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基于广泛靶向代谢组学和转录组学的高硫化物条件下密叶拟马鞭藻的代谢网络响应和耐受机制。

The metabolic network response and tolerance mechanism of Thalassia hemprichii under high sulfide based on widely targeted metabolome and transcriptome.

机构信息

Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China; University of Chinese Academy of Sciences, Beijing 100049, China.

Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China; University of Chinese Academy of Sciences, Beijing 100049, China; Sanya Institute of Ocean Eco-Environmental Engineering, Sanya 572100, China.

出版信息

Sci Total Environ. 2024 Nov 15;951:175702. doi: 10.1016/j.scitotenv.2024.175702. Epub 2024 Aug 22.

DOI:10.1016/j.scitotenv.2024.175702
PMID:39179040
Abstract

Costal eutrophication leads to increased sulfide levels in sediments, which has been identified as a major cause of the global decline in seagrass beds. The seagrass Thalassia hemprichii, a dominant tropical species in the Indo-Pacific, is facing a potential threat from sulfide, which can be easily reduced from sulfate in porewater under the influence of global climate change and eutrophication. However, its metabolic response and tolerance mechanisms to high sulfide remain unclear. Thus, the current study investigated the physiological responses and programmed metabolic networks of T. hemprichii through a three-week mesocosm experiment, integrating physiology, stable isotope, widely targeted metabolomics, transcriptomics, and microbial diversity assessments. High sulfide reduced the sediment microbial diversity, while increased sediment sulfate reduced bacterial abundance and δS. The exposure to sulfide enhanced root δS while decreased leaf δS in T. hemprichii. High sulfide was shown to inhibit photosynthesis via damaging PSII, which further reduced ATP production. In response, abundant up-regulated differentially expressed genes in energy metabolism, especially in oxidative phosphorylation, were activated to compensate high energy requirement. High sulfide also promoted autophagy by overexpressing the genes related to phagocytosis and phagolysosome. Meanwhile, metabolomic profiling revealed that the contents of many primary metabolites, such as carbohydrates and amino acids, were reduced in both leaves and roots, likely to provide more energy and synthesize stress-responsive secondary metabolites. Genes related to nitrate reduction and transportation were up-regulated to promote N uptake for sulfide detoxification. High sulfide levels specifically enhanced thiamine in roots, while increased jasmonic acid and flavonoid levels in leaves. The distinct differences in metabolism between roots and leaves might be related to sulfide levels and the growth-defense trade-off. Collectively, our work highlights the specific mechanisms underlying the response and tolerance of T. hemprichii to high sulfide, providing new insights into seagrass strategies for resisting sulfide.

摘要

滨海富营养化导致沉积物中硫化物水平升高,这已被确定为全球海草床减少的主要原因。海草 Thalassia hemprichii 是印度洋-太平洋热带地区的优势物种,正面临着来自硫化物的潜在威胁,硫化物在全球气候变化和富营养化的影响下,很容易从孔隙水中的硫酸盐还原而来。然而,其对高硫化物的代谢响应和耐受机制尚不清楚。因此,本研究通过为期三周的中观实验,整合生理学、稳定同位素、广泛靶向代谢组学、转录组学和微生物多样性评估,研究了 T. hemprichii 的生理响应和程序化代谢网络。高硫化物降低了沉积物微生物多样性,而增加的沉积物硫酸盐降低了细菌丰度和 δS。暴露于硫化物会增强 T. hemprichii 的根 δS,同时降低其叶 δS。高硫化物通过破坏 PSII 来抑制光合作用,从而进一步降低 ATP 产生。作为响应,能量代谢中大量上调的差异表达基因被激活,以补偿高能量需求,特别是在氧化磷酸化中。高硫化物还通过过度表达与吞噬和吞噬体相关的基因来促进自噬。同时,代谢组学分析表明,许多初级代谢物(如碳水化合物和氨基酸)的含量在叶片和根中均降低,这可能为提供更多能量和合成应激响应的次生代谢物。与硝酸盐还原和运输相关的基因被上调,以促进 N 吸收用于硫化物解毒。高硫化物水平特异性地增加了根中的硫胺素,而增加了叶中的茉莉酸和类黄酮水平。根和叶之间代谢的明显差异可能与硫化物水平和生长-防御权衡有关。总之,我们的工作强调了 T. hemprichii 对高硫化物的响应和耐受的特定机制,为海草抵抗硫化物提供了新的见解。

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