Preparatory immunity: Seasonality of mucosal skin defences and Batrachochytrium infections in Southern leopard frogs

Preparatory immunity: Seasonality of mucosal skin defences and Batrachochytrium infections in Southern leopard frogs
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DOI:
10.1111/1365-2656.13386
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发表时间:
2020-11-29
影响因子:
4.8
通讯作者:
Rollins-Smith, Louise A.
Rollins-Smith, Louise A.
中科院分区:
环境科学与生态学1区
文献类型:
--
作者:
Le Sage, Emily H.;LaBumbard, Brandon C.;Rollins-Smith, Louise A.

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准确预测气候变化对野生动物健康的影响需要更深入地了解宿主-病原体相互作用的季节性节律。两栖类病原菌,树枝状串珠壶菌(Batrachochytrium dendrobaestrium,Bd),发病率呈季节性;然而,宿主防御中的生物节律在定义这种模式中所起的作用在很大程度上仍然未知。本研究的目的是检查宿主对Bd的免疫和微生物组防御是否与感染风险以及温度和湿度的季节性波动相对应。在一年的过程中,对美国田纳西州的五个南方豹蛙种群(Rana [Lithobates] sphenocephala)进行了宿主免疫力、微生物组和病原体动态调查。青蛙拭子的病原体负荷和皮肤细菌多样性和刺激释放存储的抗菌肽(AMP)。分析分泌物以估计总疏水肽浓度、已知AMP的存在和体外Bd生长抑制的有效性。细菌读数的多样性和比例与99%匹配的序列的分离株已知抑制Bd生长在体外被用来作为一个估计的预测抗Bd功能的皮肤microbiome.Batrachochytrium dendrobatim动力学遵循预期的季节性波动,在凉爽的月份,这正好与宿主粘膜防御最有效的抗Bd。具体而言,存储AMP的浓度和表达与Bd动力学同步循环。虽然微生物组的变化随着时间的推移遵循更线性的趋势,当Bd感染的风险最高时,能够抑制Bd生长的细菌的比例最大。我们解释了秋季肽储存的增加以及向更抗Bd的转变。Bd微生物组在冬季作为随后的感染风险的准备反应,在较冷的时期,AMP合成和细菌生长缓慢,病原体压力从这种适应低温的真菌很高。考虑到储存的AMP浓度的减少,在春天温暖的温度可能意味着更大的分泌率,随后的患病率下降表明,季节性的Bd在这个主机可能部分由年度免疫节律调节,并占主导地位的温度的影响。
Accurately predicting the impacts of climate change on wildlife health requires a deeper understanding of seasonal rhythms in host-pathogen interactions. The amphibian pathogen, Batrachochytrium dendrobatidis (Bd), exhibits seasonality in incidence; however, the role that biological rhythms in host defences play in defining this pattern remains largely unknown.The aim of this study was to examine whether host immune and microbiome defences against Bd correspond with infection risk and seasonal fluctuations in temperature and humidity.Over the course of a year, five populations of Southern leopard frogs (Rana [Lithobates] sphenocephala) in Tennessee, United States, were surveyed for host immunity, microbiome and pathogen dynamics. Frogs were swabbed for pathogen load and skin bacterial diversity and stimulated to release stored antimicrobial peptides (AMPs). Secretions were analysed to estimate total hydrophobic peptide concentrations, presence of known AMPs and effectiveness of Bd growth inhibition in vitro. The diversity and proportion of bacterial reads with a 99% match to sequences of isolates known to inhibit Bd growth in vitro were used as an estimate of predicted anti-Bd function of the skin microbiome.Batrachochytrium dendrobatidis dynamics followed the expected seasonal fluctuations-peaks in cooler months-which coincided with when host mucosal defences were most potent against Bd. Specifically, the concentration and expression of stored AMPs cycled synchronously with Bd dynamics. Although microbiome changes followed more linear trends over time, the proportion of bacteria that can function to inhibit Bd growth was greatest when risk of Bd infection was highest.We interpret the increase in peptide storage in the fall and the shift to a more anti-Bd microbiome over winter as a preparatory response for subsequent infection risk during the colder periods when AMP synthesis and bacterial growth is slow and pathogen pressure from this cool-adapted fungus is high. Given that a decrease in stored AMP concentrations as temperatures warm in spring likely means greater secretion rates, the subsequent decrease in prevalence suggests seasonality of Bd in this host may be in part regulated by annual immune rhythms, and dominated by the effects of temperature.