Evolutionary conservation and in vitro reconstitution of microsporidian iron–sulfur cluster biosynthesis

Sven-a. Freibert, Alina V. Goldberg, Christian Hacker, Sabine Molik, Paul Dean, Tom A. Williams, Sirintra Nakjang, Shaojun Long, Kacper Sendra, Eckhard Bill, Eva Heinz, Robert P. Hirt, John M Lucocq, T. Martin Embley, Roland Lill

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    Abstract

    Microsporidians are obligate intracellular parasites that have minimized their genome content and sub-cellular structures by reductive evolution. Here, we demonstrate that cristae-deficient mitochondria (mitosomes) of Trachipleistophora hominis are the functional site of iron–sulfur cluster (ISC) assembly, which we suggest is the essential task of these organelles. Cell fractionation, fluorescence imaging and immunoelectron microscopy demonstrate that mitosomes contain a complete pathway for [2Fe–2S] cluster biosynthesis that we biochemically reconstituted using purified mitosomal ISC proteins. The T. hominis cytosolic iron–sulfur protein assembly (CIA) pathway includes the essential Cfd1–Nbp35 scaffold complex that assembles a [4Fe–4S] cluster as shown by spectroscopic methods in vitro. Phylogenetic analyses reveal that the ISC and CIA pathways are predominantly bacterial, but their cytosolic and nuclear target Fe/S proteins are mainly archaeal. This mixed evolutionary history of Fe/S-related proteins and pathways, and their strong conservation among highly reduced parasites, provides compelling evidence for the ancient chimeric ancestry of eukaryotes.
    Original languageEnglish
    Pages (from-to)13932
    JournalNature Communications
    Volume8
    DOIs
    Publication statusPublished - 4 Jan 2017

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    Freibert, S., Goldberg, A. V., Hacker, C., Molik, S., Dean, P., Williams, T. A., Nakjang, S., Long, S., Sendra, K., Bill, E., Heinz, E., Hirt, R. P., Lucocq, J. M., Embley, T. M., & Lill, R. (2017). Evolutionary conservation and in vitro reconstitution of microsporidian iron–sulfur cluster biosynthesis. Nature Communications, 8, 13932. https://doi.org/10.1038/ncomms13932