Biogenesis, inheritance and 3D ultrastructure of the microsporidian mitosome

Christian Hacker, Kacper Sendra, Priyanka Devi Keisham, Teodora Filipescu, James Lucocq, Fatemeh Salimi, Sophie Grace Alicia Ferguson, David Bhella, Stuart MacNeill, Martin Embley, John Milton Lucocq*

*Corresponding author for this work

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Abstract

During the reductive evolution of obligate intracellular parasites called microsporidia, a tiny remnant mitochondrion (mitosome) lost its typical cristae, organellar genome, and most canonical functions. Here, we combine electron tomography, stereology, immunofluorescence microscopy, and bioinformatics to characterise mechanisms of growth, division, and inheritance of this minimal mitochondrion in two microsporidia species (grown within a mammalian RK13 culture-cell host). Mitosomes of Encephalitozoon cuniculi (2–12/cell) and Trachipleistophora hominis (14–18/nucleus) displayed incremental/non-phasic growth and division and were closely associated with an organelle identified as equivalent to the fungal microtubule-organising centre (microsporidian spindle pole body; mSPB). The mitosome–mSPB association was resistant to treatment with microtubule-depolymerising drugs nocodazole and albendazole. Dynamin inhibitors (dynasore and Mdivi-1) arrested mitosome division but not growth, whereas bioinformatics revealed putative dynamins Drp-1 and Vps-1, of which, Vps-1 rescued mitochondrial constriction in dynamin-deficient yeast (Schizosaccharomyces pombe). Thus, microsporidian mitosomes undergo incremental growth and dynamin-mediated division and are maintained through ordered inheritance, likely mediated via binding to the microsporidian centrosome (mSPB).
Original languageEnglish
Article numbere202201635
Number of pages23
JournalLife Science Alliance
Volume7
Issue number1
Early online date30 Oct 2023
DOIs
Publication statusPublished - 1 Jan 2024

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