Eukaryotes and Multicells:OriginBen Waggoner,University of Central Arkansas, Conway, Arkansas, USAAmong the most important evolutionary events of all time are the origins of eukaryotic cellsand of multicellularity. Both the evolution of eukaryotes and the origins of multicellularity(convergently evolved in numerous taxa) can be studied using insights from bothpalaeontology and molecular biology.Eukaryotes: Basic DefinitionsThe defining feature of eukaryotic cells is the presence of amembrane-bound nucleus containing the genome. In alleukaryotes, the genome is composed of linear chromo-somes, instead of the circular genome typical of prokar-yotes. The DNA is complexed with specialized proteins,the histones. Furthermore, eukaryotic cell division isfundamentally different from prokaryotic fission: mosteukaryote nuclei divide by mitosis. Mitosis depends on thepresence of microtubules, made up of specific tubulinproteins, which make up the motility system that pullschromosomes apart. These microtubules are often, thoughnot always, organized by small organelles known ascentrioles. Microtubules also make up part of thecytoskeleton, a network of intracellular filaments that ismuch more complex than anything seen in prokaryotes.Besides microtubules, the cytoskeleton includes microfila-ments and intermediate filaments, also made of specializedproteins.The vast majority of known eukaryotes contain othermembrane-bound organelles, notably mitochondria, thesites of oxidative respiration. The few eukaryotes that lackmitochondria may represent very early branches of theeukaryote tree, although some have probably secondarilylost their mitochondria. Photosynthetic eukaryotes carryout photosynthesis in additional organelles, the plastids.Also characteristic of eukaryotes are dictyosomes (alsoknown as the Golgi apparatus), the endoplasmic reticulum(a complex network of infolded membranes), and vacuolesfor endocytosis and exocytosis. These collectively make upthe endomembrane system for synthesis, uptake, andtransport of large molecules. Finally, many eukaryotesbear undulipodia – elongated motility organelles, with aninternal structure of nine pairs of microtubules surround-ing two inner tubules (‘9 1 2’ structure). These are rootedby basal bodies, which have the same structure ascentrioles; both centrioles and basal bodies are known asmicrotubule organizing centres (MTOCs) (Figures 1, 2a).Cell biological evidenceThe closest living relatives to eukaryotes are probably theprokaryotes in the domain Archaea. The Archaea, oncereferred to as Archaebacteria, include many members thatinhabit extreme environments. Archaea are metabolicallymost like true Bacteria, with which they were grouped for along time, but share many similarities with the Eukaryota.These include histone proteins; similar nucleic acidreplication proteins, including polymerases and TATA-binding proteins; and similar processing of tRNA introns(Edgell and Doolittle, 1997; Olsen and Woese, 1997; Pace,1997). At least some archaeans – notably Thermoplasma,awall-less hyperthermophile – show further similarities witheukaryotes, such as flexible cell membranes containingsterols; actin-like cytoplasmic filaments; homologues oftypical eukaryote proteins such as calmodulin and super-oxide dismutase; uniquely shaped ribosomes; and aglycoprotein coat resembling a eukaryote glycocalyx (Dyerand Obar, 1994; Kandler, 1994).It is not settled yet whether eukaryotes and archaeans aremonophyletic sister taxa, or whether archaeans areparaphyletic and eukaryotes are the sister taxon to asubgroup of thermophilic archaeans, the Eocytes orCrenarchaeota. The bulk of molecular phylogeneticevidence seems to favour the former hypothesis (Pace,1997; Woese, 1998; but see Forterre, 1997). However,archaeans also share some features with true Bacteria, suchas operonic genome organization, restriction endonu-cleases and various metabolic features (Ouzounis andKyrpides, 1996; Olsen and Woese, 1997). Archaeans alsohave a number of ‘orphan’ features not found anywhereelse, such as ether-linked membrane phospholipids.Archaeans are not ‘Eukaryota in miniature’. Nor arearchaeans necessarily ‘archaic’, having evolved, adaptedand diversified for over 3.5 billion years (Forterre, 1997).What is certain is that a number of ‘typical eukaryote’features appear to go back to the archaean–eukaryoteArticle ContentsSecondary article.Eukaryotes: Basic Definitions.Multicellularity: Basic Definitions1ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.netcommon ancestor, if not further (Olsen and Woese, 1997).Discrepancies among gene-based phylogenies may beexplained by horizontal gene transfer, still widespreadamong prokaryotes and possibly the dominant evolution-ary dynamic in the earliest living systems (Pace, 1997;Woese, 1998). It is noteworthy that the earliest branches ofboth the Archaea and the Bacteria are thermophilic (Pace,1997). Archaean features that originally were adaptive forlife at high temperatures, such as membrane sterols, mayhave been co-opted for other functions in early eukaryotes.Many prokaryotes have complex folded membranes with-in their cells. It is plausible that such a system was present ineukaryote ancestors – perhaps increasing surface area formetabolic functions – and was modified to produce anuclear membrane and endoplasmic reticulum. Sterolsincrease membrane fluidity, and were probably a necessaryprecondition for these evolutionary steps (Knoll, 1983).The circular genomes of prokaryotes are apparentlyconstrained in size: prokaryotic genomes typically fallbetween 106and 107base pairs, whereas eukaryotes rangeFigure 1 Semidiagrammatic drawing of a generalized eukaryote cell. The connections between the endoplasmic reticulum, the organelles and thenuclear membrane would not necessarily exist permanently in a living cell; they have been included to show the topological arrangements of the organellesand membrane system. The cytoskeleton has been omitted for clarity.Eukaryotes and Multicells: Origin2ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.netfrom 107to 1011base pairs. Linear chromosomes may havepermitted this increase in genome size. Yet their actualorigins are problematic: how did DNA evolve a linear formfrom a circular ancestral state? According to Woese (1998),it may not have. The earliest ‘progenotes’ may have