Analysis of diverse eukaryotes suggests the existence of an ancestral mitochondrial apparatus derived from the bacterial type II secretion system

Lenka Horváthová, Vojtěch Žárský, Tomáš Pánek, Romain Derelle, Jan Pyrih, Alžběta Motyčková, Veronika Klápšťová, Martina Vinopalová, Lenka Marková, Luboš Voleman, Vladimír Klimeš, Markéta Petrů, Zuzana Vaitová, Ivan Čepička, Klára Hryzáková, Karel Harant, Michael W. Gray, Mohamed Chami, Ingrid Guilvout, Olivera Francetic, B. Franz Lang, Čestmír Vlček, Anastasios D. Tsaousis, Marek Eliáš () and Pavel Doležal ()
Additional contact information
Lenka Horváthová: Charles University, BIOCEV
Vojtěch Žárský: Charles University, BIOCEV
Tomáš Pánek: University of Ostrava
Romain Derelle: University of Birmingham
Jan Pyrih: University of Kent
Alžběta Motyčková: Charles University, BIOCEV
Veronika Klápšťová: Charles University, BIOCEV
Martina Vinopalová: Charles University, BIOCEV
Lenka Marková: Charles University, BIOCEV
Luboš Voleman: Charles University, BIOCEV
Vladimír Klimeš: University of Ostrava
Markéta Petrů: Charles University, BIOCEV
Zuzana Vaitová: Charles University, BIOCEV
Ivan Čepička: Charles University
Klára Hryzáková: Charles University
Karel Harant: Charles University, BIOCEV
Michael W. Gray: Dalhousie University
Mohamed Chami: University of Basel
Ingrid Guilvout: Biochemistry of Macromolecular Interactions Unit, Department of Structural Biology and Chemistry, Institut Pasteur, CNRS UMR3528
Olivera Francetic: Biochemistry of Macromolecular Interactions Unit, Department of Structural Biology and Chemistry, Institut Pasteur, CNRS UMR3528
B. Franz Lang: Université de Montréal
Čestmír Vlček: Czech Academy of Sciences
Anastasios D. Tsaousis: University of Kent
Marek Eliáš: University of Ostrava
Pavel Doležal: Charles University, BIOCEV

Nature Communications, 2021, vol. 12, issue 1, 1-18

Abstract: Abstract The type 2 secretion system (T2SS) is present in some Gram-negative eubacteria and used to secrete proteins across the outer membrane. Here we report that certain representative heteroloboseans, jakobids, malawimonads and hemimastigotes unexpectedly possess homologues of core T2SS components. We show that at least some of them are present in mitochondria, and their behaviour in biochemical assays is consistent with the presence of a mitochondrial T2SS-derived system (miT2SS). We additionally identified 23 protein families co-occurring with miT2SS in eukaryotes. Seven of these proteins could be directly linked to the core miT2SS by functional data and/or sequence features, whereas others may represent different parts of a broader functional pathway, possibly also involving the peroxisome. Its distribution in eukaryotes and phylogenetic evidence together indicate that the miT2SS-centred pathway is an ancestral eukaryotic trait. Our findings thus have direct implications for the functional properties of the early mitochondrion.

Date: 2021
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DOI: 10.1038/s41467-021-23046-7

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