Genomic features underlying the evolutionary transitions of Apibacter to honey bee gut symbionts

Abstract

The symbiotic bacteria associated with honey bee gut have likely transformed from a free-living or parasitic lifestyle, through a close evolutionary association with the insect host. However, little is known about the genomic mechanism underlying bacterial transition to exclusive adaptation to the bee gut. Here we compared the genomes of bee gut symbionts Apibacter with their close relatives living in different lifestyles. We found that despite of general reduction in the Apibacter genome, genes involved in amino acid synthesis and monosaccharide detoxification were retained, which were likely beneficial to the host. Interestingly, the microaerobic Apibacter species have specifically acquired genes encoding for the nitrate respiration (NAR). The NAR system is also conserved in the cohabiting bee microbe Snodgrassella, although with a differed structure. This convergence implies a crucial role of respiratory nitrate reduction for microaerophilic microbiomes to colonize bee gut epithelium. Genes involved in lipid, histidine degradation are substantially lost in Apibacter, indicating a transition of the energy source utilization. Particularly, genes involved in the phenylacetate degradation to generate host toxic compounds, as well as other virulence factors were lost, suggesting the loss of pathogenicity. Antibiotic resistance genes were only sporadically distributed among Apibacter species, but condensed in their pathogenic relatives, which may be related to the remotely living feature and less exposure to antibiotics of their bee hosts. Collectively, this study advances our understanding of genomic transition underlying specialization in bee gut symbionts. ImportanceInvestigations aiming to uncover the genetic determinants underlying the transition to a gut symbiotic lifestyle were scarce. The vertical transmitted honey bee gut symbionts of genus Apibacter provided an rare opportunity to tackle this, as evolving from family Flavobacteriaceae, they had phylogenetic close relatives living various lifestyles. Here, we documented that Apibacter have both preserved and horizontally acquired host beneficial genes including monosaccharides detoxification that may have seeded a mutualistic relationship with the host. In contrast, multiple virulence factors and antibiotic resistance genes have been lost. Importantly, an highly efficient and genomic well organized respiratory nitrate reduction pathway is conserved across all Apibacter spp., as well as in majority of Snodgrassella, which colonize the same habitat as Apibacter, suggesting an crucial role it played in living inside the gut. These findings highlight genomic changes paving ways to the transition to a honey bee gut symbiotic lifestyle.