Three-dimensional images reveal the impact of the endosymbiont Midichloria mitochondrii on the host mitochondria

Zerrin Uzum (), Dmitry Ershov, Michael J. Pavia, Adeline Mallet, Olivier Gorgette, Olivier Plantard, Davide Sassera and Fabrizia Stavru
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Zerrin Uzum: Institut Pasteur; CNRS UMR2001
Dmitry Ershov: Institut Pasteur
Michael J. Pavia: Arizona State University
Adeline Mallet: Institut Pasteur
Olivier Gorgette: Institut Pasteur
Olivier Plantard: INRAE, BIOEPAR, Oniris
Davide Sassera: University of Pavia
Fabrizia Stavru: Institut Pasteur; CNRS UMR2001

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract The hard tick, Ixodes ricinus, a main Lyme disease vector, harbors an intracellular bacterial endosymbiont. Midichloria mitochondrii is maternally inherited and resides in the mitochondria of I. ricinus oocytes, but the consequences of this endosymbiosis are not well understood. Here, we provide 3D images of wild-type and aposymbiotic I. ricinus oocytes generated with focused ion beam-scanning electron microscopy. Quantitative image analyses of endosymbionts and oocyte mitochondria at different maturation stages show that the populations of both mitochondrion-associated bacteria and bacterium-hosting mitochondria increase upon vitellogenisation, and that mitochondria can host multiple bacteria in later stages. Three-dimensional reconstructions show symbiosis-dependent morphologies of mitochondria and demonstrate complete M. mitochondrii inclusion inside a mitochondrion. Cytoplasmic endosymbiont located close to mitochondria are not oriented towards the mitochondria, suggesting that bacterial recolonization is unlikely. We further demonstrate individual globular-shaped mitochondria in the wild type oocytes, while aposymbiotic oocytes only contain a mitochondrial network. In summary, our study suggests that M. mitochondrii modulates mitochondrial fragmentation in oogenesis possibly affecting organelle function and ensuring its presence over generations.

Date: 2023
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DOI: 10.1038/s41467-023-39758-x

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