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Discovery of EMRE in fungi resolves the true evolutionary history of the mitochondrial calcium uniporter

Author

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  • Alexandros A. Pittis

    (The Barcelona Institute of Science and Technology
    Universitat Pompeu Fabra (UPF)
    University of British Columbia (UBC)
    Berlin Institute for Advanced Study)

  • Valerie Goh

    (Helmholtz Zentrum München)

  • Alberto Cebrian-Serrano

    (Helmholtz Zentrum München
    German Center for Diabetes Research (DZD))

  • Jennifer Wettmarshausen

    (Helmholtz Zentrum München)

  • Fabiana Perocchi

    (Helmholtz Zentrum München
    Munich Cluster for Systems Neurology)

  • Toni Gabaldón

    (The Barcelona Institute of Science and Technology
    Universitat Pompeu Fabra (UPF)
    ICREA, Pg. Lluís Companys 23
    Barcelona Supercomputing Centre (BSC-CNC) and Institute for Research in Biomedicine (IRB))

Abstract

Calcium (Ca2+) influx into mitochondria occurs through a Ca2+-selective uniporter channel, which regulates essential cellular processes in eukaryotic organisms. Previous evolutionary analyses of its pore-forming subunits MCU and EMRE, and gatekeeper MICU1, pinpointed an evolutionary paradox: the presence of MCU homologs in fungal species devoid of any other uniporter components and of mt-Ca2+ uptake. Here, we trace the mt-Ca2+ uniporter evolution across 1,156 fully-sequenced eukaryotes and show that animal and fungal MCUs represent two distinct paralogous subfamilies originating from an ancestral duplication. Accordingly, we find EMRE orthologs outside Holoza and uncover the existence of an animal-like uniporter within chytrid fungi, which enables mt-Ca2+ uptake when reconstituted in vivo in the yeast Saccharomyces cerevisiae. Our study represents the most comprehensive phylogenomic analysis of the mt-Ca2+ uptake system and demonstrates that MCU, EMRE, and MICU formed the core of the ancestral opisthokont uniporter, with major implications for comparative structural and functional studies.

Suggested Citation

  • Alexandros A. Pittis & Valerie Goh & Alberto Cebrian-Serrano & Jennifer Wettmarshausen & Fabiana Perocchi & Toni Gabaldón, 2020. "Discovery of EMRE in fungi resolves the true evolutionary history of the mitochondrial calcium uniporter," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-17705-4
    DOI: 10.1038/s41467-020-17705-4
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