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The Origin of Eukaryotic Cells Michael Buratovich

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The Origin of Eukaryotic Cells Michael Buratovich Communication The Origin of Eukaryotic Cells Michael Buratovich he cells of modern organisms come in In an attempt to resolve this mystery, Ttwo main structural types: prokaryotic William Martin and Eugene Koonin have and eukaryotic. Prokaryotic cells, which devised a revolutionary and wonderfully are represented by the eubacteria and novel hypothesis to explain the origin of archaea, contain precious little internal com- the nucleus.6 The following features of this partmentalization and have transcriptionally hypothesis with the accompanying evidences coupled translation, whereas eukaryotic that argue in its favor are outlined below. cells, which compose plants, fungi, algae, (Also, see Figure 1.) animals, and a widely diverse group of uni- cellular protists, are equipped with a large 1. The original host of the initial endosymbiosis cadre of intracellular compartments that are that led to mitochondria was a prokaryote related Michael Buratovich functionally specialized for specific intra- to the modern archaea and not a nucleated cellular tasks.1 proto-eukaryote. Phylogenetic analyses of ribosomal RNAs The origin of the more complicated strongly suggested that eukaryotes are a The origin eukaryotic cell type has been partially eluci- sister group of the archaea.7 However, the dated by the now widely-accepted endo- utilization of different genes in another set symbiont theory, which posits that two of of phylogenetic analyses suggested that of the … the major membrane-bound compartments eukaryotes are more closely related to the of eukaryotic cells—mitochondria, the energy- eubacteria.8 An analysis with completely eukaryotic cell making organelles, and chloroplasts, the sequenced genomes has shown that eukar- organelles where photosynthesis occurs in yotic genomes result, at least in part, from type has been plant cells—were formed from ancient a fusion between archaeal and eubacterial bacteria that invaded the cytoplasm of an genomes.9 ancient proto-eukaryotic cell and eventually partially took up residence in that cell. Given the im- Other studies not only corroborate the pressive molecular and genetic similarities dual contribution of archaeal and eubacterial elucidated by between modern mitochondria and one spe- genes to eukaryotic genomes but also cific group of bacteria, the a-proteobacteria,2 strongly suggest that the primitive cell that the now and modern chloroplasts and cyanobacteria,3 played host to the original a-proteobacterial this hypothesis has won widespread accep- invader did not have a nucleus. For exam- widely-accepted tance among biologists and is a common ple, those proteins specific to the nuclear staple of most high school and college biol- envelope and components of the nuclear endosymbiont ogy textbooks. pore complexes, which allow the transport of large molecules to and from the nucleus, While the endosymbiont theory is the best are cobbled together from protein domains theory … present answer to the question of eukaryotic specific to eubacteria and archaea, with vari- cell origins, there is still widespread uncer- ous eukaryotic innovations.10 Also proteomic tainty regarding the identity of the original cell that hosted the initial endosymbiosis. Michael Buratovich holds B.S. and M.A. degrees in bacteriology and The prevailing model asserts that the host microbiology, respectively, from the University of California Davis and a Ph.D. cell initially invaded by those ancient bacte- in cell and developmental biology from the University of California Irvine. ria that eventually became modern mito- He also worked as a postdoctoral research fellow at Sussex University and at the chondria had a nucleus, and, therefore, the University of Pennsylvania and presently is associate professor of biochemistry genesis of mitochondria occurred after the at Spring Arbor University. His research interests range from the tracheal formation of the nucleus and played no me- system of the sow bug to iron metabolism in mitochondria. Buratovich is chanistic role in nuclear formation.4 However, also a steady contributor to the contemporary debate over biological origins. problems abound with this scenario.5 He can be reached by email at: [email protected] Volume 59, Number 3, September 2007 219 Communication The Origin of Eukaryotic Cells analyses of the proteins in the nucleolus, a eubacterial endosymbiont as a source of that dense portion of the nucleoplasm where eubacterial genes. ribosomal RNAs are transcribed and ribosome biogenesis occurs, have also demonstrated 2. The presence of transposable, self-splicing William that these proteins are derived from eubac- group II introns in the genomes of the invading terial and archaeal ancestors.11 These data bacterium posed problems for the host organism, Martin and are best explained if the nucleus and nucleo- since its genome was soon colonized and overrun lus arose in a cell that already contained by transposons whose excision was rather slow. Eugene Koonin have devised Endomembrane Separating splicing a revolutionary accumulation and from translation emergence of solves the intron nuclear membrane. problem: and Spliceosome forms, transcription with nuclear and splicing wonderfully transport. in the nucleus, Continued translation novel gene transfer in the cytoplasm. through lysis. hypothesis to explain the origin of the nucleus. … Most progeny Despite … do not survive. Eubacterial genes drawbacks, and group II introns Genetic chimerism. transpose into host Martin and Gene transfer chromosomes. through occasional Introns disperse and lysis. degenerate. Koonin’s Expression of unspliced introns. hypothesis is a fresh, new and thought- Prokaryotic host provoking piece with prokaryotic symbiont. of theorizing Two independent gene expression that should systems. Coordination of spur new division. experimental examinations into eukaryotic cellular origins. a-Proteobacterial Archaebacterial symbiont host Figure 1 220 Perspectives on Science and Christian Faith Michael Buratovich Modern eukaryotic genomes are loaded with intervening Under these conditions, this early “proto-eukaryote” sequences called introns that interrupt coding sequences. would have certainly made some nonfunctional protein. Introns are initially transcribed when the initial messenger RNA (mRNA) is synthesized but are subsequently The spliceosome components seem to have evolved removed by a process called RNA splicing prior to nuclear from group II intron mRNAs and the Sm protein domain, transport of the mature mRNA to the cytoplasm for transla- which is involved in RNA-processing reactions in 22 tion. RNA splicing is executed by a complex of proteins and archaea. The recruitment of Sm domain proteins to re- small nuclear RNAs (snRNAs) called the spliceosome.12 place the function of the group II intron-encoded maturase provided the impetus for the formation of the spliceo- Spliceosome-excised introns are widely viewed as some. The modern spliceosome contains some twenty having evolved from self-splicing group II introns. An paralogous Sm-domain-containing proteins, and this core impressive list of structural, biochemical, and functional complex is common to all eukaryotes and, therefore, must similarities between group II introns and the processing of have been present in the last common ancestor of all nuclear introns by the spliceosome supports this claim. eukaryotes.23 First of all, the catalytic mechanisms employed by the two types of introns and their use of metal catalysts are strik- 4. Natural selection therefore pressured cells to physically ingly similar.13 Secondly, in vitro experiments have estab- separate the slow process of intron excision from the fast process lished that, like group II introns, the RNA component of of mRNA translation in order to preserve the integrity of gene 24 the spliceosome forms its catalytic core.14 Third, the metal- expression. binding domain of II introns (domain V) can functionally This early cell was under tremendous selective pressure to substitute for the metal-binding portion of one of the isolate the genome from the translational apparatus to RNA components (the U6atac snRNA stem-loop) of the prevent the constant synthesis of junk protein. spliceosome.15 Finally, one of the RNA components of the spliceosome (snRNA U5) can functionally substitute for The nuclear envelope is contiguous with another inter- a particular portion of the group II intron (ID3 subdomain nal cell membrane system: the endoplasmic reticulum. stem-loop).16 These remarkable mechanistic resemblances The cell uses the endoplasmic reticulum to initiate the syn- and functional equivalences imply that spliceosome- theses of membrane-specific proteins, secreted proteins, dependent introns are the evolutionary descendants of membrane phospholipids and steroids. Gene duplication group II introns. patterns suggest that the endoplasmic reticulum arose be- fore the nucleus.25 This means that the nuclear membrane Group II introns, however, are very common in might have resulted from the membranes of the already- eubacteria but extremely rare in the archaea.17 Further- existing endoplasmic reticulum aggregating around the more, group II introns are mobile genetic elements that can region that contains the genome (nucleoplasm).26 Once transpose from one location within a genome to another surrounded by these membranes, this barrier would have and require an intron-encoded reverse transcriptase/ effectively isolated the genome from the translational maturase protein for transposition and proper splicing.18
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