The Origin of Mitochondrial Cristae from Alphaproteobacteria

• Published in: Molecular biology and evolution Vol. 34; no. 4; pp. 943 - 956
• Main Authors: Muñoz-Gómez, Sergio A, Wideman, Jeremy G, Roger, Andrew J, Slamovits, Claudio H
• Format: Journal Article
• Language: English
• Published: United States 01.04.2017
• Subjects: Alphaproteobacteria - genetics; Alphaproteobacteria - metabolism; Biological Evolution; Evolution, Molecular; Membrane Proteins - genetics; Mitochondria - genetics; Mitochondria - metabolism; Mitochondria - ultrastructure; Mitochondrial Membranes - metabolism; Mitochondrial Proteins - genetics; Phylogeny; Protein Binding; Symbiosis - genetics; purple bacteria; magnetosomes; ICMs; MICOS; endosymbiosis; Mic60
• ISSN: 0737-4038; 1537-1719
• DOI: 10.1093/molbev/msw298

Mitochondria are the respiratory organelles of eukaryotes and their evolutionary history is deeply intertwined with that of eukaryotes. The compartmentalization of respiration in mitochondria occurs within cristae, whose evolutionary origin has remained unclear. Recent discoveries, however, have revived the old notion that mitochondrial cristae could have had a pre-endosymbiotic origin. Mitochondrial cristae are likely homologous to the intracytoplasmic membranes (ICMs) used by diverse alphaproteobacteria for harnessing energy. Because the Mitochondrial Contact site and Cristae Organizing System (MICOS) that controls the development of cristae evolved from a simplified version that is phylogenetically restricted to Alphaproteobacteria (alphaMICOS), ICMs most probably transformed into cristae during the endosymbiotic origin of mitochondria. This inference is supported by the sequence and structural similarities between MICOS and alphaMICOS, and the expression pattern and cellular localization of alphaMICOS. Given that cristae and ICMs develop similarly, alphaMICOS likely functions analogously to mitochondrial MICOS by culminating ICM development with the creation of tubular connections and membrane contact sites at the alphaproteobacterial envelope. Mitochondria thus inherited a pre-existing ultrastructure adapted to efficient energy transduction from their alphaproteobacterial ancestors. The widespread nature of purple bacteria among alphaproteobacteria raises the possibility that cristae evolved from photosynthetic ICMs.