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

The gut bacteria of honey bee recognized as a mutualistic partner with the insect host might have originated from a free-living or parasitic lifestyle. However, little is known about the genomic features underlying this lifestyle transition. Here we compared the genomes of bee gut bacteria Apibacter with their close relatives living in different lifestyles. We found that despite general reduction in the Apibacter genome, genes involved in amino acid synthesis and monosaccharide detoxification were retained, which is putatively beneficial to the host. Interestingly, the microaerobic Apibacter species specifically acquired genes encoding for the nitrate respiration (NAR). These together with nitrate transporter and enzymatic cofactor synthesis genes were found clustered in the genomes. The NAR system is also conserved in the cohabitating bee gut microbe Snodgrassella, although with a different structure. This convergence suggests a key role of respiratory nitrate reduction for microaerophilic microbiomes to colonize bee gut epithelium. Genes involved in lipid, histidine degradation were found partially or completely lost in Apibacter. Particularly, genes encoding for the conversion to the toxic intermediates in phenylacetate degradation, as well as other potential virulence factors, are specifically lost in Apibacter group. Antibiotic resistance genes are only sporadically distributed among Apibacter species, but are prevalent in their relatives, which may be related to the remotely living feature and less exposure to antibiotics of their bee hosts. Collectively, this study advanced our knowledge of genomic features specialized to bee gut symbionts.