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Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, 3529-6270 University Boulevard, Vancouver, BC, Canada V6T 1Z4
Correspondence
Patrick J. Keeling
pkeeling{at}interchange.ubc.ca
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the sequences reported in this paper are AY729814–AY729874 and AY739894–AY739895.
Individual ProML phylogenies (Figs A–E) are available as supplementary material in IJSEM Online.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Indeed, plastids illustrate this need especially well, since much of what is known about algal relationships is based on plastid-encoded genes or genes for plastid-targeted proteins (Fast et al., 2001; Harper & Keeling, 2003; Yoon et al., 2002b), which can evolve independently of the host. This does not invalidate such inferences, but it is desirable to buttress these conclusions with supporting data from host lineages.
The first large-scale molecular phylogenies of eukaryotes, based on small-subunit rRNA (SSU rRNA), consisted of a basal ladder of protists followed by an explosive ‘crown’ of other eukaryotes – animals, fungi and plants (Cavalier-Smith & Chao, 1996; Kumar & Rzhetsky, 1996; Sogin & Silberman, 1998; Van de Peer & De Wachter, 1997). The first protein-coding gene phylogenies gave similar results (Brown & Doolittle, 1995; Hashimoto et al., 1994; Kamaishi et al., 1996), but also contained important incongruencies and over time, these contradictions have added up to serious questions about the ‘shape’ of the eukaryotic tree. Comparative phylogenetics based on several well-sampled protein-coding genes has shown that the overall ladder–crown structure of the tree is not a true representation of eukaryotic evolution. Nearly all of the statistically well-supported ‘deep-branching’ eukaryotes are now known to be artifacts of heterogeneous evolutionary rates or long-branch attraction (Embley & Hirt, 1998; Gribaldo & Philippe, 2002; Hirt et al., 1999; Morin, 2000; Philippe, 2000; Van de Peer et al., 2000b). All individual gene phylogenies seem to contain a few misleading branches and problematic taxa, but fortunately different trees seem to have different problems. Thus, reconstructing a global eukaryotic tree seems to remain within reach.
A new hypothesis is emerging based on several different kinds of mutually reinforcing data from many different genes. These data can take the following forms: a single phylogeny based on multiple concatenated genes (Bapteste et al., 2002; Yoon et al., 2002b); several individual phylogenies that all converge on the same relationship (Fast et al., 2002; Simpson et al., 2002b); non-phylogenetic molecular evidence such as insertions, deletions, gene duplications or gene fusions (Archibald et al., 2002; Baldauf & Palmer, 1993; Keeling & Palmer, 2001; Stechmann & Cavalier-Smith, 2002); and/or non-molecular data such as ultrastructure (Simpson et al., 2002a). The hypothesis emerging from this approach is that there are five major divisions or ‘supergroups' of eukaryotes representing most or perhaps even all eukaryotic diversity (Keeling, 2004). Many of these do not have formal taxonomic names that are universally accepted, so for simplicity they can be informally referred to as the rhizaria, chromalveolates, excavates, unikonts and plants.
The chromalveolate supergroup represents a large fraction of known eukaryotic diversity, ranging from tiny microbial parasites to kelps as long as 50 m. In fact, chromalveolates account for about half of the recognized species of protists and algae (Cavalier-Smith, 2004). The chromalveolates comprise six subgroups, each of which is a large and diverse group in its own right. The alveolates contain the apicomplexans, ciliates and dinoflagellates, whereas the chromists are made up of the cryptomonads, haptophytes and heterokonts (also called stramenopiles). Various permutations including some, but not all, of these lineages have been put forward in the past (e.g. Chadefaud, 1950; Christensen, 1989), but these were largely restricted to photosynthetic members and included some groups (e.g. euglenids) that are now known to be very distantly related to other putative chromalveolates. Moreover, the current chromalveolate hypothesis is based on a very specific model of plastid evolution. Cryptomonads, haptophytes, heterokonts and dinoflagellates all have members that contain plastids derived from secondary endosymbiosis with a red alga, whereas apicomplexans contain a cryptic plastid of putative red algal origin (Blanchard & Hicks, 1999; Fast et al., 2001; Funes et al., 2002; Köhler et al., 1997; McFadden & Waller, 1997; Williamson et al., 1994; Zhang et al., 2000). Based on this, it was proposed that these plastids originated from a single endosymbiotic event in their common ancestor (Cavalier-Smith, 1999).
A single endosymbiotic event also leads to the prediction that both the host lineages and their plastids share a common evolutionary history. The only molecular evidence, in addition to other kinds of evidence, supporting this supergroup comes from plastid-targeted and plastid-encoded proteins. In the first instance, plastid-targeted GAPDH has been shown to be the product of a rare gene duplication of the cytosolic homologue, which has replaced the ancestral, cyanobacterial form (Fast et al., 2001; Harper & Keeling, 2003). This replacement is a strong marker for a common origin of chromalveolate plastids. From the plastid genome itself, a phylogeny based on five concatenated genes supports the union of cryptomonads, haptophytes and heterokonts (Yoon et al., 2002a). Given that plastids can move between lineages, however, these conclusions will be significantly stronger if the host lineages can also be demonstrated to be related. Molecular data have confirmed the alveolates as a group (Fast et al., 2002; Van de Peer et al., 2000a; Van de Peer & De Wachter, 1997) and there are data from a four-gene concatenated set indicating that ciliates, apicomplexans and heterokonts form a group (Baldauf et al., 2000). However, no large-scale analysis of nuclear-cytoplasmic genes has included all major chromalveolate lineages and, moreover, none has included representation from the remaining four supergroups, which is desirable to make certain than none of these are positioned between members of the supergroup being tested.
Here, the monophyly of the chromalveolates has been examined within the context of a global phylogeny of eukaryotes using six nucleus-encoded genes for cytoplasmic proteins: actin, alpha-tubulin, beta-tubulin, elongation factor-1 alpha (EF-1 alpha), heat-shock protein 70 (HSP70) and heat-shock protein 90 (HSP90). Homologues of these genes were characterized from a variety of chromalveolates so that each gene was known from at least one representative of all six chromalveolate subgroups. In addition, genes from representatives of two other supergroups (rhizarians and excavates) have also been characterized since molecular data from these groups are sparse. Consequently, this is the first analysis that includes multiple gene data from all five supergroups.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The heterokont Spumella uniguttata was the prey organism for a culture of the apicomplexan Colpodella edax isolated from a freshwater pond near Borok (Yaroslavskaja, Russian Federation). Genes were obtained from Spumella uniguttata in several attempts to sequence the Colpodella edax homologues (Kuvardina et al., 2002).
Genomic DNAs (gDNAs) from the oomycete heterokonts Apodachlya brachynema CBS 557.69, Brevilegnia macrospora CBS 132.37, Phytophthora palmivora CBS 236.30, Plectospira myriandra CBS 523.87, Pythium graminicola CBS 327.62 and Thraustotheca clavata CBS 343.33 were kindly donated by A. W. DeCock (Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands) and gDNA from the raphidophyte heterokont Heterosigma akashiwo was kindly donated by K. Ishida (Department of Biology, Kanazawa University, Kanazawa, Japan).
Algal cultures were harvested by centrifugation and cell pellets were lysed by grinding in a Knotes Duall 20 tissue homogenizer. gDNAs were extracted using the DNeasy Plant Mini kit (Qiagen) and total RNA was isolated using Trizol reagent (Invitrogen).
Characterization of new gene and cDNA sequences.
PCR amplification was carried out using the following primers: actin, GGCCTGGAARCAYTTNCGRTGNAC and GAGAAGATGACNCARATH or TGGGAYGAYATGGARAARATHTGG; alpha-tubulin, CGCGGCCTCARGTNGGNAAYGCNTGYTGGGA and CGCGCCATNCCYTCNCCNACRTACCA; beta-tubulin, GCCTGCAGGNCARTGYGGNAAYCA and TCCTCGAGTRAAYTCCATYTCRTCCAT; EF-1 alpha, AACATCGTCGTGATHGGNCAYGTNGA and CTTGATCACNCCNACNGCNACNGT; HSP70, AAGATCATCGGNATHGAYYTN and CTGAACGATNCCRTTNGCATC; and HSP90, ACGTTYTAYWSNAAYAARGARAT and CGCCTTCATMATNCSYTCCATRTTNGC. PCR products were gel-purified and then cloned into the TOPO-TA vector pCR2.1 (Invitrogen) and multiple clones of each were sequenced on both strands with ABI BigDye terminator chemistry (Applied Biosystems).
HSP90 and HSP70 cDNAs from the host and endosymbiont of the chlorarachniophyte Bigelowiella natans CCMP 621 were obtained from an ongoing EST (expressed sequence tag) project and each was fully sequenced. HSP70 cDNA was identified in ongoing EST projects from Isochrysis galbana and was fully sequenced. HSP70 from the oxymonad Streblomastix strix was amplified using primers AAGATCATCGGNATHGAYYTNGGNACNAC and CTGAACGATNCRTTNGCRTCDATRTCRAA from DNA isolated from enriched hindgut material of the Pacific dampwood termite (Zootermopsis angusticolis) as described previously (Keeling & Leander, 2003).
Molecular phylogeny.
Newly determined sequences were added to existing amino acid alignments. A total of eight alignments was subjected to phylogenetic analyses. Six of these were the respective alignments for the six protein-coding genes. The two remaining alignments were concatenations of different genes. One was a concatenation of actin, alpha-tubulin, beta-tubulin and HSP90 (AABH), whereas the second was a concatenation of all six genes (AABHHE). The resulting dimensions (number of taxaxnumber of amino acid positions) for all eight alignments were as follows: actin, 78x245; alpha-tubulin, 71x391; beta-tubulin, 73x380; EF-1 alpha, 48x422; HSP70, 45x505; HSP90, 61x516; AABH, 50x1554; and AABHHE, 50x2481. The amino acid alignments are available from the authors on request.
Distance analyses were performed on the individual datasets and the four-gene concatenated dataset only (AABH). Parsimony and maximum-likelihood (ML) analyses were performed on all datasets. For the six individual datasets and the four-gene concatenated dataset, ML distances were calculated using TREE-PUZZLE 5.0 (Strimmer & von Haeseler, 1996), using the WAG substitution matrix with the frequency of amino acid usage calculated from the data. Rate-across-site variation was modelled on a discrete gamma distribution with eight rate categories, estimating invariable sites and the shape parameter alpha from the data. Distance trees were constructed with weighted neighbour-joining using WEIGHBOR 1.0.1a (Bruno et al., 2000) and Fitch–Margoliash using FITCH 3.6a (Felsenstein, 1993). Fitch–Margoliash trees were inferred using the global rearrangements option and 10 input-order jumbles. Weighted neighbour-joining and Fitch–Margoliash bootstrap trees were constructed (without global rearrangements and implementing two input-order jumbles in Fitch–Margoliash) from 100 resampled datasets with gamma-corrected distances (with the rate category parameters above) using PUZZLEBOOT 1.0.3 (by M. Holder and A. Roger; http://www.tree-puzzle.de).
Protein ML analyses were performed using ProML 3.6a (Felsenstein, 1993) and PhyML (Guindon & Gascuel, 2003). ProML was performed with amino acid frequencies estimated from the data and rate-across-site variation was modelled on a gamma curve using the -r option with eight variable rate categories and an invariable sites category (rates and frequencies estimated by TREE-PUZZLE). Trees were searched with global rearrangements and a randomized input order of sequences with two jumbles. ProML bootstrap trees were constructed as above, but with no site-to-site rate variation and a single randomized input order. PhyML was performed using an input tree generated by BIONJ, the JTT model of amino acid substitution, the proportion of variable rates estimated from the data and nine categories of substitution rates (eight variable and one variable; parameters estimated by TREE-PUZZLE). PhyML bootstrap trees were constructed using the same parameters as the individual ML trees.
Parsimony analysis was completed using PAUP 4.0b10 (50 random sequence additions; gaps treated as missing data) using a heuristic search with steepest descent and tree bisection-reconnection branch swapping (Swofford, 2002). Parsimony bootstraps were completed (100 replicates) using 10 random sequence additions.
Distance analyses were not performed on the six-gene concatenated dataset due to missing data for a number of taxa (see Table 1). Parsimony, ML and the respective bootstrap analyses were performed on this dataset as described above for the other gene analyses.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). A table of GenBank/EMBL/DDBJ accession numbers for all taxa included in our various phylogenetic analyses is available as supplementary material in IJSEM Online. The overall aim was for all six major subgroups of chromalveolate and all five hypothesized supergroups to be represented in all six datasets and for representation to be sufficiently similar to allow genes to be concatenated. In addition, missing genes or cDNAs were also characterized from the excavate (oxymonad) Streblomastix strix and the rhizarian (the chlorarachniophyte cercozoan) Bigelowiella natans. No multiple gene phylogeny of eukaryotes has yet included a rhizarian (e.g. a cercozoan), which is an important omission when testing the monophyly of any one of the other supergroups.
Individual gene phylogenies
Of the six genes analysed here, the phylogeny of HSP90 (Fig. 1) has been investigated the least, but has shown promise. The phylogeny of alveolates has recently been examined with an expanded HSP90 dataset (Leander & Keeling, 2004). Moderate support was found for grouping alveolates and heterokonts, a result that has received varying levels of support from other molecular investigations (Baldauf et al., 2000; Ben Ali et al., 2001; Dacks et al., 2002; Stechmann & Cavalier-Smith, 2003; Van de Peer & De Wachter, 1997). Sequence data for cryptomonads, haptophytes or a diverse sample of heterokonts, however, has been lacking from these analyses. With the addition of these data, our HSP90 phylogeny shows a weak relationship between the strongly supported alveolate and heterokont clades. Interestingly, the strongly supported cryptomonad and haptophyte clades branch together with intermediate to weak support. The positions of both these larger groups, however, remain equivocal.
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; Baldauf et al., 2000; Bhattacharya & Weber, 1997; Hashimoto et al., 1995; Keeling, 2001; Keeling & Doolittle, 1996; Leander & Keeling, 2004; Saldarriaga et al., 2003) and the general characteristics of our phylogenies are similar to those given in these published reports. Bootstrap supports from these analyses are summarized in Table 2 [phylogenies (Figs A–E) are available as supplementary material in IJSEM Online]. Overall, the monophyly of each of the chromist lineages was recovered and strongly supported. As a group, the chromists were not recovered by any of the analyses of the six genes. Alveolates were resolved as monophyletic in actin, with the previously noted exception of ciliates (Keeling, 2001), and HSP70 phylogenies, but not with any appreciable bootstrap support. Not surprisingly, a chromalveolate clade was never recovered, but topologically, alveolates were positioned as a sister clade to the heterokonts in analyses of actin, EF-1 alpha, HSP70 and HSP90. For comparison, the support for four other more widely accepted groupings is also shown in Table 2 (green algae+streptophytes, animals+fungi, euglenozoans+heteroloboseans and diplomonads+parabasalia). Most of these groups are not overwhelmingly supported by individual phylogenies either and instead are supported erratically by different genes.
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). Accordingly, datasets of four- and six-gene concatenations were analysed to compare with the results of the individual phylogenies (see Table 1 for a complete list of taxa used in these concatenations). A four-gene concatenation consisting of actin, alpha-tubulin, beta-tubulin and HSP90 (AABH) was possible for 50 taxa representing the six subgroups of chromalveolates and the five eukaryotic supergroups. In many respects, the phylogeny inferred from these data (Fig. 2) is similar to that recovered for HSP90. There were, however, some notable differences (e.g. the monophyly of the discicristates: euglenozoans+heteroloboseans) and bootstrap support for most nodes was significantly higher (Table 2). Support for the various groupings of chromalveolate taxa was also similar to the results of HSP90 analyses. Alveolates and heterokonts were grouped with moderate support, whereas a cryptomonad and haptophyte clade received weak support, a topology also recovered by Stechmann & Cavalier-Smith (2003). The individual chromalveolate groups all received strong support, with the exception of the cryptomonads, which were represented by a single set of concatenated genes.
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) with topology that was essentially identical to that recovered by analysis of the four-gene dataset (Fig. 2). Bootstrap support was also virtually identical to the four-gene tree with the following qualitative differences: a slight decrease in support for monophyly of the alveolates, a slight increase in support for an alveolate/heterokont clade and increased support for monophyly of the opisthokonts (animals+fungi).
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). Indeed, molecular investigations based on plastid-encoded genes and plastid-targeted proteins have provided overlapping results that strongly support this hypothesis (Fast et al., 2001; Harper & Keeling, 2003; Yoon et al., 2002b). There is now growing support from individual and multiple gene phylogenies based on nucleus-encoded cytosolic proteins for the monophyly of an alveolate/heterokont clade. Moreover, the weak relationship observed between cryptomonads and haptophytes (never seen in nuclear gene trees before) is also consistent with the chromalveolate hypothesis. Considering these data within the context of the original cellular characteristics that prompted the recognition of the chromalveolates suggests that these groups are all related and that, by extension, their plastids probably originated via a single secondary endosymbiotic event. Though there is presently no evidence from the phylogeny or cell biology of chromalveolates to suggest that they are not a monophyletic assemblage, it is also clear that more evidence from the nuclear-host lineage is necessary.
In general, uniting distant relatives (for, if the chromalveolates are a monophyletic group, they are an ancient group and distantly related) is a difficult problem that requires considerably more data than are currently available. A global phylogeny of eukaryotes based on nuclear-cytosolic proteins has been examined with four genes and 61 taxa (Baldauf et al., 2000), providing reasonable resolution. However, adding more taxa (six lineages that had not been previously represented were analysed here – cercozoans, cryptomonads, dinoflagellates, oxymonads, Entamoeba and haptophytes) has undermined overall support for the tree considerably. Other multiple gene analyses of eukaryotic phylogeny (e.g. Bapteste et al., 2002) have used many more genes (100) but fewer taxa (30) and were addressing important, but relatively narrow questions. A global phylogeny representing even an approximation of eukaryotic diversity remains to be achieved and will likely require a mixture of these approaches when more taxa have been sampled sufficiently to include a number of additional genes for analysis.
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ACKNOWLEDGEMENTS |
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