Tsaousis Anastasios D, Kunji Edmund R S, Goldberg Alina V, Lucocq John M, Hirt Robert P, Embley T Martin
Institute for Cell and Molecular Biosciences, Catherine Cookson Building, Framlington Place, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.
Nature. 2008 May 22;453(7194):553-6. doi: 10.1038/nature06903. Epub 2008 Apr 30.
Mitochondria use transport proteins of the eukaryotic mitochondrial carrier family (MCF) to mediate the exchange of diverse substrates, including ATP, with the host cell cytosol. According to classical endosymbiosis theory, insertion of a host-nuclear-encoded MCF transporter into the protomitochondrion was the key step that allowed the host cell to harvest ATP from the enslaved endosymbiont. Notably the genome of the microsporidian Encephalitozoon cuniculi has lost all of its genes for MCF proteins. This raises the question of how the recently discovered microsporidian remnant mitochondrion, called a mitosome, acquires ATP to support protein import and other predicted ATP-dependent activities. The E. cuniculi genome does contain four genes for an unrelated type of nucleotide transporter used by plastids and bacterial intracellular parasites, such as Rickettsia and Chlamydia, to import ATP from the cytosol of their eukaryotic host cells. The inference is that E. cuniculi also uses these proteins to steal ATP from its eukaryotic host to sustain its lifestyle as an obligate intracellular parasite. Here we show that, consistent with this hypothesis, all four E. cuniculi transporters can transport ATP, and three of them are expressed on the surface of the parasite when it is living inside host cells. The fourth transporter co-locates with mitochondrial Hsp70 to the E. cuniculi mitosome. Thus, uniquely among eukaryotes, the traditional relationship between mitochondrion and host has been subverted in E. cuniculi, by reductive evolution and analogous gene replacement. Instead of the mitosome providing the parasite cytosol with ATP, the parasite cytosol now seems to provide ATP for the organelle.
线粒体利用真核生物线粒体载体家族（MCF）的转运蛋白来介导包括ATP在内的多种底物与宿主细胞胞质溶胶的交换。根据经典的内共生理论，将宿主细胞核编码的MCF转运蛋白插入原线粒体是宿主细胞从被奴役的内共生体获取ATP的关键步骤。值得注意的是，微小孢子虫兔脑炎微孢子虫的基因组已经失去了所有与MCF蛋白相关的基因。这就提出了一个问题，即最近发现的被称为“线粒体小体”的微小孢子虫残余线粒体是如何获取ATP来支持蛋白质导入和其他预测的ATP依赖活动的。兔脑炎微孢子虫的基因组确实包含四个与一种不相关的核苷酸转运蛋白有关的基因，质体和细菌细胞内寄生虫（如立克次氏体和衣原体）利用这种转运蛋白从其真核宿主细胞的胞质溶胶中导入ATP。由此推断，兔脑炎微孢子虫也利用这些蛋白质从其真核宿主那里窃取ATP，以维持其作为专性细胞内寄生虫的生活方式。在这里我们表明，与这一假设一致，兔脑炎微孢子虫的所有四种转运蛋白都能转运ATP，并且其中三种在寄生虫生活在宿主细胞内时会在其表面表达。第四种转运蛋白与线粒体热休克蛋白70共同定位于兔脑炎微孢子虫的线粒体小体。因此，在真核生物中独一无二的是，在兔脑炎微孢子虫中，线粒体与宿主之间的传统关系通过简化进化和类似的基因替代而被颠覆。不是线粒体小体为寄生虫胞质溶胶提供ATP，现在似乎是寄生虫胞质溶胶为这个细胞器提供ATP。
