Field Kenneth A, Sewall Brent J, Prokkola Jenni M, Turner Gregory G, Gagnon Marianne F, Lilley Thomas M, Paul White J, Johnson Joseph S, Hauer Christopher L, Reeder DeeAnn M
Department of Biology, Bucknell University, Lewisburg, Pennsylvania.
Department of Biology, Temple University, Philadelphia, Pennsylvania.
Mol Ecol. 2018 Aug 6. doi: 10.1111/mec.14827.
Hibernation, the use of prolonged torpor to depress metabolism, is employed by mammals to conserve resources during extended periods of extreme temperatures and/or resource limitation. Mammalian hibernators arouse to euthermy periodically during torpor for reasons that are not well understood, and these arousals may facilitate immune processes. To determine whether arousals enable host responses to pathogens, we used dual RNA-Seq and a paired sampling approach to examine gene expression in a hibernating bat, the little brown myotis (Myotis lucifugus). During torpor, transcript levels differed in only a few genes between uninfected wing tissue and adjacent tissue infected with Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome. Within 70-80 min after emergence from torpor, large changes in gene expression were observed due to local infection, particularly in genes involved in pro-inflammatory host responses to fungal pathogens, but also in many genes involved in immune responses and metabolism. These results support the hypothesis that torpor is a period of relative immune dormancy and arousals allow for local immune responses in infected tissues during hibernation. Host-pathogen interactions were also found to regulate gene expression in the pathogen differently depending on the torpor state of the host. Hibernating species must balance the benefits of energy and water conservation achieved during torpor with the costs of decreased immune competence. Interbout arousals allow hibernators to optimize these, and other, trade-offs during prolonged hibernation by enabling host responses to pathogens within brief, periodic episodes of euthermy.
冬眠是哺乳动物在极端温度和/或资源有限的长时间内利用长时间的蛰伏来降低新陈代谢,以保存资源的一种方式。哺乳动物冬眠者在蛰伏期间会周期性地苏醒到正常体温,其原因尚不清楚,而这些苏醒可能有助于免疫过程。为了确定苏醒是否能使宿主对病原体产生反应,我们使用了双RNA测序和配对采样方法来研究冬眠蝙蝠——小棕蝠(Myotis lucifugus)的基因表达。在蛰伏期间,未感染的翼组织和感染了导致白鼻综合征的真菌病原体——毁灭拟裸球壳菌的相邻组织之间,只有少数基因的转录水平存在差异。从蛰伏中苏醒后70 - 80分钟内,由于局部感染,观察到基因表达发生了巨大变化,特别是在参与对真菌病原体的促炎性宿主反应的基因中,但也在许多参与免疫反应和新陈代谢的基因中。这些结果支持了这样一种假设,即蛰伏是一个相对免疫休眠的时期,而苏醒允许在冬眠期间受感染组织中产生局部免疫反应。还发现宿主 - 病原体相互作用根据宿主的蛰伏状态不同地调节病原体中的基因表达。冬眠物种必须在蛰伏期间实现的能量和水分保存的益处与免疫能力下降的成本之间取得平衡。间歇性苏醒使冬眠者能够在长时间冬眠期间通过在短暂的、周期性的正常体温发作期间使宿主对病原体产生反应来优化这些以及其他权衡。