Lipid metabolic response patterns to heat stress in two Symbiodiniaceae species with different environmental sensitivities (Cladocopium goreaui and Durusdinium trenchii)
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摘要: 虫黄藻是珊瑚共生体系中不可或缺的伙伴，不同种类的虫黄藻对环境胁迫的敏感性不同，从而影响珊瑚宿主的环境适应能力。本研究从脂质代谢角度，探讨了广泛分布的两种珊瑚共生虫黄藻—环境敏感型Cladocopium goreaui（C. goreaui）和环境耐受型Durusdinium trenchii（D. trenchii）在热胁迫下的应激模式。研究发现，热胁迫显著影响两者的生长密度、光合色素含量、称为光系统II（PSII）的光化学效率（Fv/Fm）及抗氧化活性，且差异均具有统计学意义（P < 0.05）。脂质组学显示，C. goreaui和D. trenchii在应对热胁迫时，磷脂酰胆碱、甘油三酯、磷脂酰乙醇胺和溶血磷脂酰胆碱等脂质差异代谢物显著富集于甘油磷脂代谢、甘油酯代谢及多不饱和脂肪酸相关代谢通路。值得注意的是，两者在鞘脂代谢方面存在显著差异：D. trenchii通过下调神经酰胺水平减少细胞氧化应激损伤，调控自噬过程，并适应膜流动性的变化；而C. goreaui主要通过上调富含多不饱和脂肪酸的脂质分子，以维持膜稳定性和调控信号传导。深入解析不同环境敏感性虫黄藻在热胁迫下的脂质代谢应激机制，有助于从共生伙伴的角度，为提升珊瑚对环境变化的适应能力提供新的见解。Abstract: Symbiodiniaceae are indispensable partners in the coral symbiotic system, and different species exhibit varying sensitivities to environmental stress, thereby influencing the environmental adaptability of their coral hosts. This study investigates the stress response patterns of two widely distributed coral symbiotic Symbiodiniaceae species—environmentally sensitive Cladocopium goreaui (C. goreaui) and environmentally tolerant Durusdinium trenchii (D. trenchii)—under heat stress from the perspective of lipid metabolism. The results showed that heat stress significantly affected their cell density, photosynthetic pigment content, photochemical efficiency of photosystem II (Fv/Fm), and antioxidant activity, with statistically significant differences (P < 0.05). Lipidomics revealed that lipid-differentiated metabolites such as phosphatidylcholine, triglycerides, phosphatidylethanolamine and lysophosphatidylcholine were significantly enriched in glycerophospholipid metabolism, triglyceride metabolism, and polyunsaturated fatty acid-related metabolic pathways in response to heat stress in C. goreaui and D. trenchii. Notably, the two species exhibited significant differences in sphingolipid metabolism: D. trenchii downregulated ceramide levels to reduce oxidative stress damage, regulate autophagy, and adapt to changes in membrane fluidity, whereas C. goreaui primarily upregulated lipid molecules rich in polyunsaturated fatty acids to maintain membrane stability and regulate signal transduction. A deeper understanding of the lipid metabolic stress response mechanisms of Symbiodiniaceae with different environmental sensitivities under heat stress provides new insights into enhancing coral adaptability to environmental changes from a symbiotic partner perspective.
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Key words:
- heat stress /
- symbiodiniaceae /
- sphingolipid metabolism /
- lipidomics /
- oxidative stress
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图 1 热胁迫下两种虫黄藻的生理指标变化。（A）CC组、CT组、DC组和DT组的生长密度。（B）CC组、CT组、DC组和DT组的生长速率（μ）。（C）CC组、CT组、DC组和DT组的叶绿素a含量变化。（D）CC组、CT组、DC组和DT组的类胡萝卜素含量变化。（E）CC组、CT组、DC组和DT组的叶绿素c含量变化。（F）CC组、CT组、DC组和DT组的Fv/Fm值变化。误差棒表示SEM（3个生物学重复）。实验组和对照组之间的显著性用星号表示（*：P < 0.05；**：P < 0.01；***：P < 0.001）
Fig. 1 Physiological parameter changes of two Symbiodiniaceae species under heat stress. (A) Growth density of CC, CT, DC, and DT groups. (B) Growth rate (μ) of CC, CT, DC, and DT groups. (C) Changes in Chlorophyll a content in CC, CT, DC, and DT groups. (D) Changes in carotenoid content in CC, CT, DC, and DT groups. (E) Changes in Chlorophyll c content in CC, CT, DC, and DT groups. (F) Changes in Fv/Fm values in CC, CT, DC, and DT groups. Error bars represent SEM (n = 3 biological replicates). Statistical significance between experimental and control groups is indicated by asterisks (*: P < 0.05; **: P < 0.01; ***: P < 0.001)
图 2 热胁迫下两种虫黄藻抗氧化物活性（含量）变化。（A）CC组、CT组、DC组和DT组的可溶性蛋白浓度的变化。（B）CC组、CT组、DC组和DT组的SOD活力的变化。（C）CC组、CT组、DC组和DT组的MDA含量的变化。误差棒表示SEM（3个生物学重复）。实验组和对照组之间的显著性用星号表示（*：P < 0.05；**：P < 0.01；***：P < 0.001）
Fig. 2 Changes in antioxidant activity (content) of two Symbiodiniaceae species under heat stress. (A) Changes in soluble protein concentration in CC, CT, DC, and DT groups. (B) Changes in SOD activity in CC, CT, DC, and DT groups. (C) Changes in MDA content in CC, CT, DC, and DT groups. Error bars represent SEM (n = 3 biological replicates). Statistical significance between experimental and control groups is indicated by asterisks (*: P < 0.05; **: P < 0.01; ***: P < 0.001)
图 3 热胁迫下两种虫黄藻脂质变化注释图。（A）虫黄藻全脂质分类统计图；（B）虫黄藻脂质链不饱和度分类统计图；（C）CC组、CT组、DC组和DT组的脂质分类统计图。误差棒表示SEM（6个生物学重复）
Fig. 3 Annotated diagram of lipid changes in two types of Symbiodiniaceae species under heat stress. (A) Total lipid classification chart for Symbiodiniaceae. (B) Lipid chain unsaturation classification chart for Symbiodiniaceae. (C) Lipid classification chart for the CC, CT, DC, and DT groups. Error bars represent SEM (n = 6 biological replicates)
图 4 热胁迫下两种虫黄藻的PCA得分图和OPLS-DA得分图。（A）、（B）正、负离子模式CC组、CT组、DC组、DT组的PCA得分图；（C）、（D）正、负离子模式下CC组、CT组的OPLS-DA得分图；（E）、（F）正、负离子模式下DC组、DT组的OPLS-DA得分图。
Fig. 4 PCA score plot and OPLS-DA score plot of two types of Symbiodiniaceae species under heat stress. (A), (B) PCA score plots for the CC, CT, DC, and DT groups in positive and negative ion modes. (C), (D) OPLS-DA score plots for the CC and CT groups in positive and negative ion modes. (E), (F) OPLS-DA score plots for the DC and DT groups in positive and negative ion modes.
图 5 热胁迫下两种虫黄藻的显著差异代谢物火山图。（A）CC vs CT显著差异代谢物火山图；（B）DC vs DT显著差异代谢物火山图；（C）CC vs DC显著差异代谢物火山图；（D）CT vs DT显著差异代谢物火山图。以P值取前10的代谢物进行标记，P值越小越显著
Fig. 5 Volcano plot of significant different metabolites in two Symbiodiniaceae species under heat stress. (A) Volcano plot of significant different metabolites in CC vs. CT. (B) Volcano plot of significant different metabolites in DC vs. DT. (C) Volcano plot of significant different metabolites in CC vs. DC. (D) Volcano plot of significant different metabolites in CT vs. DT, with the top 10 metabolites marked by smallest P-values, indicating greater significance
图 6 热胁迫下两种虫黄藻的单因素方差分析柱状图。图中纵坐标轴表示代谢物名称，横坐标表示表示代谢物在不同分组中平均相对丰度，不同颜色的柱子表示不同分组；误差棒表示SEM（6个生物学重复）。星号为显著性为P值（*：0.01 < P l0.05，**：0.001 < P 0.01，***：P 0.001）
Fig. 6 One-way ANOVA histogram of two Symbiodiniaceae species under heat stress The y-axis of the chart represents metabolite names, while the x-axis represents the average relative abundance of metabolites in different groups. Bars of different colors correspond to different groups. Error bars represent SEM (n = 6 biological replicates). Asterisks indicate significance levels of P-values (*: 0.01 < P 0.05, **: 0.001 < P 0.01, ***: P 0.001)
图 7 热胁迫下两种虫黄藻差异代谢物的KEGG富集气泡图。（A）CC vs CT的差异代谢物的KEGG富集分析通路图；（B）DC vs DT的差异代谢物的KEGG富集分析通路图；（C）CC vs DC的差异代谢物的KEGG富集分析通路图；（D）CT vs DT的差异代谢物的KEGG富集分析通路图。横坐标为富集显著性P值，P值越小，在统计学上就越有显著意义，一般P < 0.05认为该功能为显著富集项；纵坐标为KEGG通路。图中气泡的颜色代表该通路富集显著性，气泡的大小代表该通路中富集到代谢集中代谢物的数量
Fig. 7 KEGG enrichment bubble plot of different metabolites in two Symbiodiniaceae species under heat stress. (A) KEGG pathway enrichment analysis of different metabolites of CC vs. CT. (B) KEGG pathway enrichment analysis of different metabolites of DC vs. DT. (C) KEGG pathway enrichment analysis of different metabolites of CC vs DC. (D) KEGG pathway enrichment analysis of different metabolites of CT vs DT. The x-axis represents the enrichment significance P-value, where smaller P-values indicate higher statistical significance. Generally, pathways with P < 0.05 are considered significantly enriched. The y-axis represents KEGG pathways. In the chart, the color of the bubbles indicates the enrichment significance of the pathway, while the size of the bubbles represents the number of metabolites enriched in the corresponding pathway
表 1 OPLS-DA模型
Tab. 1 OPLS-DA modles
模型 R2X(cum) R2Y(cum) Q2(cum) CC vs CT 0.641 0.992 0.987 CC vs CT * 0.629 0.993 0.988 DC vs DT 0.560 0.998 0.990 DC vs DT * 0.593 0.997 0.991 注：*代表负离子模式。 
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