A sophisticated, differentiated Golgi in the ancestor of eukaryotes

Abstract

BackgroundThe Golgi apparatus is a central meeting point for the endocytic and exocytic systems in eukaryotic cells, and the organelle’s dysfunction results in human disease. Its characteristic morphology of multiple differentiated compartments organized into stacked flattened cisternae is one of the most recognizable features of modern eukaryotic cells, and yet how this is maintained is not well understood. The Golgi is also an ancient aspect of eukaryotes, but the extent and nature of its complexity in the ancestor of eukaryotes is unclear. Various proteins have roles in organizing the Golgi, chief among them being the golgins.ResultsWe address Golgi evolution by analyzing genome sequences from organisms which have lost stacked cisternae as a feature of their Golgi and those that have not. Using genomics and immunomicroscopy, we first identify Golgi in the anaerobic amoeba Mastigamoeba balamuthi. We then searched 87 genomes spanning eukaryotic diversity for presence of the most prominent proteins implicated in Golgi structure, focusing on golgins. We show some candidates as animal specific and others as ancestral to eukaryotes.ConclusionsNone of the proteins examined show a phyletic distribution that correlates with the morphology of stacked cisternae, suggesting the possibility of stacking as an emergent property. Strikingly, however, the combination of golgins conserved among diverse eukaryotes allows for the most detailed reconstruction of the organelle to date, showing a sophisticated Golgi with differentiated compartments and trafficking pathways in the common eukaryotic ancestor.Electronic supplementary materialThe online version of this article (10.1186/s12915-018-0492-9) contains supplementary material, which is available to authorized users.

The GRASP domain in golgi reassembly and stacking proteins: differences and similarities between lower and higher Eukaryotes

“…The Golgi apparatus is an ancient and ubiquitous organelle in eukaryotic cells . Interestingly, it has been suggested before, based on a Golgi evolution phylogenetic analyses, that a GRASP65‐homolog is likely to have been present in the last eukaryotic common ancestor since a GRASP65‐homolog was observed in all six eukaryotic supergroups, although not in all the genomes tested . We decided to analyze the sequence similarity between the DGRASPs (SPR‐free sequence) in the human and the fungi, inside the Opisthokonta supergroup context, to look for correlations between the experimental data and protein sequence evolution.…”

The GRASP domain in Golgi Reassembly and Stacking Proteins: differences and similarities between lower and higher Eukaryotes

“…The Golgi apparatus is an ancient and ubiquitous organelle in eukaryotic cells [60]. Interestingly, it has been suggested before, based on a Golgi evolution phylogenetic analyses, that a GRASP65-homologue is likely to have been present in the last eukaryotic common ancestor since a GRASP65-homologue was observed in all 6 eukaryotic supergroups, although not in all the genomes tested [61]. We decided to analyze the sequence similarity between the DGRASPs (SPRfree sequence) in the human and the fungi, inside the Opisthokonta supergroup context, to look for correlations between the experimental data and protein sequence evolution.…”

Bacterial genes outnumber archaeal genes in eukaryotic genomes

“…Eukaryotic cells are generally much larger in size, more complex in organization and have larger genomes possessing introns that are removed (spliced) from the mRNA on spliceosomes [2]. Eukaryotic cells always harbor a system of internal membranes [3,4] that form the endoplasmic reticulum and the cell nucleus, where splicing takes place [5]. Furthermore, eukaryotes typically possess double membrane bounded bioenergetic organelles, mitochondria, which were present in the eukaryote common ancestor (LECA) [6,7], but have undergone severe reduction in some lineages [8,9].…”