Massive Protein Import into the Early-Evolutionary-Stage Photosynthetic Organelle of the Amoeba Paulinella chromatophora

Massive Protein Import into the Early-Evolutionary-Stage Photosynthetic Organelle of the Amoeba Paulinella chromatophora
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DOI:
10.1016/j.cub.2017.08.010
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发表时间:
2017-09-25
期刊:
影响因子:
9.2
通讯作者:
Nowack, Eva C. M.
Nowack, Eva C. M.
中科院分区:
生物学1区
文献类型:
--
作者:
Singer, Anna;Poschmann, Gereon;Nowack, Eva C. M.

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超过 1 Ga 之前,内共生获得线粒体和质体对真核生物的进化产生了深远的影响。了解细胞器进化的核心是将内共生蛋白质组重新排列成宿主控制的细胞器蛋白质组。然而,这一过程的早期阶段以及细胞器整合背后的事件发生时间仍然知之甚少。阿米巴 Paulinella chromatophora 含有蓝藻衍生的光合细胞器,称为“色素细胞”,是最近(大约 100 Ma 前)获得的。为了探索细胞器蛋白质组在整合到真核宿主细胞过程中的重新排列,在这里我们通过蛋白质质谱法表征了色素细胞蛋白质组。显然,对色素细胞的遗传控制 已显着转移至细胞核。两类核编码的蛋白质(蛋白质长度不同)很可能通过独立的途径被输入到色素细胞中。长输入蛋白携带假定的、保守的 N 末端靶向信号,并且许多特异性地填补了色素细胞编码的代谢途径或过程中的空白。令人惊讶的是,在植物细胞中异源表达后,假定的色素细胞靶向 信号赋予叶绿体定位。这一发现表明,色素细胞和质体这两种独立进化的细胞器的蛋白质输入途径存在共同特征,并且彼此相距超过 1 Ga。通过将实验数据与计算机预测相结合,我们提供了近 450 种核编码、色素细胞靶向蛋白质的综合目录。有趣的是,大多数进口蛋白质似乎都来自祖先 宿主基因,表明内共生基因转移引起的核编码蛋白的重新定位在色素细胞整合开始时仅发挥次要作用。
The endosymbiotic acquisition of mitochondria and plastids more than 1 Ga ago profoundly impacted eukaryote evolution. At the heart of understanding organelle evolution is the re-arrangement of the endosymbiont proteome into a host-controlled organellar proteome. However, early stages in this process as well as the timing of events that underlie organelle integration remain poorly understood. The amoeba Paulinella chromatophora contains cyanobacterium-derived photosynthetic organelles, termed "chromatophores,'' that were acquired more recently (around 100 Ma ago). To explore the re-arrangement of an organellar proteome during its integration into a eukaryotic host cell, here we characterized the chromatophore proteome by protein mass spectrometry. Apparently, genetic control over the chromatophore has shifted substantially to the nucleus. Two classes of nuclear-encoded proteins-which differ in protein length-are imported into the chromatophore, most likely through independent pathways. Long imported proteins carry a putative, conserved N-terminal targeting signal, and many specifically fill gaps in chromatophore-encoded metabolic pathways or processes. Surprisingly, upon heterologous expression in a plant cell, the putative chromatophore targeting signal conferred chloroplast localization. This finding suggests common features in the protein import pathways of chromatophores and plastids, two organelles that evolved independently and more than 1 Ga apart from each other. By combining experimental data with in silico predictions, we provide a comprehensive catalog of almost 450 nuclear-en-coded, chromatophore-targeted proteins. Interestingly, most imported proteins seem to derive from ancestral host genes, suggesting that the re-targeting of nuclear-encoded proteins that resulted from endosymbiotic gene transfers plays only a minor role at the onset of chromatophore integration.