickness and African animal trypanosomosis or nagana in some 37 countries throughout Sub-Saharan Africa (Leak, 1998; Simarro et al, 2003)
After the intra-hemocoelic injections of virus suspension into the teneral adults, all six tsetse taxa were found to be susceptible to Glossina pallidipes Salivary Gland Hypertrophy Virus (GpSGHV) infection under laboratory conditions and the virus relative density increased over time in most taxa (Supplementary Figure 1)
The main findings can be summarized as follows: (a) the presence of the GpSGHV in artificially infected laboratory populations affects the densities of the three bacterial symbionts in a species-dependent manner while, in general, sex does not seem to play an important role; (b) with the exception of G. fuscipes where the high density of the GpSGHV was found in the presence of high density of Sodalis, there seems to be a negative correlation between GpSGHV and tsetse symbionts in all taxa; and (c) it seems that G. pallidipes have the lowest Wigglesworthia density compared to the other taxa

Summary

Introduction

Tsetse flies (Diptera: Glossinidae) are medically and agriculturally important vectors of trypanosomes, the causative agents of human African trypanosomosis or sleeping sickness and African animal trypanosomosis or nagana in some 37 countries throughout Sub-Saharan Africa (Leak, 1998; Simarro et al, 2003). The presence of tsetse and trypanosomes are considered as one of the most important roots of hunger and poverty in humans, hindering the adoption of more productive livestock (Dyck et al, 2021; Feldmann et al, 2021). Among available vector control methods (Jordan, 1974; Thompson et al, 1991; Green, 1994), the sterile insect technique (SIT) is considered very powerful for the sustainable management of the disease as part of area-wide integrated pest management (Vreysen et al, 2000; Hendrichs et al, 2007). SIT is based on the mass production, radiationbased sterilization and release of sterile insects over a target area to suppress or locally eliminate a target insect pest population (Dyck et al, 2021)

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