Origin of Eukaryotes

Much of the visible living world around us is characterized by cells that contain a nucleus enclosing the genetic material, a highly specialized network of dynamic interconnected membrane compartments, energy-producing mitochondria, and a cytoskeletal meshwork that can produce a dazzling variety of cellular shapes. These “eukaryotic” cells, which only represent a small fraction of the total cellular diversity on earth, have an internal organization that is strikingly different from that of “prokaryotes,” which lack nuclei or any internal membrane-bound compartments. Given the great structural chasm between these cell types, the question of eukaryotic origins is one of the most enduring mysteries in modern biology. Over the course of the 20th century, advances in cytology, the characterization of DNA as the universal genetic material, and pioneering work on phylogenies of ribosomal RNA all combined to establish a common origin for all life and identified a deep split in the prokaryotic world between the domains of archaea (once called Archaebacteria) and bacteria (once called Eubacteria). At the close of the 20th century, phylogenetic data had been used to support either the three-domain view of life (monophyletic Bacteria, Archaea, and Eukarya) or a competing two-domain model, which features a paraphyletic archaeal grade from which the eukaryotes emerged. These two competing views are relevant to the origin of the eukaryotes since they each suggest different characteristics of the eukaryotic progenitor. Apart from the convincing demonstration that plastids, of which chloroplasts are the most familiar, and mitochondria are derived from endosymbiotic bacteria, the field of eukaryotic origins remains full of uncertainties and controversy. Cell biological arguments have been used to support a bewildering variety of models for the origins of the nucleus and other aspects of eukaryotic cellular organization. Studies of the breadth of eukaryotic diversity help paint a convincing picture of a last eukaryotic common ancestor possessed of mitochondria, a complete cytoskeleton and trafficking machinery. In parallel, newly sequenced bacterial and archaeal genomes have revealed prokaryotic homologues for many genes originally deemed eukaryotic “inventions,” reducing the perceived gap between prokaryotic and eukaryotic complexity. The last few years in particular have generated a great deal of excitement, as newly discovered archaeal genomes, which includes a complete genome from the recently cultured Asgard archaeon Prometheoarchaeum syntrophicum, have shifted the consensus steadily toward models of eukaryotes emerging from the symbiosis of an Asgard-like archaeal host and a protomitochondrial bacterial cell. Recent advances in super-resolution microscopy, meta-genomics, and gene editing techniques mean that archaea and bacteria can be studied in greater cellular and ecological detail than ever before, raising hopes that insights from comparative cell biology will help us distinguish between competing models of eukaryogenesis in the near future.