An loss of independence: genomic insights into a pest fruit fly-bacterial mutualism

Tephritid fruit flies are invasive species of ripening fruit and vegetables. The olive fly (Bactrocera oleae) a specialist of olives, harbors a symbiotic gut bacterium Candidatus Erwinia dacicola, which is crucial to the olive flys exploitation of Oleaceae. This study characterized the genome of Ca. E. dacicola to investigate functional pathways that facilitate its obligate symbiosis. We used an extremely high-quality Ca. E. dacicola genome produced in tandem with an olive fly genome and paired that reference with transcriptomics. Of 4,675 genes, 1,783 (38.13%) were classified as pseudogenes. Overall, many pathways are complete, mostly associated with nutritional components. The symbiont also has genes encoding hypothetical proteins to degrade the phenolics in olives. Some pathways were heavily pseudogeneized, suggesting that Ca. E. dacicola have impaired functions in generalized metabolism, carbon utilization, pathogenicity, and signaling systems. Gene selection analyses in Ca. E. dacicola compared to related organisms, indicated positive selection on genes related to amino acid metabolism, carbon utilization, secretion and transport, and energy production. Our results indicate that the main service likely provided by Ca. E. dacicola is the production of amino acids and metabolism of oleuropein. The high pseudogenization rate implies incipient erosion of a formerly free-living symbiont.