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Evidence supporting an antimicrobial origin of targeting peptides to endosymbiotic organelles

View ORCID ProfileClotilde Garrido, View ORCID ProfileOliver D. Caspari, Yves Choquet, Francis-André Wollman, View ORCID ProfileIngrid Lafontaine
doi: https://doi.org/10.1101/2020.03.04.974964
Clotilde Garrido
1UMR7141, Institut de Biologie Physico-Chimique (CNRS/Sorbonne Université), 13 Rue Pierre et Marie Curie, 75005 Paris, France
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Oliver D. Caspari
1UMR7141, Institut de Biologie Physico-Chimique (CNRS/Sorbonne Université), 13 Rue Pierre et Marie Curie, 75005 Paris, France
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Yves Choquet
1UMR7141, Institut de Biologie Physico-Chimique (CNRS/Sorbonne Université), 13 Rue Pierre et Marie Curie, 75005 Paris, France
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Francis-André Wollman
1UMR7141, Institut de Biologie Physico-Chimique (CNRS/Sorbonne Université), 13 Rue Pierre et Marie Curie, 75005 Paris, France
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Ingrid Lafontaine
1UMR7141, Institut de Biologie Physico-Chimique (CNRS/Sorbonne Université), 13 Rue Pierre et Marie Curie, 75005 Paris, France
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  • For correspondence: ingrid.lafontaine@ibpc.fr
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Abstract

Mitochondria and chloroplasts emerged from primary endosymbiosis. Most proteins of the endosymbiont were subsequently expressed in the nucleo-cytosol of the host and organelle-targeted via the acquisition of N-terminal presequences, whose evolutionary origin remains enigmatic. Using a quantitative assessment of their physico-chemical properties, we show that organelle targeting peptides, which are distinct from signal peptides targeting other subcellular compartments, group with a subset of antimicrobial peptides. We demonstrate that extant antimicrobial peptides target a fluorescent reporter to either the mitochondria or the chloroplast in the green alga Chlamydomonas reinhardtii and, conversely, that extant targeting peptides still display antimicrobial activity. Thus, we provide strong computational and functional evidence for an evolutionary link between organelle-targeting and antimicrobial peptides. Our results support the view that resistance of bacterial progenitors of organelles to the attack of host antimicrobial peptides has been instrumental in eukaryogenesis and in emergence of photosynthetic eukaryotes.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 21, 2020.
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Evidence supporting an antimicrobial origin of targeting peptides to endosymbiotic organelles
Clotilde Garrido, Oliver D. Caspari, Yves Choquet, Francis-André Wollman, Ingrid Lafontaine
bioRxiv 2020.03.04.974964; doi: https://doi.org/10.1101/2020.03.04.974964
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Evidence supporting an antimicrobial origin of targeting peptides to endosymbiotic organelles
Clotilde Garrido, Oliver D. Caspari, Yves Choquet, Francis-André Wollman, Ingrid Lafontaine
bioRxiv 2020.03.04.974964; doi: https://doi.org/10.1101/2020.03.04.974964

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