DESCRIPTION OF THE PHYLUM HETEROLOBOSA (PAGE AND BLANTON 1985)

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Heterolobosa (he-te-ro-lo-BO-sa) is made of two Greek roots that mean different (heteros -έτερος) and rounded projection (lobos -λοβός). The reference is to the cells living different lives as flagellated cells and creeping amoebae that move by lobose pseudopodia.

INTRODUCTION TO THE HETEROLOBOSA The Heterolobosa (also called the amoeboflagellates or schizopyrendia) are somewhat enigmatic as a group. In general, they appear as amoebae that produce small, eruptive lobose (text with tooltip) Lobose (adj.) usually refers to the rounded shape of certain pseudopods. pseudopodia (text with tooltip) tipso . Most of them can sprout flagella under certain conditions and swim away. A few are economically important. For example, Naegleria gruberi (Figure 1) can be pathogenic to humans by causing meningoencephalitis. Acrasis (Figure 2) and its related taxa are free-living and form cellular slime molds that superficially resemble those of Dictyostelium but much smaller. Psalteriomonas (Figure 3) is a free-living, but microaerophilic taxon, which although it has no cristae (text with tooltip) Cristae (crista, sing.) generally refer to folds of the inner membranes of mitochondria. , is otherwise similar to the other heteroloboseans (Figure 3 shows both amoeboid and flagellated forms). Percolomonas (Figure 4) does not have an amoeboid stage and has variable cristae; however, careful work by Brugerolle and Simpson (2004) demonstrates that it is a heterolobosean. Margulis and Schwartz (1988) considered this to be part of a large, heterogeneous group of flagellated organisms called the “Zoomastigina” (Pr-8). Then, Margulis and Schwartz (1998) modified the taxonomy to include them together with the euglenoids and trypanosomes in a taxon called Discomitochondria (Pr-12). We have raised the classes of the Discomitochondria to the phylum level. Dyer (1990) also grouped the amoeboflagellates into the “Zoomastigina,” but added to the taxonomic confusion by reporting that the DNA of Naeglaria was similar to the base composition of Physarum (a plasmodial slime mold in which amoeboid and flagellated stages also occur). Kudo (1966), Grell (1976), Lee et al. (1985) and Sleigh et al. (1984) considered these to be members of the amoebae or “Sarcodina.” However, like Margulis and Schwartz (1988 and 1998), we accept that the production of pseudopodia is too variable as a character to establish a phylogenetic taxonomy. Also, the amoeboflagellates produce pairs of flagella or at least pairs of basal bodies, a character that is not found in the Rhizopods. Patterson (1999) and Taylor (1999) summarize information that confirms the association of the amoeboflagellates and acrasids (a group of cellular slime molds) with the discomitochondrial line. Like the Kinetoplastids and Euglenoids, the Heterolobosa have parallel basal bodies and mitochondria with saccate (swollen) cristae. Baldauf (2003) also places the amoeboflagellates (she calls them the vahlkampfid amoebae) as sisters to the acrasid slime molds within the “Discicristates”. The proposal of Cavalier-Smith (2003) groups all of the Heterolobosa into a taxon with the other discicristates together with the euexcavates into an infrakingdom. His phylum, Percolozoa, however, lumps together the amoeboflagellates, acrasids, and the very odd taxon, Stephanopogon on the suggestion that the ancestral taxa have basal bodies in groups of four subparallel basal bodies. Because Stephanopogon does not have clear affinities, we have separated it into a separate “phylum” of uncertain status; however, Figure 5 does suggest that it belongs within the Heterolobosa. Percolomonas (Figure 4), a motile taxon that has no amoeboid stage, seems to have an unclear relationship with the rest of the Heterolobosa. Cavalier-Smith (2003a) places it in a subgroup with Stephanopogon. Nikolaev et al. (2004) find that Percolomonas emerges within the Valkampfid clade, and, therefore, a member of the Schizopyrenida. However, because their analysis is based solely on small subunit rRNA, we are reluctant to place it in the Schizopyrenida. The morphological work by Brugerolle and Simpson (2004) demonstrates that there is no fundamental difference between the Percolomonads and the rest of the Heteroloboseans as Cavalier-Smith (2003a) and Panek et al. (2011) suggest. Figure 5 illustrates a summary of the analysis of the Heterolobosa by Panek et al. (2011). Their analysis used the SSU rDNA gene and the Maximum Likelihood method to generate a phylogeny in which the Schizopyrenida occupy three different clades. We have named these clades the Naegleria Clade (Schizopyrenida I), Tetramitus clade (Schizopyrenida II), and the Paravalkampfia clade (Schizopyrendia III). A further surprise is the sister relationship between the Percolomonadida and the Pseudociliata (a separate phylum in our system). If the results of Panek et al. (2011) are confirmed, major revisions in the taxonomy of the Heterlobosea will be necessary.

FIGURE 1. Naegleria, amoeboflagellate that is pathogenic to humans and causes meningoencephalitis. Image from CDC, in the Public Domain	FIGURE 2. Acrasis, a “cellular slime mold” with clear affinities to the heteroloboseans. The image shows the fruiting body of a colony. Image from http://cosmos.bot.kyoto-u.ac.jp/csm/photos2/Ar3s.jpeg	FIGURE 3. An illustration of Psalteriomonas, with the motile and amoeboid forms. Note that the flagella come in groups of fours. Image from http://cosmos.bot.kyoto-u.ac.jp/csm/photos2/Ar3s.jpeg	FIGURE 4. Percolomonas, a heterolobosean that never forms an amoeboid form. Like Psalteriomonas, its flagella occur in a group of four. Image from http://microscope.mbl.edu/scripts/microscope.php?func=imgDetail&imageID=621

FIGURE 5. Relationships within the Heterolobosea (taxa in shaded box) according to Panek et al. (2011), who used the SSU rDNA gene and the Maximum Likelihood method. The Schizopyrenida emerges as three major clades: Naegleria Clade (Schizopyrenida I), Tetramitus clade (Schizopyrenida II), and the Paravalkampfia clade (Schizopyrendia III).

LITERATURE CITED Brugerolle, G., and A. G. B. Simpson. 2004. The flagellar apparatus of heteroloboseans. Journal of Eukaryotic Microbiology. 51(1): 96-107. Cavalier-Smith, T. 2003a. Protist phylogeny and the high-level classification of Protozoa. European Journal of Protistology. 39:338-348. Dyer, B.D. 1990a. Amoebomastigota. In: Margulis, L., J.O. Corliss, M. Melkonian, and D.J. Chapman, eds. 1990. Handbook of the Protoctista; the Structure, Cultivation, Habits and Life Histories of the Eukaryotic Microorganisms and Their Descendants Exclusive of Animals, Plants and Fungi. Jones and Bartlett Publishers. Boston. pp. 186-190. Grell, K. G. 1973. Protozoology. Springer-Verlag. New York. Kudo, R.R. 1966. Protozoology. 5th ed. Charles C. Thomas Publisher. Springfield. Lee, J. J., S. H. Hunter, and E. C. Bovee, eds. 1985. An Illustrated Guide to the Protozoa. Society of Protozoologists. Lawrence, Kansas. Margulis, L. and K. Schwartz. 1988. Five kingdoms, an illustrated guide to the phyla of life on earth. 2nd Edition. W.H. Freeman and Co. New York. Margulis, L. and K. Schwartz. 1998. Five kingdoms, an illustrated guide to the phyla of life on earth. 3rd Edition. W. H. Freeman and Company. New York. Nikolaev, S.I., C. Berney, J. Fahrni, I. Bolivar, S. Polet, A.P. Mylnikov, V.V. Aleshin, N.B. Petrov, and J. Pawlowski. 2004. The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proceedings of the National Academy of Sciences. USA. 101(21): 8066-8071. Page, F. C. and R. L. Blanton. 1985. The Heterolobosea (Sarcodina: Rhizopoda), a new class uniting Schizopyrenida and the Acrasidae (Acrasida). Protostologica. 21:121-132. Panek, T., J. D. Silberman, N. Yubuki, B. S. Leander, and I. Cepicka. 2011. Diversity, evolution and molecular systematics of the Psalteriomonidae, the main lineage of anaerobic/microaerophilic heteroloboseans (Excavata: Discoba). Protist. in press. doi:10.1016/j.protis.2011.11.002. Patterson, D. J. 1999. The diversity of eukaryotes. American Naturalist. 154 (Suppl.): S96–S124. Sleigh, M.A., J.D. Dodge and D.J. Patterson. 1984. Kingdom Protista. In: Barnes, R.K.S., ed. A Synoptic Classification of Living Organisms. Sinauer Associates, Inc. Sunderland, Mass.

By Jack R. Holt. Last revised: 02/17/2014