Bactrocera oleae gut microbiome shows metabolic potential to complement the decline of symbiotic ‘Candidatus Erwinia dacicola’ in artificially-reared flies

The olive fly Bactrocera oleae has a gut microbiome dominated by the symbiont ‘ Candidatus Erwinia dacicola’. Laboratory rearing conditions result in symbiont loss, reducing insect fitness. This work combined transcriptomics and culture-based approaches to examine B. oleae gut microbiome dynamics over multiple artificially-reared generations prior to complete symbiont loss. Ca. E. dacicola was dominant in field-derived parental generation but decreased in laboratory-reared offspring, which showed increased abundance of other bacterial taxa. Bacterial genes involved in nitrogen biosynthesis, glycolysis, and coenzyme A production pathways showed consistent expression differences between generations, with higher levels in flies with high Ca. E. dacicola density. Genomic pathway potential for these processes was also identified among other culturable gut community members. Laboratory-reared flies had significant infections with cultivable Enterobacter hormaechei , Pseudomonas sp., and Stenotrophomonas maltophilia , showing genomic pathway potential overlapping with Ca. E. dacicola and distinct genomic pathway specializations among isolates. These findings indicate that culturable bacteria with overlapping metabolic pathway potential may represent promising candidates for functionally compensating for the uncultivable obligate symbiont when it cannot be retained by the host.