Phylogenetic Analysis of Eukaryotic Thiolases Suggests Multiple Proteobacterial Origins

Abstract

Eukaryotic thiolases are essential enzymes located in three different compartments (peroxisome, mitochondrion, and cytosol) that can display catabolic or anabolic functions. They are responsible for the thiolytic cleavage of oxidized acyl-CoA (thiolase I; EC 2.3.1.16) and the synthesis or degradation of acetoacetyl-CoA (thiolase II; EC 2.3.1.9). Phylogenetic analysis of eukaryotic thiolase sequences showed that they form six distinct clusters, one of them highly divergent, which are in good correlation with their class and subcellular location. When analyzed together with a representative sample of prokaryotic thiolases, all eukaryotic thiolase groups emerged close to proteobacterial sequences. Metazoan cytosolic thiolase II was related to alpha-proteobacterial sequences, suggesting a mitochondrial origin. Unexpectedly, cytosolic thiolases from green plants and fungi as well as at least one member of all eukaryotic peroxisomal and mitochondrial thiolases had delta-proteobacteria as closest relatives. Our analysis suggests that these eukaryotic peroxisomal and mitochondrial thiolases may have been acquired from delta-proteobacteria prior to the ancestor of all known eukaryotes.

Molecular characterization of ltp3 and ltp4, essential for C24-branched chain sterol-side-chain degradation in Rhodococcus rhodochrous DSM 43269

“…Strikingly, in a phylogenetic analysis of annotated thiolase proteins of strain RHA1 and characterized thiolases (Peretó et al, 2005), Ltp3 DSM 43269 and Ltp4 DSM 43269 cluster separately from most of the previously characterized thiolase enzymes (Fig. 4).…”

Selective forces for the origin of the eukaryotic nucleus

“…Their phylogenetic distribution in eukaryotes suggests that they were present in the last common eukaryotic ancestor. (51) Regarding the archaeal heritage, although most archaeal metabolic pathways were lost in favour of the moreefficient bacterial ones, some may have been retained, at least partially, and adapted to particular functions. This appears to be the case of the mevalonate pathway leading to the formation of isopentenyl-diphosphate in the biosynthesis of isoprenoids, a route shared by archaea and eukaryotes but not by bacteria, which use mainly the deoxyxyllulose-5-phosphate pathway.…”

“…We propose that the loss of the myxobacterial outer membrane improved the exchange of molecules with the external environment and was also linked to the fact that many metabolic reactions that previously took place in the periplasm (a metabolic compartment) were transferred to other membranous compartments. These include the mitochondrion and also peroxisomes, which may have evolved very early, (51) accompanying the development of an endomembrane system and the emergence of phagocytic capacities in the ancestral eukaryote. The eukaryotic genome would have resulted from the integration of genes from three different origins.…”

Special delivery from mitochondria to peroxisomes

“…Although the current view is that peroxisomes arise both from the division of pre-existing peroxisomes and from the endoplasmic reticulum (ER) [1][2][3][4][5] , previous studies have invoked mitochondrion 6 , the ER [2][3][4][5]7 or endosymbionts 8 as sources of peroxisomes, based on knowledge of metabolites shared between peroxisomes, mitochondria and the ER and either the proximity of these organelles with each other, or even physical contacts between them 9,10 . Some of the work in a recent paper by Neuspiel et al 11 adds to this body of knowledge by providing strong support that previously uncharacterized mitochondriallyderived vesicles (MDVs) might account for a specific form of vesicular traffic between mitochondria and peroxisomes.…”