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Microsporidia Are Related to Fungi: Evidence from the Largest Subunit of RNA Polymerase II and Other Proteins

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Microsporidia Are Related to Fungi: Evidence from the Largest Subunit of RNA Polymerase II and Other Proteins Proc. Natl. Acad. Sci. USA Vol. 96, pp. 580–585, January 1999 Evolution Microsporidia are related to Fungi: Evidence from the largest subunit of RNA polymerase II and other proteins ROBERT P. HIRT*†,JOHN M. LOGSDON,JR.†‡,BRYAN HEALY*, MICHAEL W. DOREY‡,W.FORD DOOLITTLE‡, AND T. MARTIN EMBLEY*§ *Department of Zoology, The Natural History Museum, London SW7 5BD, United Kingdom; and ‡Canadian Institute for Advanced Research, Program in Evolutionary Biology and Department of Biochemistry, Halifax, NS, B3H 4H7, Canada Edited by Estella B. Leopold, University of Washington, Seattle, WA, and approved December 1, 1998 (received for review August 12, 1998) ABSTRACT We have determined complete gene se- Here we report sequences for the largest subunit of RNA quences encoding the largest subunit of the RNA polymerase polymerase II (RPB1) from two Microsporidia, Vairimorpha II (RBP1) from two Microsporidia, Vairimorpha necatrix and necatrix and Nosema locustae. Several phylogenetic methods Nosema locustae. Phylogenetic analyses of these and other applied to these and other RPB1 sequences strongly support a RPB1 sequences strongly support the notion that Microspo- close relationship of Microsporidia and Fungi. A reanalysis of ridia are not early-diverging eukaryotes but instead are the apparently conflicting EF data show that the support that specifically related to Fungi. Our reexamination of elongation these sequences lend to a deeply diverging Microsporidia is factors EF-1a and EF-2 sequence data that had previously weak and attributable to artifacts. Furthermore, the EF-1a been taken as support for an early (Archezoan) divergence of gene from the microsporidian Glugea plecoglossi (5) carries an these amitochondriate protists show such support to be weak insertion encoding 11 amino acids that is otherwise only found and likely caused by artifacts in phylogenetic analyses. These in, and is diagnostic for, the EF-1a genes of Fungi and Metazoa EF data sets are, in fact, not inconsistent with a Microsporidia (animals) (11), which form a clade based on other criteria (6, 11). 1 Fungi relationship. In addition, we show that none of these An alternative hypothesis to reconcile the apparently con- proteins strongly support a deep divergence of Parabasalia flicting gene trees and to allow Microsporidia to retain their and Metamonada, the other amitochondriate protist groups early status is that they might have borrowed genes from host currently thought to compose early branches. Thus, the phy- genomes (6). We conclude that such chimeric theories are not logenetic placement among eukaryotes for these protist taxa necessary because there is no significant conflict between is in need of further critical examination. these proteins concerning the position of Microsporidia. Where a convincing phylogenetic signal is present, it relates Microsporidia are highly specialized eukaryotic unicells, living them to Fungi. Numerous recent reports indicate that the Microsporidia, only as obligate intracellular parasites of other eukaryotes (1). Metamonada, and Parabasalia possess nuclear genes of a-pro- They lack the mitochondria and peroxisomes typical of most teobacterial provenance whose products normally (in mito- eukaryotes. Thus, in 1983 Cavalier-Smith (2) included the chondriate eukaryotes) serve mitochondrial functions; the Microsporidia with other amitochondriate protists, Parabasa- presence of such genes indicates mitochondrial loss from these lia (e.g., Trichomonas), Metamonada (e.g., Giardia), and Ar- protists (9, 10, 12–16). Although the ancestral presence of chamoebae (e.g., Entamoeba) in the kingdom Archezoa. These mitochondria does not itself preclude a deep divergence of any protists were presumed to have diverged from other eu- of these taxa, our analyses of RPB1 and reanalyses of EF data karyotes before the acquisition of mitochondria and were (in addition to challenging the deep placement of Microspo- suggested as the earliest eukaryotic lineages. ridia) show that the support for an early divergence for Phylogenetic trees based initially on small-subunit ribosomal Trichomonas and Giardia is also weaker than generally sup- RNA (SSUrRNA) (3) and then on protein translation elon- a posed. The inferred early branching positions of Metamonada gation factor (EF-1 and EF-2) (4, 5) sequences showed that and Parabasalia largely depend on a single data set, i.e., Microsporidia indeed diverged early, along with the Parabasa- SSUrRNA. The Microsporidia thus may be the only member lia and Metamonada. Thus, these data apparently confirmed of the (now former) Archezoa (sensu Cavalier-Smith, ref. 17) the archezoal hypothesis in general and what we call the about whose phylogenetic position we now have confidence ‘‘Microsporidia-early’’ hypothesis in particular—Archamoe- based on multiple molecular data sets. bae were eliminated from the Archezoa when their SSUrRNAs neither placed them together nor as early branches (6). However, more recent trees constructed from tubulin (7, 8) MATERIALS AND METHODS and Hsp70 data (9, 10) placed Microsporidia in the eukaryotic Isolation of Genomic Clones. Two sets of oligonucleotide ‘‘crown,’’ favoring a position within, or as the sister group to, primers—RPB1-F1 (cgGACTTYGAYGGNGAYGARATG- Fungi. Although the support for the ‘‘Microsporidia 1 Fungi’’ hypothesis (or M 1 F) from the Hsp70 data is not compelling This paper was submitted directly (Track II) to the Proceedings office. [when judged by maximum-likelihood (ML) difference tests or Abbreviations: BP, bootstrap proportions; CSR, constant-site re- other support values] (9, 10), support from a-tubulin is firm moval; ISR, invariant-site removal; CTD, C-terminal domain; EF, (7). If Microsporidia are truly related to Fungi, then their elongation factor (protein translation); LBP, local bootstrap propor- simplified cell structures and small genomes are degenerate tions; ML, maximum likelihood; MP, maximum parsimony; RPB1, RNA polymerase II largest subunit; SSUrRNA, small subunit ribo- features permitted, or perhaps encouraged, by their parasitic somal RNA; M 1 F, Microsporidia 1 Fungi; FSR, fast-site removal. lifestyles. Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AF060234 and The publication costs of this article were defrayed in part by page charge AF061288). †R.P.H. and J.M.L. contributed equally to this work. payment. This article must therefore be hereby marked ‘‘advertisement’’ in §To whom reprint requests should be addressed at: Department of accordance with 18 U.S.C. §1734 solely to indicate this fact. Zoology, Natural History Museum, Cromwell Road, London SW7 PNAS is available online at www.pnas.org. 5BD, United Kingdom. e-mail: [email protected]. 580 Downloaded by guest on September 24, 2021 Evolution: Hirt et al. Proc. Natl. Acad. Sci. USA 96 (1999) 581 A)yR1 (CCCGCKNCCNCCCATNGCRTGRAA) (codons 5 expected if these sequences diverged a long time ago (30–33). capital letters) and RPB1-F2 (cgcgATHGASYACIGCNGT- All of the data sets we investigated contained sites that are NAARAC)yR2 (ccggGTCATYTGNGTNGCNGGYTC) am- constant in all taxa in the alignment and thus potentially plified '1.1-kbp and 1.2-kbp fragments of RPB1 from V. invariant. ML models in PROTML have no site-by-site rate necatrix genomic DNA (9). Amplicons were used as probes in correction and so may be susceptible to this source of error. We Southern blots to confirm the source of the single-copy V. therefore investigated the effect of reducing site rate hetero- necatrix RPB1 gene and to screen a V. necatrix EcoRI genomic geneity for PROTML analyses by editing the data to remove the library (9). Two EcoRI fragments were cloned to obtain the category of fastest evolving sites (fast-site removal, FSR) or a full-length RPB1 gene that was sequenced on both strands by fraction of inferred invariant sites (invariant-site removal, ISR; primer walking. ref. 30) before phylogenetic analysis. The fraction of invariant Oligonucleotide primers RPB1-F4 (CTACGTGGCAAGY- sites was estimated by using a two-site rate (either variable or TNATGGG)yRPB1-R3 (AGACCTTCACGNCCNWCCAT) invariant) ML model with the JTT-F substitution matrix in were used to amplify a '1,500-bp fragment of RPB1 from N. PUZZLE Version 4.0. For FSR we used PUZZLE Version 4.0 to locustae genomic DNA. Nested amplification with primers estimate a discrete g distribution for each data set (comprising RPB1 F3 (GCATTCGATGGCGAYGARATG)yRPB1-R3 one invariant-site rate and eight variable-site rates) under the resulted in a '1-kbp fragment. This was used as a probe to JTT-F model. Because tree topology can affect these calcu- isolate clones from a N. locustae SauIIIA partial-digest lations, the rates for the RPB1 data set were calculated over genomic library (18). One clone containing the entire RPB1 two MP trees (themselves constrained to represent either the gene was completely sequenced on both strands. M 1 F or the Microsporidia-early hypothesis). Sites in the Sequence Alignments. The inferred amino acid sequences of fastest rate category common to both trees were excluded from the two microsporidian RPB1 sequences were aligned to the PROTML phylogenetic analyses. Rate categories for the published RPB1, RPA1 (RNA polymerase I largest subunit), EF-1a and EF-2 protein data sets were calculated by using and RPC1 (RNA polymerase III largest subunit) sequences, by published ML trees (which placed Microsporidia early) (4, 5). using CLUSTALW Version 1.7 (19) with further manual adjust- Analysis of
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