Origin of Eukaryotes

by

Gautam Dey, Buzz Baum, David A. Baum

• LAST REVIEWED: 26 August 2020
• LAST MODIFIED: 26 August 2020
• DOI: 10.1093/obo/9780199941728-0108

Introduction

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.

General Overviews

For reviews of eukaryogenesis, refer to Martin, et al. 2015 and Baum 2015. Martin 2005 provides an older, but still useful review, whereas Harold 2014 is an accessible, book-length exploration of cell evolution. Gould, et al. 2008 focuses on the acquisition of plastids and subsequent additional endosymbiotic events. Koonin, et al. 2010 and Lombard, et al. 2012 discuss protein regulatory networks and membrane chemistry across the three domains of life and their implications for eukaryogenesis. Eme, et al. 2014 links molecular data, which drive much of the field, to fossil evidence. Williams, et al. 2013 summarizes phylogenetic arguments for the phylogenetic model that dominates current thinking, namely that archaea/eukarya and bacteria represent the two primary domains of life. Eme, et al. 2017 builds upon the relationship between archaea and models of eukaryogenesis.

• Baum, D. A. 2015. A comparison of autogenous theories for the origin of eukaryotic cells. American Journal of Botany 102:1954–1965.

  Compares different autogenous theories for the origin of the nucleus and eukaryogenesis in general, framed in the context of cellular topology, consilience with modern cell biology and the timing of mitochondrial acquisition.

• Eme, L., S. C. Sharpe, M. W. Brown, et al. 2014. On the age of eukaryotes: Evaluating evidence from fossils and molecular clocks. Cold Spring Harbor Perspectives in Biology 6:a016139.

  Reviews the phylogenetic and fossil evidence on the age of eukaryotes.

• Eme, L., A. Spang, J. Lombard, C. W. Stairs, and T. J. G. Ettema. 2017. Archaea and the origin of eukaryotes. Nature Reviews Microbiology 15:711–723.

  Discusses models for eukaryogenesis in the light of newly discovered and characterized archaeal lineages.

• Gould, S. B., R. F. Waller, and G. I. McFadden. 2008. Plastid evolution. Annual Review of Plant Biology 59:491–517.

  Provides a comprehensive overview of plastid evolution, encompassing primary and secondary endosymbioses, protein targeting to plastids and plastid metabolism.

• Harold, F. M. 2014. In search of cell history: The evolution of life’s building blocks. Chicago: Chicago Univ. Press.

  Provides a synthetic overview of the origin and evolution of cells, with a major focus on the origin of eukaryotes.

• Koonin, E. V., J. Dacks, W. Doolittle, et al. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biology 11:209.

  Analyzes the origins of key eukaryotic protein regulatory modules using comparative genomics.

• Lombard, J., P. López-García, and D. Moreira. 2012. The early evolution of lipid membranes and the three domains of life. Nature Reviews Microbiology 10:507–515.

  Reviews the molecular composition of archaeal and bacterial phospholipid membranes and consequences for models of eukaryogenesis.

• Martin, W. F. 2005. Archaebacteria (Archaea) and the origin of the eukaryotic nucleus. Current Opinion in Microbiology 8:630–637.

  Summarizes the diversity of models for the origin of the nuclear compartment, arguing against nuclear endosymbiotic models.

• Martin, W. F., S. Garg, and V. Zimorski. 2015. Endosymbiotic theories for eukaryote origin. Philosophical Transactions of the Royal Society B: Biological Science 370.1678: 20140318.

  Surveys models of eukaryogenesis with a historical slant, focusing on origins of the nuclear and mitochondrial compartment as well as metabolic considerations.

• Williams, T. A., P. G. Foster, C. J. Cox, et al. 2013. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231–236.

  Summarizes support for having only two primary domains of life, with eukaryotes being embedded within a paraphyletic Archaea.