Epstein Hannah E, Brown Tanya, Akinrinade Ayọmikun O, McMinds Ryan, Pollock F Joseph, Sonett Dylan, Smith Styles, Bourne David G, Carpenter Carolina S, Knight Rob, Willis Bette L, Medina Mónica, Lamb Joleah B, Thurber Rebecca Vega, Zaneveld Jesse R
School of Life Sciences, University of Essex, Wivenhoe Park, Colchester, Essex, CO4 3SQ, UK.
Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, OR, 97331, USA.
Anim Microbiome. 2025 Jan 3;7(1):1. doi: 10.1186/s42523-024-00370-z.
Evolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea.
Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the "Global Coral Microbiome Project") and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates.
These results demonstrate that the evolution of Endozoicomonas symbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs.
生活史策略之间的进化权衡在动物进化中很重要。由于微生物可影响宿主生理学的多个方面,包括生长速率以及对疾病或压力的易感性,动物与微生物共生关系的变化有可能调节生活史权衡。石珊瑚提供了一个生物多样性丰富、数据充足且与生态相关的宿主系统来探究这一观点。
我们采用比较方法,通过开展一项跨物种珊瑚微生物组调查(“全球珊瑚微生物组计划”),并将结果与长期全球疾病流行率及珊瑚特征数据相结合,来测试在4.25亿年的珊瑚进化过程中,珊瑚微生物组是否与疾病易感性相关。在系统发育背景下解读这些数据时,我们发现微生物优势地位可预测疾病易感性,并将这种优势 - 疾病关联追溯到一个假定有益的共生菌属——内共生菌属。在40个珊瑚属中,珊瑚组织内共生菌属的相对丰度解释了疾病易感性变异的30%以及微生物组优势地位变异的60%,同时也与高生长速率密切相关。
这些结果表明,珊瑚内共生菌共生关系的进化与疾病流行率和生长速率均相关,并提示了一种调节作用。探索这些发现的机制基础对于我们理解微生物共生如何影响动物生活史权衡至关重要。