Phalansterium digitatum, from Haeckel (1899–1904).

Belongs within: Amoebozoa.

Amoebozoan oddments
Published 15 September 2009
Arachnula, a branched marine amoeboid of uncertain affinities. Photo by D. Patterson et al.

Under the Cavalier-Smith et al. (2004) classification of Amoebozoa, the Variosea was the weakest of the classes they recognised. The characters it was based upon (usually single cilia or centrosomes, no fruiting bodies, non-eruptive pseudopodia) are almost certainly plesiomorphic for Amoebozoa (or possibly the clade of Amoebozoa excluding Breviata), and even the name ‘Variosea’ was coined to refer to the diverse morphologies the class covered. Molecular studies have not indicated variosean monophyly, though the majority of ‘varioseans’ may fall into a paraphyletic series below Archamoebae and Mycetozoa. The Smirnov et al. (2005) classification contained no grouping comparative to Variosea: they simply left the ‘varioseans’ as “Amoebozoa incertae sedis“. Still, this is as good a place as any to introduce the ‘varioseans’, plus a couple of other amoebozoan taxa that don’t fall under the aegis of any of the other major amoebozoan subgroups. In no particular order, these are the ‘Varipodida’, Centramoebida (or Acanthopodida), Stereomyxa, Corallomyxa, Phalansterium, Trichosphaerium and Multicilia.

The name ‘Varipodida’ was introduced by Cavalier-Smith et al. (2004) for a grouping of the non-ciliate genera Gephyramoeba and Filamoeba (though as it turns out ‘Gephyramoeba‘ was misidentified; the varipodidan has been redescribed as Acramoeba, while true Gephyramoeba is a member of Leptomyxida and hence tubulinean; Smirnov et al. 2008). Subsequent studies have been equivocal about the monophyly of such a grouping. Generally, the two genera are close to the clade containing Archamoebae and Mycetozoa (more on that clade in the next post), either just outside it or just within it. Filamoeba is a flattened, fan-shaped amoeboid which produces extremely slender, spine-like subpseudopodia that look superficially like filose pseudopodia (hence the name). However, unlike true filose pseudopodia as found in Rhizaria, the subpseudopodia of Filamoeba do not function in movement. Acramoeba has branched cells, with the branches producing slender subpseudopodia like those of Filamoeba. It’s also worth mentioning Arachnula, which is similar to Acramoeba but larger and multinucleate. Similar slender subpseudopodia are also produced by dictyostelian slime moulds, adding further support to a relationship between Varipodida and Mycetozoa.

Balamuthia mandrillaris. Photo from here.

The Centramoebida include the flattened soil-living amoebae Acanthamoeba and Balamuthia. Acanthamoeba is similar to Filamoeba in producing slender subpseudopodia but Balamuthia does not. Both genera can be pathogenic to humans, though that is probably not their main mode of life—Acanthamoeba has been connected to eye infections, while both Acanthamoeba and Balamuthia can cause meningitis. The really interesting thing about the centramoebids, however, is that unlike any of the amoebozoans I’ve covered recently, they possess a centrosome. The centrosome is an organelle that is involved in controlling the activity of the microtubules that run through the cytoplasm. The centrosome (or, specifically, the centrioles within the centrosome) is also the organelle responsible for the production of cilia. Up until now, I’ve been looking at non-ciliate amoebozoans, but the common ancestor of the Amoebozoa would have been ciliate and some amoebozoans remain so. Just how many times cilia have been lost in the Amoebozoa is unknown—at least five, probably more (Nikolaev et al. 2006). Centramoebids have lost the cilium and the centrioles, but they still retain the evidence of their former presence in the centrosome.

Corallomyxa, though without a species name I’m not certain whether this is supposed to be true Corallomyxa or the rhizarian Filoreta tenera, originally misidentified as a Corallomyxa. Photo by David Patterson.

A similar centrosome to that of Centramoebida is also found in the marine genera Stereomyxa and Corallomyxa, and the three taxa may form a clade (Cavalier-Smith et al. 2004). Stereomyxa and Corallomyxa have slender branched, reticulate pseudopodia, making them look at first glance a bit like a small plasmodial slime mould (though they differ in lacking fruiting bodies). A recent study suggesting that Corallomyxa, at least, may be rhizarian rather than amoebozoan has turned out to be based on another misidentification (Bass et al. 2009).

Trichosphaerium in the naked phase. Photo by David Patterson.

Trichosphaerium is perhaps the most bizarre of all the amoebozoans—and not merely because of its ability to happily chow down on plastic. Trichosphaerium is a relatively large, multinucleate marine amoeboid that lives enclosed in a membranous test. The test is pierced by numerous openings, and the amoeboid extends its pseudopodia through those openings for feeding and locomotion (this differs from the situation in Pellita because the openings are permanent, rather than each individual pseudopodium forcing its way out through the covering). The life cycle of Trichosphaerium alternates between asexual and sexual generations; in the asexual generation, the test has a covering of sharp spicules, but in the sexual generation it is smooth. Reproduction in the asexual stage is by division, but division is generally unequal – a relatively small piece of cytoplasm containing a few nuclei is pinched off to become a separate cell, and the nuclear membrane does not break down during division. In the sexual generation, asexual division may occur as in the asexual generation while the cell is growing, but when the cell finishes growing it forms a cyst. Within the cyst, the cell divides rapidly so that each individual nucleus is contained within its own individual biciliate cell; when the cyst breaks open, these uninucleate cells fuse to give rise to the next generation (Hickson 1909). Under crowded conditions, normal multinucleate cells have also been recorded fusing to give rise to gigantic amoeboid cells up to three millimetres in diameter, with over a thousand nuclei, that break apart into more normal multinucleate within the course of a week.

Phalansterium—drawing of a colony and of an individual cell embedded in its matrix. Image by Stuart Hedley & David Patterson.

Phalansterium is another highly unusual amoebozoan, for the simple reason that it is not an amoeboid (Cavalier-Smith et al. 2004). It’s not even an amoeboflagellate. At one time, Phalansterium was united with the choanoflagellates, which it resembles in having a collar around the base of its single cilium and by living in colonies; however, in Phalansterium the collar is a single undivided fold while in choanoflagellates it is divided into microvilli, while Phalansterium has only a single centriole at the base of its cilium to choanoflagellates’ two. Molecular analysis firmly plonks Phalansterium among the amoebozoans. Cavalier-Smith has made some pretty big calls in relation to unassuming little Phalansterium, claiming it is the closest known organism to the probable ancestral morphology for all eukaryotes. This, however, is based on his assumption that the unikont morphology is ancestral.

Drawing of Multicilia instructa. Image by Won Je Lee.

Finally, Multicilia is a marine amoebozoan with a covering of numerous radially-arranged cilia. Mikrjukov & Mylnikov (1998) found that movement in Multicilia was by irregular, uncoordinated beating of the flagella, causing the cell to roll over the substrate without any obvious organisation into front or back or up or down. Short pseudopodia are extended to capture Multicilia‘s favoured food—other amoebozoans. Generally cells are roughly globular, but in certain unfavourable conditions large branched cells can develop. Cavalier-Smith et al. (2004) suggested that Multicilia was related to the Flabellinea due to the presence of glycostyles in the cell coat, but Nikolaev et al. (2008) placed it closer to other ciliate amoebozoans.

Systematics of Variosea
<==Variosea [Variosia]C-SCL16
    |--Holomastigida [Holomastiga, Holomastigea]C-SCL16
    |    |--Artodiscus [Artodiscidae]AB19
    |    `--Multicilia Cienkowski 1881 [Multiciliidae, Multiciliomonada, Multiflagellata]MM98
    |         |--*M. marina Cienkowski 1881 [incl. Tetracilia paradoxa Valkanov 1970, Polymastix sol Gruber 1884]MM98
    |         |--M. lacustris Lauterborn 1895MM98
    |         `--M. palustris Penard 1903MM98
    |--Varipodida [Gracilipodida]C-SCL16
    |    |--FlamellidaeC-SCL16
    |    |    |--Telaepolella tubasferensAB19
    |    |    `--FlamellaAB19
    |    |         |--F. aegyptiaAB19
    |    |         |--F. balneariaAB19
    |    |         `--F. fluviatilisC-SCL15
    |    `--FilamoebidaeC-SCL16
    |         |--Heliamoeba Berney, Bass & Geisen 2015C-SCL16, AB19
    |         |    `--H. mirabilisC-SCL16
    |         `--Filamoeba Page 1967C-SCO04
    |              |--F. nolandiSN05
    |              `--F. sinensisTA16
    |--Ramamoebida [Cavosteliida]C-SCL16
    |    |--Angulamoeba Berney, Bass & Geisen 2015AB19 [AngulamoebidaeC-SCL16]
    |    |    |--A. fungorumAB19
    |    |    `--A. microcystivoransAB19
    |    |--IschnamoebidaeC-SCL16
    |    |    |--Ischnamoeba Berney, Bass & Geisen 2015AB19
    |    |    |    `--I. montanaC-SCL16
    |    |    `--Darbyshirella Berney, Bass & Geisen 2015C-SCL16, AB19
    |    |         `--D. terrestrisC-SCL16
    |    `--Cavosteliidae [Cavosteliaceae]C-SCL16
    |         |--Tychosporium Spiegel 1995C-SCL16, KC01
    |         |--Cavostelium Olive 1965KC01
    |         |    `--C. apophysatumC-SCO04
    |         `--Schizoplasmodiopsis Olive 1967C-SCL16, KC01
    |              `--S. micropunctataPHK96
    |--Phalansteriida [Schizoplasmodiida]C-SCL16
    |    |  i. s.: Rhizomonas [Rhizomonadidae]C-SCL16
    |    |         Rigidimastix [Rigidomastigidae]C-SCL16
    |    |         TrichonemidaeC-SCL16
    |    |           |--Mitophora Perty 1952C-SCL16
    |    |           `--Trichonemum Cavalier-Smith in Cavalier-Smith, Chao & Lewis 2016 (see below for synonymy)C-SCL16
    |    |                `--*T. hirsutum (Fromentel 1876) [=*Trichonema hirsuta]C-SCL16
    |    |--Arboramoeba Berney, bass & Geisen 2015AB19 [ArboramoebidaeC-SCL16]
    |    |    `--A. reticulataC-SCL16
    |    `--+--Dictyamoeba Berney, Bass & Geisen 2015 [Dictyamoebidae]C-SCL16
    |       |    `--D. voraxC-SCL16
    |       `--Phalansterium Cienkowski 1870C-SCL16, AB19 [Phalansterea, Phalansteriidae]
    |            |--P. consociatumC-SCO04
    |            |--P. digitatumH04
    |            |--P. filosumC-SCL16
    |            `--P. solitariumSN05
    `--Protosteliida [Protostelea]C-SCL16
         |--Protosteliidae [Protosteliaceae]C-SCL16
         |    |--Planoprotostelium Olive & Stoian. 1971C-SCL16, KC01
         |    |    `--P. aurantiumC-SCO04
         |    |--Microglomus Olive & Stoian. 1977KC01
         |    |    `--M. paxillus Olive & Stoianovitch 1977AS12
         |    `--Protostelium Olive & Stoian. 1960KC01
         |         |--P. mycophagaLB90
         |         `--P. nocturnumAB19
              |--Acramoeba [Acramoebidae]C-SCL16
              |    `--A. dendroidaC-SCL16
              |    |--Grellamoeba robustaC-SCL16
              |    `--SoliformovumAS12
              |         |--S. expulsumC-SCL16
              |         `--S. irregularisAB19
                   |--Ceratiomyxella Olive & Stoian. 1971C-SCL16, KC01
                   |    `--C. tahitiensisC-SCL16
                   |--Schizoplasmodium Olive & Stoian. 1966KC01
                   |    `--S. cavostelioidesAB19
                   `--Nematostelium Olive & Stoian. 1970C-SCL16, KC01
                        |--N. gracileAB19
                        `--N. ovatumC-SCL16

Trichonemum Cavalier-Smith in Cavalier-Smith, Chao & Lewis 2016 [=Trichonema Fromentel 1876 nec Ker Gawl. 1802 (ICBN) nec Cobbold 1874]C-SCL16

*Type species of generic name indicated


[AB19] Adl, S. M., D. Bass, C. E. Lane, J. Lukeš, C. L. Schoch, A. Smirnov, S. Agatha, C. Berney, M. W. Brown, F. Burki, P. Cárdenas, I. Čepička, L. Chistyakova, J. del Campo, M. Dunthorn, B. Edvardsen, Y. Eglit, L. Guillou, V. Hampl, A. A. Heiss, M. Hoppenrath, T. Y. James, A. Karnkowska, S. Karpov, E. Kim, M. Kolisko, A. Kudryavtsev, D. J. G. Lahr, E. Lara, L. Le Gall, D. H. Lynn, D. G. Mann, R. Massana, E. A. D. Mitchell, C. Morrow, J. S. Park, J. W. Pawlowski, M. J. Powell, D. J. Richter, S. Rueckert, L. Shadwick, S. Shimano, F. W. Spiegel, G. Torruella, N. Youssef, V. Zlatogursky & Q. Zhang. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66: 4–119.

[AS12] Adl, S. M., A. G. B. Simpson, C. E. Lane, J. Lukeš, D. Bass, S. S. Bowser, M. W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, E. Le Gall, D. H. Lynn, H. McManus, E. A. D. Mitchell, S. E. Mozley-Stanridge, L. W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C. L. Schoch, A. Smirnov & F. W. Spiegel. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59 (5): 429–493.

Bass, D., E. E.-Y. Chao, S. Nikolaev, A. Yabuki, K. Ishida, C. Berney, U. Pakzad, C. Wylezich & T. Cavalier-Smith. 2009. Phylogeny of novel naked filose and reticulose Cercozoa: Granofilosea cl. n. and Proteomyxidea revised. Protist 160 (1): 75–109.

[C-SCL16] Cavalier-Smith, T., E. E. Chao & R. Lewis. 2016. 187-gene phylogeny of protozoan phylum Amoebozoa reveals a new class (Cutosea) of deep-branching, ultrastructurally unique, enveloped marine Lobosa and clarifies amoeba evolution. Molecular Phylogenetics and Evolution 99: 275–296.

[C-SCO04] Cavalier-Smith, T., E. E.-Y. Chao & B. Oates. 2004. Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. European Journal of Protistology 40: 21–48.

[H04] Haeckel, E. 1899–1904. Kunstformen der Natur. Bibliographisches Institut: Leipzig und Wien.

Hickson, S. J. 1909. The Lobosa. In: Lankester, R. (ed.) A Treatise on Zoology pt 1. Introduction and Protozoa first fascicle. Adam & Charles Black: London.

[KC01] Kirk, P. M., P. F. Cannon, J. C. David & J. A. Stalpers. 2001. Ainsworth & Bisby’s Dictionary of the Fungi 9th ed. CAB International: Wallingford (UK).

[LB90] Lousier, J. D., & S. S. Bamforth. 1990. Soil protozoa. In: Dindal, D. L. (ed.) Soil Biology Guide pp. 97–136. John Wiley & Sones: New York.

[MM98] Mikrjukov, K. A., & A. P. Mylnikov. 1998. The fine structure of a carnivorous multiflagellar protist, Multicilia marina Cienkowski, 1881 (Flagellata incertae sedis). European Journal of Protistology 34: 391–401.

Nikolaev, S. I., C. Berny, N. B. Petrov, A. P. Mylnikov, J. F. Fahrni & J. Pawlowski. 2006. Phylogenetic position of Multicilia marina and the evolution of Amoebozoa. International Journal of Systematic and Evolutionary Microbiology 56: 1449–1458.

[PHK96] Prescott, L. M., J. P. Harley & D. A. Klein. 1996. Microbiology 3rd ed. Wm. C. Brown Publishers: Dubuque (Iowa).

[SN05] Smirnov, A., E. Nassonova, C. Berney, J. Fahrni, I. Bolivar & J. Pawlowski. 2005. Molecular phylogeny and classification of the lobose amoebae. Protist 156: 129–142.

Smirnov, A. V., E. S. Nassonova & T. Cavalier-Smith. 2008. Correct identification of species makes the amoebozoan rRNA tree congruent with morphology for the order Leptomyxida Page 1987; with description of Acramoeba dendroida n. g., n. sp., originally misidentified as ‘Gephyramoeba sp.’ European Journal of Protistology 44 (1): 35–44.

Smirnov, A. V., E. S. Nassonova, E. Chao & T. Cavalier-Smith. 2007. Phylogeny, evolution, and taxonomy of vannellid amoebae. Protist 158 (3): 295–324.

[TA16] Tekle, Y. I., O. R. Anderson, L. A. Katz, X. X. Maurer-Alcalá, M. A. Cerón Romero & R. Molestina. 2016. Phylogenomics of ‘Discosea’: a new molecular phylogenetic perspective on Amoebozoa with flat body forms. Molecular Phylogenetics and Evolution 99: 144–154.

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