Abstract
Bacterial virulence factors facilitate host colonization and set the stage for the evolution of parasitic and mutualistic interactions. The Sodalis-allied clade of bacteria exhibit striking diversity in the range of both plant and animal feeding insects they inhabit, suggesting the appropriation of universal molecular mechanisms that facilitate establishment. Here, we report on the infection of the tsetse fly by free-living Sodalis praecaptivus, a close relative of many Sodalis-allied symbionts. Key genes involved in quorum sensing, including the homoserine lactone synthase (ypeI) and response regulators (yenR and ypeR) are integral for the benign colonization of S. praecaptivus. Mutants lacking ypeI, yenR and ypeR compromised tsetse survival as a consequence of their inability to repress virulence. Genes under quorum sensing, including homologs of the binary insecticidal toxin PirAB and a putative symbiosis-promoting factor CpmAJ, demonstrated negative and positive impacts, respectively, on tsetse survival. Taken together with results obtained from experiments involving weevils, this work shows that quorum sensing virulence suppression plays an integral role in facilitating the establishment of Sodalis-allied symbionts in diverse insect hosts. This knowledge contributes to the understanding of the early evolutionary steps involved in the formation of insect-bacterial symbiosis. Further, despite having no established history of interaction with tsetse, S. praecaptivus can infect reproductive tissues, enabling vertical transmission through adenotrophic viviparity within a single host generation. This creates an option for the use of S. praecaptivus in the biocontrol of insect disease vectors via paratransgenesis.
Highlights
Bacteria occupy countless niches, including numerous adaptive associations with plants and animals
It was previously shown that S. praecaptivus, a free-living relative of the Sodalis-host associated symbionts found within many different insects, was capable of sustaining infections within Si. zeamais grain weevils cleared of their endogenous Ca
S. praecaptivus was introduced into flies either per os in heat-inactivated (HI) blood or by intrathoracic microinjection at concentrations similar to those previously used for the inoculation of foreign bacteria into tsetse [27,32] (Table 1)
Summary
Bacteria occupy countless niches, including numerous adaptive (mutualistic) associations with plants and animals. Bacterial genera that are capable of infecting a wide range of arthropods and persisting by vertical transmission (such as Wolbachia, Arsenophonus, Rickettsia and Sodalis [9,10,11,12]) offer insight into these molecular features. Deciphering these key traits that facilitate host relations is useful for developing applications which require establishment and maintenance of genetically modified symbionts within a host, such as the use of probiotics to restore the composition of gut flora or the implementation of paratransgenesis to express novel genes in a host using genetically engineered symbionts [13,14]. Following S. praecaptivus introduction, tsetse were returned to colony rearing conditions and fed defibrinated bovine blood with mortality recorded every 48 hours
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