Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE, 68588, USA.
School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE, 68588, USA.
Nat Commun. 2024 Feb 20;15(1):1548. doi: 10.1038/s41467-024-45813-y.
Mitochondrial cytochrome c maturation (CCM) requires heme attachment via distinct pathways termed systems I and III. The mosaic distribution of these systems in Archaeplastida raises questions about the genetic mechanisms and evolutionary forces promoting repeated evolution. Here, we show a recurrent shift from ancestral system I to the eukaryotic-specific holocytochrome c synthase (HCCS) of system III in 11 archaeplastid lineages. Archaeplastid HCCS is sufficient to rescue mutants of yeast system III and Arabidopsis system I. Algal HCCS mutants exhibit impaired growth and respiration, and altered biochemical and metabolic profiles, likely resulting from deficient CCM and reduced cytochrome c-dependent respiratory activity. Our findings demonstrate that archaeplastid HCCS homologs function as system III components in the absence of system I. These results elucidate the evolutionary trajectory and functional divergence of CCM pathways in Archaeplastida, providing insight into the causes, mechanisms, and consequences of repeated cooption of an entire biological pathway.
线粒体细胞色素 c 成熟（CCM）需要通过不同的途径（称为系统 I 和 III）附着血红素。这些系统在古生菌中的镶嵌分布引发了关于促进重复进化的遗传机制和进化力量的问题。在这里，我们在 11 个古生菌谱系中显示了从祖先系统 I 到真核生物特有的全细胞色素 c 合酶（HCCS）的系统 III 的反复转变。古生菌 HCCS 足以拯救酵母系统 III 和拟南芥系统 I 的突变体。藻类 HCCS 突变体表现出生长和呼吸受损，以及改变的生化和代谢特征，可能是由于 CCM 缺陷和减少的细胞色素 c 依赖性呼吸活性所致。我们的研究结果表明，古生菌 HCCS 同源物在没有系统 I 的情况下作为系统 III 的组成部分发挥作用。这些结果阐明了古生菌中 CCM 途径的进化轨迹和功能分化，为重复采用整个生物途径的原因、机制和后果提供了深入了解。
