A non-photosynthetic green alga illuminates the reductive evolution of plastid electron transport systems
A non-photosynthetic green alga illuminates the reductive evolution of plastid electron transport systems
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DOI：
10.1186/s12915-020-00853-w
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发表时间：
2020-09-16
期刊：
影响因子：
5.4
通讯作者：
Kamikawa, Ryoma
中科院分区：
文献类型：
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作者：
Kayama, Motoki;Chen, Jun-Feng;Kamikawa, Ryoma
背景质体电子传输系统不仅对于光合作用至关重要，而且对于耗散过量的还原能力和吸收各种氧化还原反应产生的过量电子也至关重要。尽管许多具有质体的生物体已经失去了光合自养的生活方式，但在非光合作用的藻类/植物谱系中，残余质体仍然具有一系列已知的功能；一些非光合质体仍然保留涉及氧化还原反应的多种代谢途径，而其他质体，例如顶复门寄生虫的顶质体，具有高度减少的功能集。然而，人们对功能多样的非光合质体中氧化还原稳态的基本机制以及质体电子传输系统的还原进化知之甚少。结果在这里，我们证明质体电子传递系统的核心成分质体醌/质体醌醇库仍然保留在缺乏光合作用相关类囊体膜复合物的专性异养绿藻的新菌株中。显微镜和基因组分析表明，Volocales 绿藻、chlamydomonad sp。菌株NrCl902，具有非光合质体和不携带光合电子传递系统基因的质体DNA。基于转录组的代谢图预测以及液相色谱分析证明了类胡萝卜素和质体醌的合成，但在非光合作用绿藻中没有叶绿素色素的痕迹。瞬时 RNA 干扰敲除会导致质体醌/质体醌醇合成受到抑制。该藻类似乎拥有由质体末端氧化酶、质体醌/质体醌醇和 II 型 NADH 脱氢酶介导的电子接收系统基因。其他非光合藻类/陆地植物也拥有该系统的关键基因，表明电子汇系统在非光合质体中广泛分布。结论 质体醌/质体醌醇库以及本文报道的所涉及的电子传递系统可能被保留用于氧化还原稳态，并且可能代表在许多非光合质体中朝着更简化的电子传递系统组迈出的中间步骤。我们的发现阐明了光合作用丧失后质体电子传输系统的还原进化的广泛分布但以前隐藏的步骤。
Background Plastid electron transport systems are essential not only for photosynthesis but also for dissipating excess reducing power and sinking excess electrons generated by various redox reactions. Although numerous organisms with plastids have lost their photoautotrophic lifestyles, there is a spectrum of known functions of remnant plastids in non-photosynthetic algal/plant lineages; some of non-photosynthetic plastids still retain diverse metabolic pathways involving redox reactions while others, such as apicoplasts of apicomplexan parasites, possess highly reduced sets of functions. However, little is known about underlying mechanisms for redox homeostasis in functionally versatile non-photosynthetic plastids and thus about the reductive evolution of plastid electron transport systems. Results Here we demonstrated that the central component for plastid electron transport systems, plastoquinone/plastoquinol pool, is still retained in a novel strain of an obligate heterotrophic green alga lacking the photosynthesis-related thylakoid membrane complexes. Microscopic and genome analyses revealed that the Volvocales green alga, chlamydomonad sp. strain NrCl902, has non-photosynthetic plastids and a plastid DNA that carries no genes for the photosynthetic electron transport system. Transcriptome-based in silico prediction of the metabolic map followed by liquid chromatography analyses demonstrated carotenoid and plastoquinol synthesis, but no trace of chlorophyll pigments in the non-photosynthetic green alga. Transient RNA interference knockdown leads to suppression of plastoquinone/plastoquinol synthesis. The alga appears to possess genes for an electron sink system mediated by plastid terminal oxidase, plastoquinone/plastoquinol, and type II NADH dehydrogenase. Other non-photosynthetic algae/land plants also possess key genes for this system, suggesting a broad distribution of an electron sink system in non-photosynthetic plastids. Conclusion The plastoquinone/plastoquinol pool and thus the involved electron transport systems reported herein might be retained for redox homeostasis and might represent an intermediate step towards a more reduced set of the electron transport system in many non-photosynthetic plastids. Our findings illuminate a broadly distributed but previously hidden step of reductive evolution of plastid electron transport systems after the loss of photosynthesis.