An ancestral bacterial division system is widespread in eukaryotic mitochondria

Abstract

Bacterial division initiates at the site of a contractile Z-ring composed of polymerized FtsZ. The location of the Z-ring in the cell is controlled by a system of three mutually antagonistic proteins, MinC, MinD, and MinE. Plastid division is also known to be dependent on homologs of these proteins, derived from the ancestral cyanobacterial endosymbiont that gave rise to plastids. In contrast, the mitochondria of model systems such as Saccharomyces cerevisiae, mammals, and Arabidopsis thaliana seem to have replaced the ancestral α-proteobacterial Min-based division machinery with host-derived dynamin-related proteins that form outer contractile rings. Here, we show that the mitochondrial division system of these model organisms is the exception, rather than the rule, for eukaryotes. We describe endosymbiont-derived, bacterial-like division systems comprising FtsZ and Min proteins in diverse less-studied eukaryote protistan lineages, including jakobid and heterolobosean excavates, a malawimonad, stramenopiles, amoebozoans, a breviate, and an apusomonad. For two of these taxa, the amoebozoan Dictyostelium purpureum and the jakobid Andalucia incarcerata, we confirm a mitochondrial localization of these proteins by their heterologous expression in Saccharomyces cerevisiae. The discovery of a proteobacterial-like division system in mitochondria of diverse eukaryotic lineages suggests that it was the ancestral feature of all eukaryotic mitochondria and has been supplanted by a host-derived system multiple times in distinct eukaryote lineages.

The changing view of eukaryogenesis – fossils, cells, lineages and how they all come together

“…The most widespread eukaryotic organelle with bacterial ancestry is the mitochondrion. An extensive set of organellar functions are clearly of direct ancestry from α-proteobacteria, including organelle maintenance and replication (Leger et al, 2015), much of aerobic energy metabolism (Müller et al, 2012, as well as others) and even some recent surprises about organelle morphology, such as the mitochondrial contact site (MICOS) complex that is responsible for cristae formation (Muñoz-Gómez et al, 2016). The α-proteobacterial contribution can also be seen in other processes, such as in Fe-S cluster formation (Barberà et al, 2010), β-oxidation of fatty acids (Bolte et al, 2015), the glycine cleavage system (Nývltová et al, 2015) and hemebiosynthesis (Cenci et al, 2016).…”

Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum

“…The bacterial divisome complex, which is built around the polymers of a tubulin ortholog, the GTPase FtsZ, has been entirely replaced in the mitochondria of many eukaryote lineages by proteins of the dynamin superfamily [17]; yet, eukaryotes that have preserved the original FtsZ-based machinery can still be found in all eukaryotic supergroups [18, 19]. …”

The Chloroplast Tubulin Homologs FtsZA and FtsZB from the Red Alga Galdieria sulphuraria Co-assemble into Dynamic Filaments

“…Miyagishima et al (4) concluded that FtsZ2 in green plants and algae and FtsZA in red algae descended from the original single FtsZ from the cyanobacterium and that FtsZ1 and FtsZB arose by separate gene duplications. There is a similar duplication of FtsZ in the mitochondria that have kept FtsZ, one with and one without the C-terminal peptide (4,19). As in Arabidopsis, the FtsZ with the C-terminal peptide may interact with a membrane protein to tether the Z ring, whereas the one without may play a regulatory role.…”