Recurrent evolutionary switches of mitochondrial cytochrome c maturation systems in Archaeplastida

Huang Li, Soujanya Akella, Carina Engstler, Joy J. Omini, Moira Rodriguez, Toshihiro Obata, Chris Carrie, Heriberto Cerutti and Jeffrey P. Mower ()
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Huang Li: Center for Plant Science Innovation, University of Nebraska-Lincoln
Soujanya Akella: Center for Plant Science Innovation, University of Nebraska-Lincoln
Carina Engstler: Ludwig-Maximilians-Universität München
Joy J. Omini: University of Nebraska-Lincoln
Moira Rodriguez: University of Nebraska-Lincoln
Toshihiro Obata: Center for Plant Science Innovation, University of Nebraska-Lincoln
Chris Carrie: University of Auckland
Heriberto Cerutti: Center for Plant Science Innovation, University of Nebraska-Lincoln
Jeffrey P. Mower: Center for Plant Science Innovation, University of Nebraska-Lincoln

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: Abstract 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.

Date: 2024
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DOI: 10.1038/s41467-024-45813-y

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