Department of Biology, Colorado State University, Fort Collins, CO 80523-1878.
Key Laboratory of Growth Regulation and Translational Research of Zhejiang Province, School of Life Sciences, Westlake University, Hangzhou 310024, China.
Proc Natl Acad Sci U S A. 2022 Sep 20;119(38):e2203708119. doi: 10.1073/pnas.2203708119. Epub 2022 Sep 12.
Fucoxanthin is a major light-harvesting pigment in ecologically important algae such as diatoms, haptophytes, and brown algae (Phaeophyceae). Therefore, it is a major driver of global primary productivity. Species of these algal groups are brown colored because the high amounts of fucoxanthin bound to the proteins of their photosynthetic machineries enable efficient absorption of green light. While the structure of these fucoxanthin-chlorophyll proteins has recently been resolved, the biosynthetic pathway of fucoxanthin is still unknown. Here, we identified two enzymes central to this pathway by generating corresponding knockout mutants of the diatom that are green due to the lack of fucoxanthin. Complementation of the mutants with the native genes or orthologs from haptophytes restored fucoxanthin biosynthesis. We propose a complete biosynthetic path to fucoxanthin in diatoms and haptophytes based on the carotenoid intermediates identified in the mutants and in vitro biochemical assays. It is substantially more complex than anticipated and reveals diadinoxanthin metabolism as the central regulatory hub connecting the photoprotective xanthophyll cycle and the formation of fucoxanthin. Moreover, our data show that the pathway evolved by repeated duplication and neofunctionalization of genes for the xanthophyll cycle enzymes violaxanthin de-epoxidase and zeaxanthin epoxidase. Brown algae lack diadinoxanthin and the genes described here and instead use an alternative pathway predicted to involve fewer enzymes. Our work represents a major step forward in elucidating the biosynthesis of fucoxanthin and understanding the evolution, biogenesis, and regulation of the photosynthetic machinery in algae.
岩藻黄素是硅藻、甲藻和褐藻（褐藻门）等重要藻类中的主要捕光色素。因此，它是全球初级生产力的主要驱动因素。这些藻类群的物种呈棕色，因为大量与光合作用机器中的蛋白质结合的岩藻黄素能够有效地吸收绿光。虽然这些岩藻黄素-叶绿素蛋白的结构最近已经得到解决，但岩藻黄素的生物合成途径仍然未知。在这里，我们通过生成由于缺乏岩藻黄素而呈绿色的硅藻的相应敲除突变体，鉴定了该途径中的两个关键酶。用来自甲藻的天然基因或同源基因对突变体进行互补，恢复了岩藻黄素的生物合成。基于在突变体和体外生化测定中鉴定的类胡萝卜素中间产物，我们提出了硅藻和甲藻中岩藻黄素的完整生物合成途径。它比预期的要复杂得多，揭示了二氢玉米黄质代谢作为连接光保护叶黄素循环和岩藻黄素形成的中心调节枢纽。此外，我们的数据表明，该途径是通过重复复制和新功能化叶黄素循环酶的基因（紫黄质脱环氧化酶和玉米黄质环氧化酶）进化而来的。褐藻缺乏二氢玉米黄质和这里描述的基因，而是使用一种预测涉及较少酶的替代途径。我们的工作代表着在阐明岩藻黄素生物合成以及理解藻类光合作用机器的进化、生物发生和调节方面迈出了重要的一步。
