What can a weevil teach a fly, and reciprocally? Interaction of host immune systems with endosymbionts in Glossina and Sitophilus

Abstract

The tsetse fly (Glossina genus) is the main vector of African trypanosomes, which are protozoan parasites that cause human and animal African trypanosomiases in Sub-Saharan Africa. In the frame of the IAEA/FAO program ‘Enhancing Vector Refractoriness to Trypanosome Infection’, in addition to the tsetse, the cereal weevil Sitophilus has been introduced as a comparative system with regards to immune interactions with endosymbionts. The cereal weevil is an agricultural pest that destroys a significant proportion of cereal stocks worldwide. Tsetse flies are associated with three symbiotic bacteria, the multifunctional obligate Wigglesworthia glossinidia, the facultative commensal Sodalis glossinidius and the parasitic Wolbachia. Cereal weevils house an obligatory nutritional symbiosis with the bacterium Sodalis pierantonius, and occasionally Wolbachia. Studying insect host-symbiont interactions is highly relevant both for understanding the evolution of symbiosis and for envisioning novel pest control strategies. In both insects, the long co-evolution between host and endosymbiont has led to a stringent integration of the host-bacteria partnership. These associations were facilitated by the development of specialized host traits, including symbiont-housing cells called bacteriocytes and specific immune features that enable both tolerance and control of the bacteria. In this review, we compare the tsetse and weevil model systems and compile the latest research findings regarding their biological and ecological similarities, how the immune system controls endosymbiont load and location, and how host-symbiont interactions impact developmental features including cuticle synthesis and immune system maturation. We focus mainly on the interactions between the obligate symbionts and their host’s immune systems, a central theme in both model systems. Finally, we highlight how parallel studies on cereal weevils and tsetse flies led to mutual discoveries and stimulated research on each model, creating a pivotal example of scientific improvement through comparison between relatively distant models.

The Tsetse Fly Displays an Attenuated Immune Response to Its Secondary Symbiont, Sodalis glossinidius

“…This compartmentalization strategy has recently been shown to be under the control of the same Imd-like pathway that regulates AMP expression upon bacterial infection (Maire et al, 2018). Interestingly, Imd-pathway activation and AMP production in response to ectopic infection did not interfere with the S. pierantonius endosymbiont load (Masson et al, 2015), implying that the bacteriome possesses an immune program adapted to maintaining endosymbiotic homeostasis under standard conditions while retaining the ability to mount an immune response against exogenous microbial intruders without affecting its primary symbiont (Zaidman-Rémy et al, 2018). In our study, we monitored the effects of attenuating or activating the tsetse immune system on the S. glossinidius densities in the fly.…”

The Role of Bacterial Symbionts in Triatomines: An Evolutionary Perspective

“…In many cases, beneficial symbionts from the microbiota are essential and have allowed insects to expand and adapt to different environments [ 1 , 2 , 3 , 4 ]. The abundance, tissue specificity, taxa represented, and location (including intra-or extracellular) of these symbionts and the general microbiota is variable among insects, and in many cases depict tight coevolutionary histories [ 5 , 6 , 7 ].…”

DNA transduction inSodalisspecies: implications for the genetic modification of uncultured endosymbionts of insects

“…CC-BY-NC-ND 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made endosymbionts could also be subjected to infection and genetic modification via P1, if they transiently exit host cells (Zaidman-Rémy et al, 2018).…”