TitleAncient dynamin segments capture early stages of host-mitochondrial integration.
Publication TypeJournal Article
Year of Publication2015
AuthorsPurkanti R, Thattai M
JournalProc Natl Acad Sci U S A
Volume112
Issue9
Pagination2800-5
Date Published2015 Mar 3
ISSN1091-6490
KeywordsAnimals, Arabidopsis, Caenorhabditis elegans, Chloroplasts, Dictyostelium, Drosophila melanogaster, Dynamins, Evolution, Molecular, Humans, Mitochondria, Mitochondrial Dynamics, Saccharomyces cerevisiae, Schizosaccharomyces
Abstract

Eukaryotic cells use dynamins-mechano-chemical GTPases--to drive the division of endosymbiotic organelles. Here we probe early steps of mitochondrial and chloroplast endosymbiosis by tracing the evolution of dynamins. We develop a parsimony-based phylogenetic method for protein sequence reconstruction, with deep time resolution. Using this, we demonstrate that dynamins diversify through the punctuated transformation of sequence segments on the scale of secondary-structural elements. We find examples of segments that have remained essentially unchanged from the 1.8-billion-y-old last eukaryotic common ancestor to the present day. Stitching these together, we reconstruct three ancestral dynamins: The first is nearly identical to the ubiquitous mitochondrial division dynamins of extant eukaryotes, the second is partially preserved in the myxovirus-resistance--like dynamins of metazoans, and the third gives rise to the cytokinetic dynamins of amoebozoans and plants and to chloroplast division dynamins. The reconstructed sequences, combined with evolutionary models and published functional data, suggest that the ancestral mitochondrial division dynamin also mediated vesicle scission. This bifunctional protein duplicated into specialized mitochondrial and vesicle variants at least three independent times--in alveolates, green algae, and the ancestor of fungi and metazoans-accompanied by the loss of the ancient prokaryotic mitochondrial division protein FtsZ. Remarkably, many extant species that retain FtsZ also retain the predicted ancestral bifunctional dynamin. The mitochondrial division apparatus of such organisms, including amoebozoans, red algae, and stramenopiles, seems preserved in a near-primordial form.

DOI10.1073/pnas.1407163112
Alternate JournalProc. Natl. Acad. Sci. U.S.A.
PubMed ID25691734
PubMed Central IDPMC4352829
Grant List500103/Z/09/Z / / Wellcome Trust / United Kingdom