Metabolomic profiles of stony coral species from the Dry Tortugas National Park display inter- and intraspecies variation.

IF 5 2区 生物学 Q1 MICROBIOLOGY mSystems Pub Date : 2024-11-19 DOI:10.1128/msystems.00856-24
Jessica M Deutsch, Alyssa M Demko, Olakunle A Jaiyesimi, Gabriel Foster, Adelaide Kindler, Kelly A Pitts, Tessa Vekich, Gareth J Williams, Brian K Walker, Valerie J Paul, Neha Garg
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引用次数: 0

Abstract

Coral reefs are experiencing unprecedented loss in coral cover due to increased incidence of disease and bleaching events. Thus, understanding mechanisms of disease susceptibility and resilience, which vary by species, is important. In this regard, untargeted metabolomics serves as an important hypothesis-building tool enabling the delineation of molecular factors underlying disease susceptibility or resilience. In this study, we characterize metabolomes of four species of visually healthy stony corals, including Meandrina meandrites, Orbicella faveolata, Colpophyllia natans, and Montastraea cavernosa, collected at least a year before stony coral tissue loss disease reached the Dry Tortugas, Florida, and demonstrate that both symbiont and host-derived biochemical pathways vary by species. Metabolomes of Meandrina meandrites displayed minimal intraspecies variability and the highest biological activity against coral pathogens when compared to other species in this study. The application of advanced metabolite annotation methods enabled the delineation of several pathways underlying interspecies variability. Specifically, endosymbiont-derived vitamin E family compounds, betaine lipids, and host-derived acylcarnitines were among the top predictors of interspecies variability. Since several metabolite features that contributed to inter- and intraspecies variation are synthesized by the endosymbiotic Symbiodiniaceae, which could be a major source of these compounds in corals, our data will guide further investigations into these Symbiodiniaceae-derived pathways.

Importance: Previous research profiling gene expression, proteins, and metabolites produced during thermal stress have reported the importance of endosymbiont-derived pathways in coral bleaching resistance. However, our understanding of interspecies variation in these pathways among healthy corals and their role in diseases is limited. We surveyed the metabolomes of four species of healthy corals with differing susceptibilities to the devastating stony coral tissue loss disease and applied advanced annotation approaches in untargeted metabolomics to determine the interspecies variation in host and endosymbiont-derived pathways. Using this approach, we propose the survey of immune markers such as vitamin E family compounds, acylcarnitines, and other metabolites to infer their role in resilience to coral diseases. As time-resolved multi-omics datasets are generated for disease-impacted corals, our approach and findings will be valuable in providing insight into the mechanisms of disease resistance.

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干特尔图加斯国家公园石珊瑚物种的代谢组图谱显示了物种间和物种内的差异。
由于疾病和白化现象的增加,珊瑚礁的珊瑚覆盖率正在经历前所未有的损失。因此,了解因物种而异的疾病易感性和恢复力机制非常重要。在这方面,非靶向代谢组学是一种重要的假设构建工具,可帮助确定疾病易感性或恢复力的分子因素。在这项研究中,我们描述了在石珊瑚组织缺失病到达佛罗里达州干特尔图加斯之前至少一年采集的四种视觉健康石珊瑚(包括 Meandrina meandrites、Orbicella faveolata、Colpophyllia natans 和 Montastraea cavernosa)的代谢组特征,并证明共生体和宿主衍生的生化途径因物种而异。与本研究中的其他物种相比,Meandrina meandrites 的代谢组显示出最小的种内变异性和最高的抗珊瑚病原体生物活性。通过应用先进的代谢物注释方法,确定了物种间变异的几种基本途径。具体来说,内共生体衍生的维生素 E 家族化合物、甜菜碱脂质和宿主衍生的酰基肉碱是预测种间变异性的主要因素。由于导致种间和种内变异的几种代谢物特征是由内共生的共生藻合成的,而共生藻可能是珊瑚中这些化合物的主要来源,因此我们的数据将指导对这些共生藻衍生途径的进一步研究:此前对热应力期间产生的基因表达、蛋白质和代谢物进行的研究表明,内共生菌衍生途径在珊瑚抗白化过程中具有重要作用。然而,我们对这些途径在健康珊瑚中的种间差异及其在疾病中的作用了解有限。我们调查了对毁灭性的石珊瑚组织缺失症具有不同易感性的四种健康珊瑚的代谢组,并应用非靶向代谢组学的先进注释方法来确定宿主和内共生体衍生途径的种间变异。利用这种方法,我们建议对维生素 E 家族化合物、酰基肉碱和其他代谢物等免疫标记物进行调查,以推断它们在珊瑚疾病恢复能力中的作用。随着受疾病影响珊瑚的时间分辨多组学数据集的生成,我们的方法和发现将对深入了解抗病机制非常有价值。
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来源期刊
mSystems
mSystems Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
10.50
自引率
3.10%
发文量
308
审稿时长
13 weeks
期刊介绍: mSystems™ will publish preeminent work that stems from applying technologies for high-throughput analyses to achieve insights into the metabolic and regulatory systems at the scale of both the single cell and microbial communities. The scope of mSystems™ encompasses all important biological and biochemical findings drawn from analyses of large data sets, as well as new computational approaches for deriving these insights. mSystems™ will welcome submissions from researchers who focus on the microbiome, genomics, metagenomics, transcriptomics, metabolomics, proteomics, glycomics, bioinformatics, and computational microbiology. mSystems™ will provide streamlined decisions, while carrying on ASM''s tradition of rigorous peer review.
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