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Euglenozoa) As Inferred from Hsp90 Gene Sequences

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Euglenozoa) As Inferred from Hsp90 Gene Sequences J. Eukaryot. Microbiol., 54(1), 2007 pp. 86–92 r 2006 The Author(s) Journal compilation r 2006 by the International Society of Protistologists DOI: 10.1111/j.1550-7408.2006.00233.x Phylogeny of Phagotrophic Euglenids (Euglenozoa) as Inferred from Hsp90 Gene Sequences SUSANA A. BREGLIA, CLAUDIO H. SLAMOVITS and BRIAN S. LEANDER Program in Evolutionary Biology, Departments of Botany and Zoology, Canadian Institute for Advanced Research, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 ABSTRACT. Molecular phylogenies of euglenids are usually based on ribosomal RNA genes that do not resolve the branching order among the deeper lineages. We addressed deep euglenid phylogeny using the cytosolic form of the heat-shock protein 90 gene (hsp90), which has already been employed with some success in other groups of euglenozoans and eukaryotes in general. Hsp90 sequences were generated from three taxa of euglenids representing different degrees of ultrastructural complexity, namely Petalomonas cantuscygni and wild isolates of Entosiphon sulcatum, and Peranema trichophorum. The hsp90 gene sequence of P. trichophorum contained three short introns (ranging from 27 to 31 bp), two of which had non-canonical borders GG-GG and GG-TG and two 10-bp inverted repeats, sug- gesting a structure similar to that of the non-canonical introns described in Euglena gracilis. Phylogenetic analyses confirmed a closer relationship between kinetoplastids and diplonemids than to euglenids, and supported previous views regarding the branching order among primarily bacteriovorous, primarily eukaryovorous, and photosynthetic euglenids. The position of P. cantuscygni within Eu- glenozoa, as well as the relative support for the nodes including it were strongly dependent on outgroup selection. The results were most consistent when the jakobid Reclinomonas americana was used as the outgroup. The most robust phylogenies place P. cantuscygni as the most basal branch within the euglenid clade. However, the presence of a kinetoplast-like mitochondrial inclusion in P. cantuscygni de- viates from the currently accepted apomorphy-based definition of the kinetoplastid clade and highlights the necessity of detailed studies addressing the molecular nature of the euglenid and diplonemid mitochondrial genome. Key Words. Entosiphon, Euglenida, Euglenozoa, heat-shock protein 90, introns, kDNA, kinetoplast, Peranema, Petalomonas, phylogeny. HE Euglenozoa constitute a monophyletic group of flagellates Diplonemids comprise a small group of mostly free-living pha- T that includes three major clades: euglenids, kinetoplastids, and gotrophs (Kivic and Walne 1984; Marande et al. 2005) and some diplonemids. Although, this monophyly has been confirmed by facultative parasites (Kent et al. 1987). There is no evidence of a studies using nuclear small subunit (SSU) recombinant DNA kDNA-like mitochondrial inclusion in diplonemids, but the struc- (rDNA) and protein sequences, the relationships between the three ture of its single mitochondrion has been shown to be unusual (e.g. major groups varies according to the methods and the markers highly branched, with few flattened cristae). The mtDNA is ar- employed (Simpson and Roger 2004; Talke and Preisfeld 2002). ranged in circular chromosomes of two slightly different sizes and The most compelling molecular phylogenetic data indicate that distributed in a pan-kDNA-like fashion (Marande et al. 2005; diplonemids and kinetoplastids are more closely related to each Maslov et al. 1999). other than to euglenids (Maslov, Yasuhira, and Simpson 1999; Euglenids form a very diverse group of free-living flagellates Moreira, Lo´pez-Garcı´a, and Vickerman 2004; Simpson, Lukeˇs, that inhabit a variety of aquatic environments. Members of this and Roger 2002; Simpson and Roger 2004; Simpson, Stevens, and group have very different modes of nutrition, such as osmotrophy, Lukeˇs 2006b; Simpson et al. 2004). Morphologically, these three phagotrophy, and phototrophy. The most distinctive structural groups share a distinctive flagellar apparatus in which the flagella, character of euglenids is a pellicle composed of proteinaceous inserting within an apical or subapical pocket, are reinforced by strips that run lengthwise over the cell (Leander and Farmer paraxonemal rods, a proteinaceous scaffolding adjacent to the 2001a). Some euglenids are completely rigid, whereas others are usual 912 axoneme (Marande, Lukeˇs, and Burger 2005; Simpson highly plastic. Cell plasticity depends on the number of pellicle 1997; Willey, Walne, and Kivic 1988). strips in the cell, and how they articulate with each other along the Kinetoplastids include both trypanosomatids (parasites) and lateral margins. Longitudinally arranged strips are usually asso- bodonids (either free living or parasites) and are apomorphically ciated with cells that cannot change their shape, whereas helically defined by a novel arrangement of mitochondrial DNA (mtDNA) arranged strips are associated with a type of peristaltic movement forming conspicuous inclusions called ‘‘kinetoplasts’’ (Lukeˇs called ‘‘euglenoid movement’’ (Leander and Farmer 2001b; et al. 2002). In the majority of kinetoplastids, the kinetoplast Leander, Witek, and Farmer 2001b; Suzaki and Williamson DNA (kDNA) is arranged in two kinds of circular molecules 1985, 1986a, b). The diversity of pellicle surface patterns pro- known as ‘‘maxicircles’’ and ‘‘minicircles.’’ Maxicircles are vides a significant amount of information useful for discriminat- present in a few dozen copies, and encode both mitochondrial ing among the euglenid lineages (Brosnan et al. 2003; Esson protein genes and some ‘‘guide rRNA’’ (gRNA) genes. Mini- and Leander 2006; Leander 2004; Leander and Farmer 2001a; circles are present in thousands of copies and encode gRNAs (Morris Leander et al. 2001b). et al. 2001). Transcripts of some protein-coding genes undergo Both morphology-based and molecular-based phylogenetic editing in which the addition or removal of uridine residues analyses suggest that rigid phagotrophs form the earliest diver- produce the final mRNA molecules (Lukeˇs, Hashimi, and Zı´kova´ ging branches within euglenids (Leander 2004; Leander, Triemer, 2005). Nonetheless, the general configuration of kDNA is vari- and Farmer 2001a). As such, an important taxon for reconstruct- able, and the main states described so far include pro-kDNA, ing early events in the evolutionary history of euglenozoans is the poly-kDNA, pan-kDNA, and mega-kDNA (see reviews by Lukeˇs phagotrophic euglenid Petalomonas cantuscygni (Busse, Patter- et al. 2002; Marande et al. 2005). son, and Preisfeld 2003; Leander et al. 2001a). Petalomonas cant- uscygni is usually considered the earliest branching euglenid because it possesses an unusual combination of ultrastructural Corresponding Author: B. Leander, Canadian Institute for Advanced characters, including a simple feeding apparatus, pellicle strips Research, Program in Evolutionary Biology, Departments of Botany (synapomorphic for euglenids), and a kDNA-like inclusion within and Zoology, University of British Columbia, Vancouver, BC, Canada each mitochondrion (Leander et al. 2001a). Unfortunately, the V6T 1Z4—Telephone number: 1604-822-2474; FAX number: 1604- SSU rDNA sequence from P. cantuscygni is highly divergent, 822-6089; e-mail: [email protected] which precludes resolution of its phylogenetic position within the 86 BREGLIA ET AL.—PHYLOGENY OF PHAGOTROPHIC EUGLENIDS 87 Resolving the branching order of P. cantuscygni and other phagotrophic euglenids is necessary to evaluate the hypotheses outlined above. However, they represent several distinctive and divergent lineages that cannot be satisfactorily resolved with SSU rDNA data (Busse and Preisfeld 2002, 2003; Busse et al. 2003; Simpson and Roger 2004). Comparison of nucleus-encoded pro- tein sequences, such as the heat-shock protein 90 (hsp90) gene, provides a viable alternative (Leander and Keeling 2003; Shal- chian-Tabrizi et al. 2006; Simpson and Roger 2004; Simpson et al. 2002, 2006a; Stechmann and Cavalier-Smith 2003). Among eu- glenids, hsp90 sequences are known only from the phototroph Euglena gracilis, precluding any attempt to analyze relationships within this group. With the aim of increasing the dataset of avail- able hsp90 sequences from euglenids and addressing our phylo- genetic hypotheses (Fig. 1), we sequenced the cytosolic hsp90 gene from three taxa, namely the phagotrophs Peranema tricho- phorum, Entosiphon sulcatum, and P. cantuscygni. Fig. 1. Hypothetical frameworks for inferring character evolution MATERIALS AND METHODS within the Euglenozoa, considering two different phylogenetic positions for Petalomonas: scenarios (A, B), P. cantuscygni is the sister lineage to Collection of organisms. Entosiphon sulcatum was isolated all other euglenids; scenarios (C, D), P. cantuscygni is the sister lineage to from sediment samples collected from a pond at the Queen Eliz- kinetoplastids. The putative synapomorphies for the Kinetoplastida and abeth Park, Vancouver, BC, in May 2004 (Fig. 2, 3). Cells were the Euglenida are ‘‘kinetoplasts’’ and ‘‘pellicle strips,’’ respectively. For manually isolated using drawn-out glass Pasteur micropipettes and each possible topology, two alternative scenarios for the evolutionary or- temporarily grown at 16 1C in an 802 Sonnerborn’s Paramecium igin and losses of pellicle strips and (kinetoplast-like) mitochondrial in- medium (rye grass Cerophyl of 250 mg/L with Klebsiella sp. as clusions are phylogenetically mapped. In scenarios
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