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Eukaryotes and Multicells: Origin Eukaryotes and Multicells: Secondary article Origin Article Contents . Eukaryotes: Basic Definitions Ben Waggoner, University of Central Arkansas, Conway, Arkansas, USA . Multicellularity: Basic Definitions Among the most important evolutionary events of all time are the origins of eukaryotic cells and of multicellularity. Both the evolution of eukaryotes and the origins of multicellularity (convergently evolved in numerous taxa) can be studied using insights from both palaeontology and molecular biology. Eukaryotes: Basic Definitions Cell biological evidence The defining feature of eukaryotic cells is the presence of a membrane-bound nucleus containing the genome. In all The closest living relatives to eukaryotes are probably the eukaryotes, the genome is composed of linear chromo- prokaryotes in the domain Archaea. The Archaea, once somes, instead of the circular genome typical of prokar- referred to as Archaebacteria, include many members that yotes. The DNA is complexed with specialized proteins, inhabit extreme environments. Archaea are metabolically the histones. Furthermore, eukaryotic cell division is most like true Bacteria, with which they were grouped for a fundamentally different from prokaryotic fission: most long time, but share many similarities with the Eukaryota. eukaryote nuclei divide by mitosis. Mitosis depends on the These include histone proteins; similar nucleic acid presence of microtubules, made up of specific tubulin replication proteins, including polymerases and TATA- proteins, which make up the motility system that pulls binding proteins; and similar processing of tRNA introns chromosomes apart. These microtubules are often, though (Edgell and Doolittle, 1997; Olsen and Woese, 1997; Pace, not always, organized by small organelles known as 1997). At least some archaeans – notably Thermoplasma,a centrioles. Microtubules also make up part of the wall-less hyperthermophile – show further similarities with cytoskeleton, a network of intracellular filaments that is eukaryotes, such as flexible cell membranes containing much more complex than anything seen in prokaryotes. sterols; actin-like cytoplasmic filaments; homologues of Besides microtubules, the cytoskeleton includes microfila- typical eukaryote proteins such as calmodulin and super- ments and intermediate filaments, also made of specialized oxide dismutase; uniquely shaped ribosomes; and a proteins. glycoprotein coat resembling a eukaryote glycocalyx (Dyer The vast majority of known eukaryotes contain other and Obar, 1994; Kandler, 1994). membrane-bound organelles, notably mitochondria, the It is not settled yet whether eukaryotes and archaeans are sites of oxidative respiration. The few eukaryotes that lack monophyletic sister taxa, or whether archaeans are mitochondria may represent very early branches of the paraphyletic and eukaryotes are the sister taxon to a eukaryote tree, although some have probably secondarily subgroup of thermophilic archaeans, the Eocytes or lost their mitochondria. Photosynthetic eukaryotes carry Crenarchaeota. The bulk of molecular phylogenetic out photosynthesis in additional organelles, the plastids. evidence seems to favour the former hypothesis (Pace, Also characteristic of eukaryotes are dictyosomes (also 1997; Woese, 1998; but see Forterre, 1997). However, known as the Golgi apparatus), the endoplasmic reticulum archaeans also share some features with true Bacteria, such (a complex network of infolded membranes), and vacuoles as operonic genome organization, restriction endonu- for endocytosis and exocytosis. These collectively make up cleases and various metabolic features (Ouzounis and the endomembrane system for synthesis, uptake, and Kyrpides, 1996; Olsen and Woese, 1997). Archaeans also transport of large molecules. Finally, many eukaryotes have a number of ‘orphan’ features not found anywhere bear undulipodia – elongated motility organelles, with an else, such as ether-linked membrane phospholipids. internal structure of nine pairs of microtubules surround- Archaeans are not ‘Eukaryota in miniature’. Nor are ing two inner tubules (‘9 1 2’ structure). These are rooted archaeans necessarily ‘archaic’, having evolved, adapted by basal bodies, which have the same structure as and diversified for over 3.5 billion years (Forterre, 1997). centrioles; both centrioles and basal bodies are known as What is certain is that a number of ‘typical eukaryote’ microtubule organizing centres (MTOCs) (Figures 1, 2a). features appear to go back to the archaean–eukaryote ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net 1 Eukaryotes and Multicells: Origin Figure 1 Semidiagrammatic drawing of a generalized eukaryote cell. The connections between the endoplasmic reticulum, the organelles and the nuclear membrane would not necessarily exist permanently in a living cell; they have been included to show the topological arrangements of the organelles and membrane system. The cytoskeleton has been omitted for clarity. common ancestor, if not further (Olsen and Woese, 1997). Many prokaryotes have complex folded membranes with- Discrepancies among gene-based phylogenies may be in their cells. It is plausible that such a system was present in explained by horizontal gene transfer, still widespread eukaryote ancestors – perhaps increasing surface area for among prokaryotes and possibly the dominant evolution- metabolic functions – and was modified to produce a ary dynamic in the earliest living systems (Pace, 1997; nuclear membrane and endoplasmic reticulum. Sterols Woese, 1998). It is noteworthy that the earliest branches of increase membrane fluidity, and were probably a necessary both the Archaea and the Bacteria are thermophilic (Pace, precondition for these evolutionary steps (Knoll, 1983). 1997). Archaean features that originally were adaptive for The circular genomes of prokaryotes are apparently life at high temperatures, such as membrane sterols, may constrained in size: prokaryotic genomes typically fall have been co-opted for other functions in early eukaryotes. between 106 and 107 base pairs, whereas eukaryotes range 2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net Eukaryotes and Multicells: Origin from 107 to 1011 base pairs. Linear chromosomes may have respiration (Whatley and Chapman-Andresen, 1990). permitted this increase in genome size. Yet their actual Parabasalian protists, such as Trichomonas and Tricho- origins are problematic: how did DNA evolve a linear form nympha (Figure 2b), have lost their mitochondria but from a circular ancestral state? According to Woese (1998), contain abundant bacterial endosymbionts, whose func- it may not have. The earliest ‘progenotes’ may have had tion is not clear (Dyer, 1990). A number of protists contain genomes consisting of small, linear DNA segments endosymbiotic cyanobacteria, ranging from symbionts distributed randomly at division, since the rudimentary that can be cultured independently to wall-less forms replication and repair mechanisms available could not incapable of independent growth (Dyer and Obar, 1994). have handled larger chromosomes. Selection at the Obligate bacterial–eukaryote endosymbioses have even subcellular level for more efficient replication would have been created in the laboratory (Jeon, 1991). Interestingly, made it possible to handle larger DNA segments, allowing some eukaryotes contain plastids derived from other the evolution of larger chromosomes, whether linear or eukaryotes. Dinoflagellate and euglenid plastids are circular. The evolution of the centromere, telomeres and surrounded by a triple membrane and apparently came mitosis might have been driven by strong selection for from ‘captured’ eukaryote plastids. Cryptomonad flagel- efficient distribution of copies of all genes to offspring lates contain plastids with a DNA-containing ‘nucleo- (Margulis, 1981; Woese, 1998). There are nonmitotic morph’, surrounded by four membranes. These apparently mechanisms for distributing genes, such as the fission of were derived from a complete, endosymbiotic eukaryote the unique achromosomal macronucleus in ciliates (Lynn (Dyer and Obar, 1994). and Small, 1990), which may be analogous to the fission of Other eukaryotic organelles may also be symbiotic in the earliest progenotes. These mechanisms, however, are origin, although the evidence is less clear. A claim that inefficient compared with mitosis (Margulis, 1981). DNA exists in the basal bodies of the undulipodia of the single-celled green alga Chlamydomonas remains uncon- firmed and contentious at best. Nonetheless, microtubule- Endosymbiosis and eukaryote evolution like structures in some spirochaete bacteria (Figure 2c); By far the best-supported theory for the origin of complex similarities between eukaryotic tubulins and certain eukaryote organelles is serial endosymbiosis, which states spirochaete proteins; peculiar linkage of undulipodia- that organelles are descended from symbiotic prokaryotes related genes in Chlamydomonas; RNA associated with that colonized the cytoplasm of early eukaryotes. This basal bodies; and extant protists that move by means of theory goes back to the late nineteenth century, but was attached symbiotic bacteria, all may support a symbiotic rejected by most biologists until its revival in the 1970s, origin for both undulipodia and centrioles (Dyer and Obar, primarily by Lynn Margulis (e.g. Margulis, 1981). The 1994). This is especially important because microtubules evidence for serial
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