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蝌蚪中的蛙病毒流行病与肠道细菌群落失调:“安娜·卡列尼娜原则”的证据?

Ranavirus Epizootics and Gut Bacteriome Dysbiosis in Tadpoles: Evidence for the Anna Karenina Principle?

作者信息

Billet Logan S, Hernández-Gómez Obed, Skelly David K

机构信息

School of the Environment, Yale University, New Haven, Connecticut, USA.

Department of Fish, Wildlife and Conservation Ecology, New Mexico State University, Las Cruces, New Mexico, USA.

出版信息

Mol Ecol. 2025 Aug;34(16):e70022. doi: 10.1111/mec.70022. Epub 2025 Jul 9.

DOI:10.1111/mec.70022
PMID:40631371
Abstract

The microbiome plays a critical role in animal health, yet its responses to pathogens under natural conditions remain poorly understood. We investigated gut bacterial community (bacteriome) dynamics in wood frog (Rana sylvatica [Lithobates sylvaticus]) tadpoles during natural ranavirus outbreaks to understand how pathogen-induced disturbances shape the bacteriome. Using 16S rRNA sequencing, we compared the bacteriomes of tadpoles in ponds experiencing ranavirus die-offs with those from unaffected ponds before, during and after die-offs. Ranavirus infection significantly altered gut bacteriome composition and increased variability (dispersion), consistent with the Anna Karenina principle. Tadpoles with high infection intensities exhibited reduced bacterial diversity and shifts in community structure, including enrichment of some genera that have been linked previously to antiviral immunity. The predicted functional pathway analyses revealed shifts toward carbohydrate metabolism pathways during die-offs, suggesting microbial adaptation to altered host physiology under infection stress. Some bacteriome changes were detectable even before die-offs occurred, highlighting potential early indicators of infection in the gut bacteriome. In a pond that recovered after an epizootic, we observed partial recovery of some of the bacteria that shifted in relative abundance during the die-off, a pattern that may reflect microbial resilience within hosts, selective survival of tadpoles that never developed severe infections, or a combination of both mechanisms. Our findings demonstrate that ranavirus epizootics disrupt gut bacteriomes in amphibians while simultaneously eliciting potentially adaptive microbial responses. These insights underscore the complex interplay between immunity, microbiome dynamics, and environmental conditions during disease outbreaks, highlighting opportunities for microbiome-based interventions to support amphibian conservation.

摘要

微生物群落在动物健康中起着关键作用,然而在自然条件下其对病原体的反应仍知之甚少。我们调查了在自然蛙病毒爆发期间林蛙(Rana sylvatica [Lithobates sylvaticus])蝌蚪的肠道细菌群落(细菌组)动态,以了解病原体引发的干扰如何塑造细菌组。利用16S rRNA测序,我们比较了经历蛙病毒死亡事件的池塘中蝌蚪的细菌组与未受影响池塘中蝌蚪在死亡事件之前、期间和之后的细菌组。蛙病毒感染显著改变了肠道细菌组的组成并增加了变异性(离散度),这与安娜·卡列尼娜原则一致。感染强度高的蝌蚪细菌多样性降低,群落结构发生变化,包括一些先前与抗病毒免疫相关的属的富集。预测的功能途径分析表明,在死亡事件期间向碳水化合物代谢途径转变,这表明微生物在感染应激下适应宿主生理变化。甚至在死亡事件发生之前就能检测到一些细菌组的变化,这突出了肠道细菌组中感染的潜在早期指标。在一次动物疫病流行后恢复的一个池塘中,我们观察到一些在死亡事件期间相对丰度发生变化的细菌部分恢复,这种模式可能反映了宿主体内微生物的恢复力、从未发生严重感染的蝌蚪的选择性存活,或这两种机制的结合。我们的研究结果表明,蛙病毒流行会破坏两栖动物的肠道细菌组,同时引发潜在的适应性微生物反应。这些见解强调了疾病爆发期间免疫、微生物组动态和环境条件之间的复杂相互作用,突出了基于微生物组的干预措施支持两栖动物保护的机会。

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