Temperate honey bees (Apis mellifera) are challenged by low temperatures and abrupt dietary shifts associated with behavioral changes during winter. Case studies have revealed drastic turnover in the gut microbiota of winter bees, highlighted by the seasonal dominance of a non-core bacterium Bartonella. However, neither biological consequence nor underlying mechanism of this microbial turnover is clear. In particular, we ask whether such changes in gut profile are related to winter dietary shift and possibly beneficial to host and associated gut microbiome? Here, we integrated evidences from genomics, metagenomics, and metabolomics in three honey bee subspecies maintained at the same locality of northern China to profile both diversity and functional variations in gut bacteria across seasons. Our results showed that winter dominance of Bartonella was shared in all tested honey bee lineages. This seasonal change was likely a consequence of winter dietary shifts characterized by greatly reduced pollen consumption and accumulation of metabolic waste due to restricted excretion. Bartonella showed expanded genomic capacity in utilizing more diverse energy substrates, such as converting metabolic wastes lactate and ethanol into pyruvate, an energy source for self-utilization and possibly also for host and other symbionts. Furthermore, Bartonella was the only bacterium capable of both producing and secreting tryptophan and phenylalanine, whose metabolic products were detected in bee guts, even though all gut bacteria lacked relevant digestion enzymes. These results thus suggested a possible mechanism where the gut bacteria might benefit the host by supplementing them with essential amino acids lacking in a protein shortage diet. IMPORTANCE The abilities to survive winter and to adapt to major food changes are key traits that have enabled successful range expansion of the honey bees from the tropic to temperate climate. Our results highlighted a new possibility that gut bacteria may have played an important role in host survival of the severe winter condition. The non-core bacterium Bartonella is not only more adaptive to the winter diet but is also equipped with the capacity to provide the host with essential nutrients and important metabolic substrates. This overall host-bacterium profile is probably favored by natural selection, resulting in a consistent winter gut strategy across varied honey bee lineages. Conversely, when the hosts start to forage again, core bacteria maintained at low abundance during winter returned to their typical dominant status, thus completing the annual gut turnover. Our study suggests a new hypothesis where seasonal gut variations may improve the fitness of the honey bee, allowing them to explore more diverse climates.
Keywords: Apis mellifera; Bartonella; essential amino acids; overwintering; pollen shortage.