Nectar-feeding bats and birds show parallel molecular adaptations in sugar metabolism enzymes

Nectar-feeding bats and birds show parallel molecular adaptations in sugar metabolism enzymes
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DOI:
10.1016/j.cub.2021.08.018
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发表时间:
2021-10-25
期刊:
影响因子:
9.2
通讯作者:
Rossiter, Stephen J.
Rossiter, Stephen J.
中科院分区:
生物学1区
文献类型:
--
作者:
Potter, Joshua H. T.;Drinkwater, Rosie;Rossiter, Stephen J.

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在大多数脊椎动物中,对作为细胞呼吸主要底物的葡萄糖的需求是通过复杂碳水化合物的分解来满足的,或者通过蛋白质和脂质分解代谢来获得能量。相比之下,一些蝙蝠和鸟类已经趋同进化为以花蜜为生,花蜜是一种富含葡萄糖、果糖和蔗糖的混合物。1-4 这些花蜜喂养者如何适应应对终生高糖摄入,同时避免代谢综合征和糖尿病的发作5-7尚不清楚。我们分析了从 127 个类群获得的基因序列,其中包括 22 个食蜜蝙蝠和鸟类属,它们共同包含四个独立的食蜜起源。我们表明,这些不同的类群在糖分解代谢途径中经历了普遍的分子适应,包括关键糖酵解和果糖分解酶的平行选择。我们还发现了进化上保守的醛缩酶 B (ALDOB) 和线粒体看门人丙酮酸脱氢酶 (PDH) 中的收敛氨基酸取代,其中醛缩酶 B 催化果糖分解和糖酵解的限速步骤,而线粒体把关者丙酮酸脱氢酶 (PDH) 连接糖酵解和三羧酸循环。代谢组学特征和酶功能测定与吸食花蜜的蝙蝠呼吸通量的增加一致,并有助于解释这些类群如何维持悬停飞行并有效清除单糖。总而言之,我们的结果表明,以花蜜为食的蝙蝠和鸟类已经经历了代谢适应,使它们能够利用脊椎动物中独特的富含能量的饮食生态位。
In most vertebrates, the demand for glucose as the primary substrate for cellular respiration is met by the breakdown of complex carbohydrates, or energy is obtained by protein and lipid catabolism. In contrast, a few bat and bird species have convergently evolved to subsist on nectar, a sugar-rich mixture of glucose, fructose, and sucrose.1-4 How these nectar-feeders have adapted to cope with life-long high sugar intake while avoiding the onset of metabolic syndrome and diabetes5-7 is not understood. We analyzed gene sequences obtained from 127 taxa, including 22 nectar-feeding bat and bird genera that collectively encompass four independent origins of nectarivory. We show these divergent taxa have undergone pervasive molecular adaptation in sugar catabolism pathways, including parallel selection in key glycolytic and fructolytic enzymes. We also uncover convergent amino acid substitutions in the otherwise evolutionarily conserved aldolase B (ALDOB), which catalyzes rate-limiting steps in fructolysis and glycolysis, and the mitochondrial gatekeeper pyruvate dehydrogenase (PDH), which links glycolysis and the tricarboxylic acid cycle. Metabolomic profile and enzyme functional assays are consistent with increased respiratory flux in nectar-feeding bats and help explain how these taxa can both sustain hovering flight and efficiently clear simple sugars. Taken together, our results indicate that nectar-feeding bats and birds have undergone metabolic adaptations that have enabled them to exploit a unique energy-rich dietary niche among vertebrates.