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Early Branching Eukaryotes? T Martin Embley* and Robert P Hirt

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Early Branching Eukaryotes? T Martin Embley* and Robert P Hirt 624 Early branching eukaryotes? T Martin Embley* and Robert P Hirt Recent phylogenetic analyses suggest that Giardia, Trichomonas Table 1 and Microsporidia contain genes of mitochondrial origin and are List of nuclear encoded genes found in Giardia, Trichomonas thus unlikely to be primitively amitochondriate as previously and Microsporidia that probably originated from the thought. Furthermore, phylogenetic analyses of multiple data sets endosymbiont that gave rise to mitochondria. suggest that Microsporidia are related to Fungi rather than being deep branching as depicted in trees based upon SSUrRNA Trichomonas Giardia Microsporidia analyses. There is also room for doubt, on the basis of a lack of vaginalis lamblia consistent support from analyses of other genes, whether Giardia Hsp10 + [9] ? ? or Trichomonas branch before other eukaryotes. So, at present, cpn 60 + [8–10] + [17••]? we cannot be sure which eukaryotes are descendants of the •• •• earliest-branching organisms in the eukaryote tree. Future mHsp70 + [9,11] ? + [14 –16 ] resolution of the order of emergence of eukaryotes will depend Valyl-tRNA + [18••] + [18••]? upon a more critical phylogenetic analysis of new and existing synthetase data than hitherto. Hypotheses of branching order should Triose-phosphate ? P [13] ? preferably be based upon congruence between independent isomerase data sets, rather than on single gene trees. Adenylate + [12] – [12] ? kinase Addresses +, mitochondrial homologue detected; –, no mitochondrial Department of Zoology, The Natural History Museum, Cromwell Road, homologue detected; P, likely α−proteobacterial origin (i.e. London SW7 5BD, UK consistent with a mitochondrial origin); ?, no published data. *e-mail: [email protected] mHsp70, mitochondrial Hsp 70. Correspondence: T Martin Embley Current Opinion in Genetics & Development 1998, 8:624–629 primitively amitochondriate condition [2,4•]. The Archezoa http://biomednet.com/elecref/0959437X00800624 hypothesis was apparently supported for these taxa at least, when phylogenetic trees based upon small subunit ribosomal © Current Biology Ltd ISSN 0959-437X RNA [5] and translation elongation factors EF-1α and EF-2 [6], showed Giardia, Trichomonas and Microsporidia Introduction branching before eukaryotes which contain mitochondria Establishing a phylogeny for eukaryotes is central to our (see Figure 1a). The Archezoa hypothesis stimulated wide- attempts to understand contemporary eukaryote diversity: spread interest in Giardia, Trichomonas and Microsporidia for example, patterns of character change can be mapped because their biology was expected to reveal stages in the over a phylogeny to fuel hypotheses of common ancestral acquisition of eukaryote cellular features; however, recent states prior to lineage splitting. Hypotheses of character data now suggest that Giardia, Microsporidia and Trichomonas evolution can be made without recourse to phylogenetic contain genes which are most likely of mitochondrial origin. analysis but phylogenies help to identify independent evo- lutionary events and to distinguish cause from effect in Mitochondrial genes in early comparative analysis [1]. If, through phylogenetic analysis, branching eukaryotes we were able to identify descendants of the first eukaryot- It is accepted that mitochondrial genes were transferred to ic branches, it might even be possible to infer something the host nucleus during the evolution of the symbiosis about the early stages of eukaryote evolution. As such, because phylogenetic analysis of host nuclear genes betrays there has been considerable effort spent in trying to identi- their mitochondrial origin (e.g. [7]). Genes for which phylo- fy early branching eukaryotes and the purpose of this genetic analysis indicates (or is consistent with) a review is to discuss prevailing ideas pertaining to this topic. mitochondrial origin have now been reported in Giardia, Trichomonas and Microsporidia (Table 1). They include The Archezoa hypothesis for early adenylate kinase, 10, 60 and 70 kDa heat shock proteins branching eukaryotes (Hsp10, cpn60, Hsp70), triose phosphate isomerase and In the premolecular era, the absence of functional mitochon- valyl tRNA-synthetase [8–13,14••–18••]. dria in protists such as Giardia, Trichomonas and Microsporidia was interpreted [2] as resulting from their early Alternative explanations, other than one-time possession of separation from other eukaryotes (i.e. prior to the mitochon- mitochondria, have been proposed to account for the pres- drion symbiosis) which is thought to have occurred once [3]. ence of these genes in Giardia, Trichomonas or Microsporidia The hypothesis that Giardia, Trichomonas and Microsporidia [19•,20•] but these seem unnecessary to explain the strong- were relicts of a pre-mitochondrial phase of eukaryote evolu- ly supported positions of cpn60s and/or Hsp70s within tion was formalised by calling them ‘Archezoa’ to denote a clades otherwise defined by mitochondrial homologues and Early branching eukaryotes? Embley and Hirt 625 Figure 1 (a)'Crown' taxa (b) Animals Animals Fungi H H Fungi i Choanozoa Microsporidia Acquisition of Plants/green algae Choanozoa ii mitochondria? Alveolates H Dictyostelium Origin of Stramenopiles ? Physarum Acquisition of eukaryotes? mitochondria? Rhodophytes Entamoebae iii iv Dictyostelium Plants/green algae v Origin of vi Entamoebae Rhodophytes eukaryotes? Euglenozoa ? Stramenopiles (2) Physarum H Alveolates Percolozoa H H Percolozoa (1) Microsporidia Euglenozoa vii Trichomonas H H Trichomonas Giardia Giardia Unidentified early branching eukaryote? Archaea Archaea Unidentified early branching primitively Putative [pre-1996 in (a)] primitively amitochondriate taxa amitochondriate Secondary loss of functional mitochondria in some or all taxa eukaryote? Highlighted taxa are those branching before the 'Crown' (boxed) in most published SSUrRNA trees H Hydrogenosomes in some or all taxa Current Opinion in Genetics & Development Alternative phylogenetic hypotheses for eukaryotes. (a) Relationships radiation. Alternative hypotheses for the origin of the eukaryotic cell among eukaryotes as interpreted on a schematic SSUrDNA tree relative to the acquisition of mitochondria are indicated in (b): (1) The suggest the acquisition of mitochondria after the divergence of eukaryotic cell originated before the acquisition of the mitochondrion Giardia, Trichomonas and Microsporidia (all Archezoa sensu [2]) endosymbiont, thus there may be primitively amitochondriate whose relative order of branching at the base of eukaryotes is eukaryotes remaining to be discovered. (2) The Hydrogen hypothesis uncertain. The placement of Archaea as the sister-group to eukaryotes [43••] posits that eukaryotes originated through symbiotic association is discussed in the text. (b) Composite phylogeny (i.e. no single gene between an Archaea (nominally the ‘host’) and the proteobacterium tree supports all branches) depicting some alternative hypotheses for (the ‘symbiont’) which subsequently gave rise to mitochondria and eukaryote relationships. The diagram was constructed by considering hydrogenosomes. In this sense the pre-‘mitochondrial’ branches in published trees from different protein datasets and some of these ‘host’ trees will be Archaea. The documented distribution of relationships are more speculative than others. All relationships should hydrogenosomes among eukaryotes [51•] is shown on both trees, as be viewed simply as more or less well-founded hypotheses which can are hypotheses of primitive or secondary absence of functional be supported or refuted through more data and further analyses. The mitochondria. The possibility that Stramenopiles may lack functional data considered to support particular hypotheses are: branch i, (see mitochondria while retaining the organelle is discussed in [52]. Note Table 2); ii, EF-1α [50], actin [5] and β-tubulin (e.g. [35•]); iii–vii, actin that the perceived distribution of hydrogenosomes may well be and β-tubulin (e.g. [5,35•]) and valyl-tRNA synthetase [18••] (and see conservative as anaerobic habitats are in general poorly described for Table 2). Branch lengths are meaningless in both diagrams and the eukaryotes they contain or for the organelles that such eukaryotes polytomies indicate lack of resolution not support for explosive may posses [38]. they are not founded upon phylogenetic analyses which hypothesis that a eukaryote may lose its mitochondria but support alternative origins for these or other genes (Table 1). still retain mitochondrial genes is now supported by recent We interpret the presence of genes in Archezoa which clus- phylogenetic analyses indicating a relationship between ter with mitochondrial orthologues, as support for the Microsporidia and Fungi (see below). hypothesis that Giardia and Microsporidia once had mito- chondria, and for the hypothesis that Trichomonas has Alternative phylogenetic relationships for early converted its mitochondria to hydrogenosomes [21,22]. branching eukaryotes The finding of mitochondrial genes in Giardia, Trichomonas Phylogenetic analyses of hydrogenosome-containing cili- and Microsporidia does not preclude these taxa from ates [23] and hydrogenosome-containing fungi [24] branching early in eukaryote evolution but there are alter- suggest that they are derived from aerobic ancestors with native, and in some cases now better supported, hypotheses mitochondria. For ciliates, fungi and Trichomonas, there is of relationships for these taxa. The deep position of also other data consistent
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