Abstract：
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.
摘要：
温带蜜蜂（Apismellifera）受到低温和冬季行为变化相关的突然饮食变化的挑战。案例研究表明，冬季蜜蜂的肠道微生物群的大量周转，非核心细菌巴尔通体的季节性优势突出显示。然而,这种微生物周转的生物学后果和潜在机制都不清楚。特别是,我们要问的是，这种肠道变化是否与冬季饮食转变有关，是否对宿主和相关的肠道微生物组有益？我们整合了基因组学的证据，宏基因组学，和在中国北方同一地区维持的三个蜜蜂亚种的代谢组学，以描绘跨季节肠道细菌的多样性和功能变化。我们的结果表明，在所有测试的蜜蜂谱系中，巴尔通体的冬季优势都是共有的。这种季节性变化可能是冬季饮食变化的结果，其特征是由于排泄受限，花粉消耗和代谢废物的积累大大减少。巴尔通体在利用更多样化的能量底物方面显示出扩大的基因组能力，例如将代谢废物乳酸和乙醇转化为丙酮酸，自我利用的能源，也可能是宿主和其他共生体的能源。此外，巴尔通体是唯一能够产生和分泌色氨酸和苯丙氨酸的细菌，其代谢产物在蜜蜂肠道中检测到，即使所有肠道细菌都缺乏相关的消化酶。因此，这些结果表明了一种可能的机制，即肠道细菌可能通过补充蛋白质缺乏饮食中缺乏的必需氨基酸来使宿主受益。重要性冬季生存和适应主要食物变化的能力是使蜜蜂从热带到温带气候成功扩展范围的关键特征。我们的结果强调了一种新的可能性，即肠道细菌可能在严冬条件下的宿主生存中发挥了重要作用。非核心细菌巴尔通体不仅更适应冬季饮食，而且还具备为宿主提供必需营养素和重要代谢底物的能力。这种总体宿主细菌谱可能受到自然选择的青睐，在不同的蜜蜂谱系中产生一致的冬季肠道策略。相反，当寄主再次开始觅食时，在冬季保持低丰度的核心细菌恢复到其典型的优势状态，从而完成年肠道营业额。我们的研究提出了一个新的假设，即季节性肠道变化可能会改善蜜蜂的健康状况，让他们探索更多样化的气候。
