Mitochondrial cristae expand the surface area of respiratory membranes and ultimately allow for the evolutionary scaling of respiration with cell volume across eukaryotes. The discovery of Mic60 homologs among alphaproteobacteria, the closest extant relatives of mitochondria, suggested that cristae might have evolved from bacterial intracytoplasmic membranes (ICMs). Here, we investigated the predicted structure and function of alphaproteobacterial Mic60, and a protein encoded by an adjacent gene Orf52, in two distantly related purple alphaproteobacteria, Rhodobacter sphaeroides and Rhodopseudomonas palustris. In addition, we assessed the potential physical interactors of Mic60 and Orf52 in R. sphaeroides. We show that the three α helices of mitochondrial Mic60's mitofilin domain, as well as its adjacent membrane-binding amphipathic helix, are present in alphaproteobacterial Mic60. The disruption of Mic60 and Orf52 caused photoheterotrophic growth defects, which are most severe under low light conditions, and both their disruption and overexpression led to enlarged ICMs in both studied alphaproteobacteria. We also found that alphaproteobacterial Mic60 physically interacts with BamA, the homolog of Sam50, one of the main physical interactors of eukaryotic Mic60. This interaction, responsible for making contact sites at mitochondrial envelopes, has been conserved in modern alphaproteobacteria despite more than a billion years of evolutionary divergence. Our results suggest a role for Mic60 in photosynthetic ICM development and contact site formation at alphaproteobacterial envelopes. Overall, we provide support for the hypothesis that mitochondrial cristae evolved from alphaproteobacterial ICMs and have therefore improved our understanding of the nature of the mitochondrial ancestor.

Center Algatech Institute of Microbiology Czech Academy of Sciences 37901 Třeboň Czech Republic

Centre for Comparative Genomics and Evolutionary Bioinformatics Department of Biochemistry and Molecular Biology Dalhousie University Halifax NS B3H 4R2 Canada

Department of Biological Sciences Purdue University West Lafayette IN 47907 USA

Department of Chemistry and Biomolecular Sciences University of Ottawa Ottawa ON K1N 6N5 Canada

Department of Microbiology and Immunology University of British Columbia Vancouver BC V6T 1Z3 Canada

Institute of Evolutionary Biology Barcelona 08003 Catalonia Spain

Institute of Parasitology Biology Center Czech Academy of Sciences 37005 České Budějovice Czech Republic

Curr Biol. 2023 Mar 27;33(6):R219-R221. doi: 10.1016/j.cub.2023.02.037. PubMed

Curr Biol. 2023 Apr 10;33(7):1396. doi: 10.1016/j.cub.2023.03.049. PubMed

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