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Phylogenetic Position of Multicilia Marina and the Evolution of Amoebozoa

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Phylogenetic Position of Multicilia Marina and the Evolution of Amoebozoa Article Phylogenetic position of Multicilia marina and the evolution of Amoebozoa NIKOLAEV, Sergey Igorievich, et al. Abstract Recent molecular phylogenetic studies have led to the erection of the phylum Amoebozoa, uniting naked and testate lobose amoebae, the mycetozoan slime moulds and amitochondriate amoeboid protists (Archamoebae). Molecular data together with ultrastructural evidence have suggested a close relationship between Mycetozoa and Archamoebae, classified together in the Conosea, which was named after the cone of microtubules that, when present, is characteristic of their kinetids. However, the relationships of conoseans to other amoebozoans remain unclear. Here, we obtained the complete small-subunit (SSU) rRNA gene sequence (2746 bp) of the enigmatic, multiflagellated protist Multicilia marina, which has formerly been classified either in a distinct phylum, Multiflagellata, or among lobose amoebae. Our study clearly shows that Multicilia marina belongs to the Amoebozoa. Phylogenetic analyses including 60 amoebozoan SSU rRNA gene sequences revealed that Multicilia marina branches at the base of the Conosea, together with another flagellated amoebozoan, Phalansterium solitarium, as well as with Gephyramoeba sp., Filamoeba nolandi [...] Reference NIKOLAEV, Sergey Igorievich, et al. Phylogenetic position of Multicilia marina and the evolution of Amoebozoa. International Journal of Systematic and Evolutionary Microbiology, 2006, vol. 56, no. 6, p. 1449-1458 DOI : 10.1099/ijs.0.63763-0 Available at: http://archive-ouverte.unige.ch/unige:121594 Disclaimer: layout of this document may differ from the published version. 1 / 1 International Journal of Systematic and Evolutionary Microbiology (2006), 56, 1449–1458 DOI 10.1099/ijs.0.63763-0 Phylogenetic position of Multicilia marina and the evolution of Amoebozoa Sergey I. Nikolaev,1,231 Ce´dric Berney,241 Nikolai B. Petrov,1 Alexandre P. Mylnikov,3 Jose´ F. Fahrni2 and Jan Pawlowski2 Correspondence 1Department of Evolutionary Biochemistry, A. N. Belozersky Institute of Physico-Chemical Sergey Nikolaev Biology, Moscow State University, Moscow, Russia Sergey.Nikolaev@medecine. 2Department of Zoology and Animal Biology, University of Geneva, Geneva, Switzerland unige.ch 3Institute of Biology of Inland Waters, Russian Academy of Sciences, Yaroslavskaya obl., Borok, Ce´dric Berney Russia [email protected] Recent molecular phylogenetic studies have led to the erection of the phylum Amoebozoa, uniting naked and testate lobose amoebae, the mycetozoan slime moulds and amitochondriate amoeboid protists (Archamoebae). Molecular data together with ultrastructural evidence have suggested a close relationship between Mycetozoa and Archamoebae, classified together in the Conosea, which was named after the cone of microtubules that, when present, is characteristic of their kinetids. However, the relationships of conoseans to other amoebozoans remain unclear. Here, we obtained the complete small-subunit (SSU) rRNA gene sequence (2746 bp) of the enigmatic, multiflagellated protist Multicilia marina, which has formerly been classified either in a distinct phylum, Multiflagellata, or among lobose amoebae. Our study clearly shows that Multicilia marina belongs to the Amoebozoa. Phylogenetic analyses including 60 amoebozoan SSU rRNA gene sequences revealed that Multicilia marina branches at the base of the Conosea, together with another flagellated amoebozoan, Phalansterium solitarium, as well as with Gephyramoeba sp., Filamoeba nolandi and two unidentified amoebae. This is the first report showing strong support for a clade containing all flagellated amoebozoans and we discuss the position of the root of the phylum Amoebozoa in the light of this result. INTRODUCTION single kinetosome surrounded by a conical microtubular sheath. Submembrane interkinetosomal fibres connect Multicilia marina is a multiflagellated amoeboid protist that each kinetosome to a neighbouring one and coordinate was first isolated in 1880 by L. Cienkowski (Cienkowski, the movement of the flagella. No microtubular connectives 1881) at the Solovetskaya station (Onega Bay, White Sea). between the basal apparatus and the nucleus have been Its cells are usually spherical, about 30–40 mm in diameter, observed (Mikrjukov & Mylnikov, 1996, 1998). The mito- although some of them can have an oblong or irregular chondrial cristae are tubular. Multicilia marina normally form. Typically, each cell has approximately 20–30 flagella. feeds by phagocytosis, using lobopodia for the capture of The basal apparatus of each flagellum is represented by a large prey (gymnamoebae). 3Present address: Department of Genetic Medicine and Development, Cienkowski (1881) described Multicilia as an intermediate Centre Me´dical Universitaire, 1 rue Michel-Servet, 1211 Geneva 4, stage between flagellates and heliozoans. Kudo (1954) con- Switzerland. sidered it to be a member of the order Rhizomastigina 4Present address: Department of Zoology, University of Oxford, The Butschli, together with the family Mastigamoebidae and two Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK. groups of heliozoans, the actinophryids and the dimorphids. 1These authors contributed equally to this work. Later ultrastructural studies revealed that the unusually Abbreviations: BV, bootstrap value; GTR, general time-reversible; ML, weak and oscillating movements of the flagella of Multicilia maximum likelihood; PP, posterior probability; SSU, small subunit. marina (resulting in their superficial similarity to heliozoan The GenBank/EMBL/DDBJ accession numbers for the SSU rRNA axopodia), together with the poor coordination in their gene sequences of Multicilia marina and the unidentified eukaryote activity and a lack of anterior and posterior ends, make clone Borok are AY268037 and AY626163, respectively. Multicilia marina distinct from all other known multi- A figure showing the predicted secondary structure of the small-subunit flagellated/ciliated protistan taxa, such as Caryoblastea, rRNA gene of Multicilia marina is available as supplementary material in Pseudociliata, Hemimastigophora, Ciliophora, Opalinata IJSEM Online. and Parabasalida. A new phylum, Multiflagellata, of 63763 G 2006 IUMS Printed in Great Britain 1449 S. I. Nikolaev and others uncertain affinities was proposed to include the genus vector system (Promega), transformed in XL-2 ultracompetent cells Multicilia (Mikrjukov & Mylnikov, 1996, 1998). In contrast, (Stratagene), sequenced using an ABI PRISM BigDye Terminator cycle Cavalier-Smith (1998) proposed that Multicilia belongs sequencing kit and analysed using an ABI-377 DNA sequencer (Perkin Elmer), all according to the manufacturers’ instructions. in the phylum Amoebozoa, uniting lobose amoebae, the mycetozoan slime moulds and the amitochondriate enta- In addition, we obtained the SSU rRNA gene sequence (as described moebids and pelobionts (Archamoebae), and that the genus above) of an unidentified amoeba (unidentified eukaryote clone is either related to Archamoebae (Cavalier-Smith, 2000) or Borok), which was a contaminant in a culture of the centrohelid to Vannellidae (Cavalier-Smith, 2003; Cavalier-Smith et al., Clathrulina elegans isolated from waste treatment plants in Borok. 2004). In the second edition of the Illustrated Guide to the SSU rRNA gene phylogenetic analyses and secondary- Protozoa, Multicilia was placed among ‘residual hetero- structure modelling. Complete SSU rRNA gene sequences of trophic flagellates’ (Patterson et al., 2000). Multicilia marina and the unidentified eukaryote clone Borok were aligned manually with sequences from diverse eukaryotes using the In spite of the rapid accumulation of sequences from amoe- Genetic Data Environment software (Larsen et al., 1993), following boid organisms during the past few years (Amaral Zettler the secondary-structure model proposed by Wuyts et al. (2001). A et al., 2000; Bolivar et al., 2001; Fahrni et al., 2003; Peglar first dataset, including the two sequences obtained in this study and et al., 2003; Cavalier-Smith et al., 2004; Nikolaev et al., 2004, sequences of 23 lobose amoebae, 25 opisthokonts and 50 bikonts, 2005), to date no molecular data have been reported for was used to infer the position of Multicilia marina among eukary- Multicilia. Previous molecular phylogenetic studies, based otes (1421 unambiguously aligned positions). More-detailed phylo- genetic relationships within the Amoebozoa were then assessed on actin and small-subunit (SSU) rRNA gene sequences, using an alignment of 64 sequences, including the two sequences indicated the monophyly of Amoebozoa, although with obtained in this study and 58 sequences of other amoebozoans very weak support (Bolivar et al., 2001; Fahrni et al., 2003; (including the more divergent mycetozoans, pelobionts and enta- Cavalier-Smith et al., 2004). Furthermore, several higher- moebids) and four opisthokonts as an outgroup (1290 unambigu- level taxonomic lineages have been distinguished within ously aligned positions). GenBank/EMBL/DDBJ accession numbers Amoebozoa (e.g. Smirnov et al., 2005). However, the for all sequences used in our analyses are indicated in Figs 1 and 2. relationships between and within these lineages remain For both datasets, a maximum-likelihood (ML) tree was obtained with unclear. It has been proposed that the ancestral amoebozoan PAUP* (Swofford, 1998), using the general time-reversible (GTR) may have been a flagellated organism similar to Phalans- model of evolution (Lanave et al., 1984; Rodriguez et al., 1990), taking terium
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