Bacterial Vesicle Secretion and the Evolutionary Origin of the Eukaryotic Endomembrane System

Eukaryotes possess an elaborate endomembrane system with endoplasmic reticulum, nucleus, Golgi, lysosomes, peroxisomes, autophagosomes, and dynamic vesicle traffic. Theories addressing the evolutionary origin of eukaryotic endomembranes have overlooked the outer membrane vesicles (OMVs) that bacteria, archaea, and mitochondria secrete into their surroundings. We propose that the eukaryotic endomembrane system originated from bacterial OMVs released by the mitochondrial ancestor within the cytosol of its archaeal host at eukaryote origin. Confined within the host's cytosol, OMVs accumulated naturally, fusing either with each other or with the host's plasma membrane. This matched the host's archaeal secretory pathway for cotranslational protein insertion with outward bound mitochondrial-derived vesicles consisting of bacterial lipids, forging a primordial, secretory endoplasmic reticulum as the cornerstone of the eukaryotic endomembrane system.Video Abstract To view the video inline, enable JavaScript on your browser. However, you can download and view the video by clicking on the icon belowHelp with MP4 filesOptionsDownload video (43050 K)

TrendsEukaryogenesis models struggle with explaining the origin of the endomembrane system and the transition from an archaeal plasma membrane based on isoprene ethers to a bacterial-type membrane based on fatty acid esters.Bacteria and archaea secrete outer menbrane vesicles (OMVs) into their surroundings. If the endosymbiont that became the mitochondrion did so in the archaeal host, it physically generated the first vesicles of the endomembrane system.Endosymbiont OMVs could only accumulate in the host's cytosol – fusion with each other could have generated compartments, fusion with the archaeal plasma membrane could have converted its chemical composition.Starting endomembrane origin with outward flux of endosymbiont-derived OMVs integrates mitochondria, their lipids, and their energetics into current models of eukaryote origin, explaining why eukaryotes had a mitochondrion-bearing ancestor.