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Archezoa and the Origin of Eukaryotes Patrick J Problems and paradigms A kingdom’s progress: Archezoa and the origin of eukaryotes Patrick J. Keeling* Summary The taxon Archezoa was proposed to unite a group of very odd eukaryotes that lack many of the characteristics classically associated with nucleated cells, in particular the mitochondrion. The hypothesis was that these cells diverged from other eukaryotes before these characters ever evolved, and therefore they repre- sent ancient and primitive eukaryotic lineages. The kingdom comprised four groups: Metamonada, Microsporidia, Parabasalia, and Archamoebae. Until re- cently, molecular work supported their primitive status, as they consistently branched deeply in eukaryotic phylogenetic trees. However, evidence has now emerged that many Archezoa contain genes derived from the mitochondrial symbiont, revealing that they actually evolved after the mitochondrial symbiosis. In addition, some Archezoa have now been shown to have evolved more recently than previously believed, especially the Microsporidia for which considerable evidence now indicates a relationship with fungi. In summary, the mitochondrial symbiosis now appears to predate all Archezoa and perhaps all presently known eukaryotes. BioEssays 20:87–95, 1998. ௠ 1998 John Wiley & Sons, Inc. INTRODUCTION cyanobacteria and they also lack flagella and basal bodies Prior to the popularization of the endosymbiotic theory, it was (for discussion see Ref. 1). However, according to the widely believed that the evolutionary link between prokary- endosymbiotic theory, the reason photosynthesis is so simi- otes and eukaryotes was the presence of photosynthesis in lar in cyanobacteria and photosynthetic eukaryotes is that cyanobacteria and algae. The biochemistry of oxygenic the plastids of plant and algal cells are derived from a photosynthesis was considered too complicated and too cyanobacterial symbiont. With increasing acceptance of the similar in detail to have arisen twice independently. There- origin of plastids from cyanobacteria, links between cyano- fore, it was reasoned that all photosynthetic organisms were bacteria and the nucleus dissolved, and with it our explana- related, and by extension that cyanobacteria had evolved tion for the origin of eukaryotes. into photosynthetic eukaryotes. This ancestral eukaryote An alternative to the cyanobacterial origin of eukaryotes was thought to be like red algae because their pigments and arose from what seemed like an unlikely source when Carl light-harvesting antennae most closely resemble those of Woese and his colleagues discovered an unexpected divi- sion in prokaryotes in 1977. Woese’s group showed that prokaryotes are composed of two very distantly related School of Botany, University of Melbourne, Parkville, groups,2 which they named Eubacteria and Archaebacteria, Victoria, Australia. now synonymous with Bacteria and Archaea. Archaebacteri- Contract grant sponsor: Natural Sciences and Engi- ologists soon began to find molecular links between archae- neering Research Council of Canada Fellowship. bacteria and eukaryotes,3 and these observations were *Correspondence to: Dr. Patrick J. Keeling, Depart- brought into focus by the demonstration that archaebacteria ment of Biology, Indiana University, Bloomington, IN and eukaryotes are one another’s closest relatives in rooted 47405. E-mail: [email protected] universal trees.4–6 This means that archaebacteria share a recent common ancestor with eukaryotes, so it makes BioEssays 20:87–95, ௠ 1998 John Wiley & Sons, Inc. BioEssays 20.1 87 Problems and paradigms TABLE 1. Some Common Names and Characteristics of Archezoan Groups Some common Group genera Mitochondria Peroxisomes Golgi Flagella Metamonads Giardia Not recognized Not recognized Not recognized Yes Hexamita Trepomonas Retortamonas Pyrsonympha Microsporidia Encephalitozoon Not recognized Not recognized Not recognized No Nosema Spraguea Vairimorpha Parabasalla Trichomonas Hydrogenosome? Not recognized Yes Yes Tritrichomonas Monocercomonas Trichonympha Archamoebae Entamoeba Not recognized Not recognized In some In some Pelomyxa Mastigamoeba Phreatamoeba perfect sense that many aspects of archaebacterial molecu- whereas those of archezoa and prokaryotes are 70S. Simi- lar biology also should be found to resemble their eukaryotic larly, eukaryotic rRNA molecules are for the most part 18S counterparts.7 Each of these shared similarities clarifies the and 28S in contrast to the smaller rRNAs found in prokary- prokaryote-eukaryote transition in a small way by showing otes and archezoa. that molecular traits previously considered ‘‘eukaryotic’’ actu- Almost immediately after the Archezoa was proposed, ally predate nucleated cells. However, these shared charac- evidence from molecular phylogeny was produced to sup- ters tie the archaebacteria to all eukaryotes. Unlike the port its validity. The small subunit rRNA genes from a cyanobacteria-to-alga hypothesis, no single group of eukary- microsporidian, a diplomonad (the most studied subdivision otes specifically resembles the archaebacteria. So what was of Metamonada), and a parabasalian were all published the nature of the first eukaryote? within a short space of time, and these three genes branched deeper in the rRNA tree than any previously known eukary- ARCHEZOA: ARCHETYPICAL EUKARYOTES otic sequence.10–12 Although the order of the three groups When the endosymbiotic theory became fashionable and the remains contentious in rRNA phylogeny, trees of other photosynthetic origin of eukaryotes less so, the absence of molecules involved in gene expression, such as EF-1a, EF-2, mitochondria in certain eukaryotic cells started to attract RNA polymerase subunits, isoleucyl-tRNA synthetase, and attention. If the mitochondrion, like the plastid, originated by an endosymbiotic event, then it was also possible that some large subunit rRNA, corroborated the deep branching posi- 6,13–16 amitochondrial eukaryotes diverged prior to this event. This tion of these organisms. was first suggested for the hypermastigotes, a group of This phylogenetic evidence fulfilled the most basic predic- Parabasalia,8 and was expanded and refined by Cavalier- tion of the Archezoa hypothesis for these groups: if they Smith in 1983.9 Cavalier-Smith proposed the Archezoa to predate the origin of the mitochondrion, then they must contain the descendants of ancient premitochondrial eukary- branch earlier than mitochondrion-containing eukaryotes in otes: the Metamonads, Parabasalia, Microsporidia, and a phylogenetic trees (see Fig. 1). However, this was the new group, the Archamoebae. Each of these groups com- high-water mark for the Archezoa. In recent years evidence prised anaerobic, amitochondrial cells that are morphologi- has emerged that several of these organisms contain a cally very simple. Not only do they lack mitochondria but also genetic residue of the mitochondrion, which means that they peroxisomes or microbodies, in most cases Golgi dictyo- could not have evolved before the endosymbiosis. The somes, and in some also flagella (see Table 1). What’s more, Archezoa is fast losing membership, and it now appears that the ribosomes of Metamonads, Parabasalia, and Microspo- the mitochondrial endosymbiosis may have taken place ridia also were known to be about the same size as those of before the evolution of any of the presently known eukaryotic prokaryotes. Eukaryotic ribosomes are typically 80S in size, lineages. 88 BioEssays 20.1 Problems and paradigms Figure 2. An archamoeba, Pelomyxa. quenced. In phylogenetic trees these also branch within the mitochondria-containing eukaryotes,19,20 so these too ap- pear to have arisen from mitochondria-containing ancestors. Furthermore, in the small subunit rRNA tree, Entamoeba and Phreatamoeba sometimes branch together,21 and some- times do not,19 raising doubts as to the validity of the Archamoebae as an evolutionary lineage, let alone a primi- Figure 1. The Archezoa as originally conceived. Mitochon- tively amitochondrial one. These phylogenetic arguments dria containing eukaryotes are purple, Archezoa are red, are not beyond reasonable doubt, however, because the Eubacteria are blue, and Archaebacteria are yellow. The Archamoebae often branch very near the origin of mitochon- symbiosis that led to the mitochondrion was proposed to have taken place after the divergence of at least four lineages dria, and other molecular trees disagree with rRNA on the 22 from other eukaryotes, the Metamonads, Microsporidia, Para- order of these deep branching taxa. basalia, and Archamoebae. The order that these four groups More substantial evidence came from a direct search of diverged was not clear, and all have since been argued to be the Entamoeba genome for molecular relics of the mitochon- the first. drial symbiont. Most of the many hundreds of mitochondrial protein-coding genes are encoded in the nucleus and targeted to the organelle after they are translated in the ARCHAMOEBAE: FIRST TROUBLE FOR cytoplasm. These genes were transferred from the symbiont ARCHEZOA genome to the nucleus but are recognizable today both Little can be said about the Archamoebae as a group because of this targeting and because the genes them- because they share almost no unifying characters other than selves closely resemble homologues from the type of bacte- the fact that they are all amitochondriate amoebae. Other- ria from which the mitochondrion evolved, the alpha- wise, they are a very diverse group inhabiting a wide variety proteobacteria.23 Finding such genes in the nucleus
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