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Molecular Phylogeny and Classification of the Lobose Amoebae

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Molecular Phylogeny and Classification of the Lobose Amoebae ARTICLE IN PRESS Protist, Vol. 156, 129—142, August 2005 http://www.elsevier.de/protis Published online date 12 July 2005 PROTIST NEWS Molecular Phylogeny and Classification of the Lobose Amoebae Introduction The lobose amoebae can be defined as presum- The involvement of microphotography and ably asexual amoeboid organisms, producing electron microscopy in the routine practice of lobopodia and possessing a simple life cycle, protozoology led to the discovery of specific involving only cell division and, in some species, ultrastructural features in many amoeboid protists. encystment. They move due to the activity of the It resulted in the re-description of many already acto-myosin cytoskeleton; cytoplasmic microtu- known amoeboid organisms and description of bules, if present, are rare and not organized in numerous new species of amoebae, and allowed bundles (Grebecki 1994; Page 1988, 1991; Ro- investigators to establish the relationships be- gerson and Patterson 2002; Smirnov and Good- tween and within some amoeboid taxa (Flickinger kov 2000). 1974; Page 1978, 1980a, 1985, 1986; Page and Amoeboid movement involves the entire cell Blanton 1985). A new synthetic system of amoe- body, and thus lobose amoebae possess neither a boid organisms, combining light- and electron- stable cell shape nor differentiated locomotory microscopical features together with some as- organelles. As a result, the number of distinctive pects of their biology and physiology was devel- morphological features in amoebae is very limited, oped (Page 1987, 1988, 1991). All naked lobose and their morphological identification and classi- amoebae were grouped in the class Lobosea, fication remain a difficult task. Earlier phylogenetic subclass Gymnamoebia, with four orders (Eua- suggestions based on light-microscopic morphol- moebida, Leptomyxida, Acanthopodida and Lo- ogy (e.g. by Schaeffer 1926) or seemingly more boreticulatida), while the testate lobose amoebae basic features, like the nuclear division pattern (order Arcellinida) were placed in the subclass (Chatton 1953; Singh 1955) were later found to be Testacealobosia. This system was mainly aimed at inadequate. In an attempt to reach a more natural resolving the low-level relationships among amoe- grouping of amoeboid taxa, T. Jahn and E. Bovee bae and provided practical tools for species created a system based on the pattern of identification. However, higher-level phylogenetic cytoplasmic flow (Jahn and Bovee 1965; Jahn et relationships within amoebae remained ‘‘unreco- al. 1974). However, this attempt did not result in a verable from morphology’’ (Page 1987), and practical system either, mainly because of the further development of Page’s system (see Ro- difficulties in defining genera and distinguishing gerson and Patterson 2002) did not improve the species. The line drawings, which were the only situation. available illustrative documentation on lobose amoebae until the early 1960s, were rather ‘‘author-specific’’ and often did not allow a reliable Molecular Phylogeny of Lobose recognition of the species by other investigators. Amoebae The growing number of species that were difficult to recognize (e.g. Bovee 1953; Leps-i 1960; Early molecular studies based on small-subunit Sawyer 1975a, b) emphasized the need to clarify ribosomal RNA (SSU rRNA) gene sequences the criteria of species identification among amoe- suggested independent origins for different bae prior to any attempt to create a comprehen- lineages of lobose amoebae (Cavalier-Smith sive system. 2000; Hinkle et al. 1994; Silberman et al. 1999; & 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.protis.2005.06.002 ARTICLE IN PRESS 130 A. Smirnov et al. Sims et al. 1999). However, as the number of corresponding to the family Vannellidae, and the available sequences increased, and with the use second comprising members of the families of more accurate methods of phylogenetic ana- Paramoebidae and Vexilliferidae. There is also lyses, it became evident that the independent good evidence from SSU rRNA- and protein- branching of lobose amoebae in early phylogenies based studies that all amitochondriate amoebae was an artifact of phylogenetic reconstructions (entamoebids, mastigamoebids, and Pelomyxa) related to the long branch attraction phenomenon. form a monophyletic group of Archamoebae Several recent phylogenetic analyses, including a (Arisue et al. 2002; Edgcomb et al. 2002; Fahrni large taxon sampling of eukaryotes, and using et al. 2003; Milyutina et al. 2001). Multigene methods correcting for among-site rate hetero- analyses of protein data strongly support the geneity, showed that all sequenced lobose amoe- relationship between Archamoebae and Myceto- bae form a clade that generally also includes zoa (Bapteste et al. 2002), classified together in mycetozoans (Bolivar et al. 2001; Cavalier-Smith the subphylum Conosa (Cavalier-Smith 1998). et al. 2004; Fahrni et al. 2003; Milyutina et al. However, because of the fast evolving SSU rRNA 2001). Although usually weakly supported, the gene sequences of most Archamoebae and monophyly of lobose amoebae and mycetozoans Mycetozoa, their grouping does not appear in was confirmed by phylogenetic analysis of actin most phylogenies based on this gene (Cavalier- (Fahrni et al. 2003), and multigene analyses of Smith et al. 2004; Fahrni et al. 2003). Finally, nuclear (Baldauf et al. 2000) and mitochondrial there is also some evidence that the free-living (Forget et al. 2002) protein sequences, as well as amoeboid protists such as Gephyramoeba the analysis of 123 genes obtained from EST and Filamoeba (Bolivar et al. 2001)orthe libraries of Entamoeba, Mastigamoeba, and Dic- flagellated Phalansterium solitarium (Cavalier- tyostelium (Bapteste et al. 2002). However, none Smith et al. 2004) might be more closely related of these multigene studies contained representa- to Mycetozoa and/or Archamoebae than to other tives of all lineages of amoebae simultaneously, lobose amoebae. nor included a typical free-living lobose amoeba. In the high-level classification of Protozoa, all naked and testate lobose amoebae, together with Molecular Phylogeny versus entamoebids, pelobionts, and mycetozoans, were Morphological Classification grouped in an emended phylum Amoebozoa (Cavalier-Smith 1998, 2002, 2003; Cavalier-Smith The molecular phylogeny of lobose amoebae is et al. 2004). broadly congruent with the morphological system While several molecular markers now support a at the level of genera and some families, but common origin of all amoebozoans, evolutionary strongly disagrees with it starting at the level of relationships within lobose amoebae are also orders and subclasses. The first attempts to find a becoming clearer. Thanks to a rapidly increasing correlation between the molecular phylogeny and sampling of species, the SSU rRNA-based phylo- the morphological characters of amoebae at geny of Amoebozoa allows the distinction of a few higher taxonomic level generally failed (Amaral well-defined clades. Bolivar et al. (2001) demon- Zettler et al. 2000; Bolivar et al. 2001; Peglar et al. strated the existence of the ‘‘Gymnamoebia sensu 2003). Only two orders of the Gymnamoebia stricto’’ containing the families Amoebidae and sensu Page (1987), Acanthopodida and Lepto- Hartmannellidae and the order Leptomyxida. This myxida, seem to be supported by molecular data. clade was also recovered in an analysis of actin The other typical naked lobose amoebae (Eu- (Fahrni et al. 2003) and in a further SSU rRNA- amoebida sensu Page 1987) are split into several based study (Cavalier-Smith et al. 2004). A recent lineages, one of which includes the Leptomyxida study revealed that the testate lobose amoebae of and the Arcellinida. the order Arcellinida also belong to this group In a revised classification of the phylum Amoe- (Nikolaev et al. 2005). Among other well-defined bozoa based on the SSU rRNA phylogeny, clades of lobose amoebae, there is good support Cavalier-Smith et al. (2004) attempted to produce for the grouping of Acanthamoeba and Bala- a system congruent with both molecular and muthia, as first shown by Amaral Zettler et al. morphological data. The authors grouped the (2000) and confirmed by subsequent studies majority of typical naked lobose amoebae in two (Bolivar et al. 2001; Cavalier-Smith et al. 2004; classes: the Lobosea, with ‘‘ancestrally cylindrical Fahrni et al. 2003). Peglar et al. (2003) established and non-eruptive’’ pseudopods, but ‘‘sometimes the existence of two additional lineages, the first flattened or eruptive’’, and ‘‘lacking glycostyles or ARTICLE IN PRESS Phylogeny and Classification of the Lobose Amoebae 131 scales’’ (e.g. the families Amoebidae and Hart- amoebae and selected sequences of Conosa mannellidae, plus the orders Leptomyxida and (Fig. 1). We focus our study on two lineages, Arcellinida); and the Discosea, defined as ‘‘flat- called here Tubulinea and Flabellinea, containing tened amoebae with leading lamellipodium’’ the majority of the Gymnamoebia sensu Page and ‘‘usually with glycostyles or organic scales’’ 1987 and the testate lobose amoebae of the order (e.g. the families Vannellidae, Paramoebidae, Arcellinida. We analyze the systematic composi- Vexilliferidae, and Thecamoebidae). A third class, tion and morphological characters of every well- Variosea, was created to accommodate the defined clade and compare them with both Acanthopodida and the genera Filamoeba, Ge- modern and ancient systems of amoebae in order phyramoeba, and Phalansterium. The shape of the to recover the shared morphological features
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