Quantitative Lipidomics and Spatial MS-Imaging Uncovered Neurological and Systemic Lipid Metabolic Pathways Underlying Troglomorphic Adaptations in Cave-Dwelling Fish.

Quantitative Lipidomics and Spatial MS-Imaging Uncovered Neurological and Systemic Lipid Metabolic Pathways Underlying Troglomorphic Adaptations in Cave-Dwelling Fish.
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定量脂质组学和空间 MS 成像揭示了洞穴鱼类类形适应背后的神经和系统脂质代谢途径

DOI:
10.1093/molbev/msac050
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发表时间:
2022-04-10
影响因子:
10.7
通讯作者:
Shui, Guanghou
Shui, Guanghou
中科院分区:
生物学1区
文献类型:
--
作者:
Lam, Sin Man;Li, Jie;Sun, Huan;Mao, Weining;Lu, Zongmin;Zhao, Qingshuo;Han, Chao;Gong, Xia;Jiang, Binhua;Chua, Gek Huey;Zhao, Zhenwen;Meng, Fanwei;Shui, Guanghou

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摘要 中华金线鱼是中国特有的稀有淡水硬骨鱼属,包括河流表层鱼类和洞穴鱼类。使用定量脂质组学和质谱成像(MSI)的组合方法,我们证明脂质分布和脂质代谢的神经区室化与中华金线鲃的穴居性状的进化相关。通过 Δ4 去饱和酶途径减弱的二十二碳六烯酸 (DHA) 生物合成导致洞穴鱼小脑中 DHA 磷脂的减少。相反,洞穴鱼会积累花生四烯酸磷脂,这可能不利于视网膜顶盖乔木的生长。重要的是,硫苷脂的 MSI 结合髓磷脂碱性蛋白的免疫染色和后脑轴突的透射电子显微镜图像揭示了穴居鱼中缝血清素能神经元的脱髓鞘。洞穴鱼的脱髓鞘与控制社会行为(例如攻击性优势)的神经可塑性的丧失同时发生。在大脑之外,定量脂质组学和 qRT-PCR 显示肝脏中膜酯化 DHA 的系统性减少,这归因于 Sprecher 途径基因(elovl2、elovl5 和 acox1)的抑制。在洞穴鱼中观察到脂肪肝的发展;可能是由储存脂质动员受阻介导的,pnpla2、lipea、lipeb、dagla 和 mgll 表达减少很明显;并通过线粒体和过氧化物酶体抑制脂肪酰基的 β-氧化,这反映在 cpt1ab、hadhaa、cpt2、decr1 和 acox1 的表达减少上。这些神经和系统代谢适应有助于减少能量消耗,形成隐性进化的基础,消除非必要的形态和行为特征,并赋予洞穴鱼在洞穴中繁衍生息的选择性优势,在洞穴中,适当的资源分配成为生存的主要决定因素。
Abstract Sinocyclocheilus represents a rare, freshwater teleost genus endemic to China that comprises the river-dwelling surface fish and the cave-dwelling cavefish. Using a combinatorial approach of quantitative lipidomics and mass-spectrometry imaging (MSI), we demonstrated that neural compartmentalization of lipid distribution and lipid metabolism is associated with the evolution of troglomorphic traits in Sinocyclocheilus. Attenuated docosahexaenoic acid (DHA) biosynthesis via the Δ4 desaturase pathway led to reductions in DHA-phospholipids in cavefish cerebellum. Instead, cavefish accumulates arachidonic acid-phospholipids that may disfavor retinotectal arbor growth. Importantly, MSI of sulfatides coupled with immunostaining of myelin basic protein and transmission electron microscopy images of hindbrain axons revealed demyelination in cavefish raphe serotonergic neurons. Demyelination in cavefish parallels the loss of neuroplasticity governing social behavior such as aggressive dominance. Outside the brain, quantitative lipidomics and qRT-PCR revealed systemic reductions in membrane esterified DHAs in the liver, attributed to suppression of genes along the Sprecher pathway (elovl2, elovl5, and acox1). Development of fatty livers was observed in cavefish; likely mediated by an impeded mobilization of storage lipids, as evident in the diminished expressions of pnpla2, lipea, lipeb, dagla, and mgll; and suppressed β-oxidation of fatty acyls via both mitochondria and peroxisomes as reflected in the reduced expressions of cpt1ab, hadhaa, cpt2, decr1, and acox1. These neurological and systemic metabolic adaptations serve to reduce energy expenditure, forming the basis of recessive evolution that eliminates nonessential morphological and behavioral traits and giving cavefish a selective advantage to thrive in caves where proper resource allocation becomes a major determinant of survival.
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