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

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 symbiosispromoting 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.

Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids

“…The regulation of virulence and titer is important in the establishment of vertical transmission. Self-regulation of both titer and virulence through quorum sensing has been demonstrated in Sodalis praecaptivus and allows this species to establish vertically transmitted infections in weevil and tsetse fly hosts (55,67). Whether mutualistic S. symbiotica strains have relied on similar mechanisms to establish persistent vertical transmission in aphids is unclear.…”

The Pathfinder plasmid toolkit for genetically engineering newly isolated bacteria enables the study ofDrosophila-colonizingOrbaceae

“…1B), which might be useful if the markers are expressed at lower levels in other species. To demonstrate functionality in a more distantly-related bacterium, we tested conjugation of the Pathfinder mix into Sodalis praecaptivus HS T , a human wound bacterial isolate previously shown to colonize weevils and tsetse flies (37)(38)(39). As with E. coli, we were able to recover transconjugants for every plasmid except for pSL3.…”

Ecological Divergence Within the Enterobacterial Genus Sodalis: From Insect Symbionts to Inhabitants of Decomposing Deadwood

“…Other related Sodalis members, the previously described free-living S. praecaptivus and symbiont Sodalis pierantonius strain SOPE, do not show a deadwood preference (Oakeson et al, 2014). While for the symbiont this is not surprising, the main habitat and ecological functions of S. praecaptivus remain to be identified, considering its genome composition (which is closer to symbionts than to wood-associated strains), wood cultivation source and ability to grow in human and insect tissues (Clayton et al, 2012;Enomoto et al, 2017;Munoz et al, 2020). Based on the presence of virulence factors, S. praecaptivus may represent a plant pathogen transmitted by insects (Clayton et al, 2012) and thus may prefer living plants rather than decomposing wood.…”

“…Consequently, due to its wide spectrum of genes and high coding density, S. praecaptivus is able to utilize several carbon (C) sources, including chitin and plant sugars (cellobiose, xylose, rhamnose) and N sources, such as ammonia and nitrate (Chari et al, 2015). While S. praecaptivus is host-independent, it is able to colonize weevils and tsetse flies through quorum sensing suppression of its virulence, which suggests a mechanism of insect symbiosis development in the Sodalis group (Enomoto et al, 2017;Munoz et al, 2020). Despite the well-characterized phylogeny and genome properties of the Sodalis group, a systematic approach to assess the environmental distribution of free-living Sodalis strains has not been performed.…”