Tubulinea

Amoeba proteus, copyright Wim van Egmond.

Belongs within: Amoebozoa.
Contains: Microcoryciidae, Arcellinida.

The Tubulinea are a group of strictly amoeboid amoebozoans that are capable of producing tubular pseudopodia.

Amoeba: much weirder than you think
Published 2 September 2009
Amoeba proteus extending pseudopodia to feed on a hapless ciliate. Note how the pseudopodia completely surround the ciliate, cutting off any escape, before they close in on it. A fantastic photo by Wim van Egmond—you owe it to yourself to visit that link.

I have been challenged (or at least, I think I have been challenged) to write some posts on amoebozoans, the clade of eukaryotes that includes such organisms as Amoeba and most slime moulds. As amoebozoans are unequivocally neat organisms, I’m happy to take up the challenge, but I thought Id start by focusing on the most famous amoebozoan genus of all, Amoeba itself. There are about five or so species of Amoeba (at least that I’m aware of), but most of what I’m going to say in this post applies equally to all of them. I think I’m safe in claiming that Amoeba is not just the most famous amoebozoan, it’s also the most famous of all unicellular eukaryotes. Almost all general biology textbooks will include two examples of ‘protists’, and one of them will always be Amoeba (the other will be either Euglena or Paramecium). The funny thing about this ubiquity of the Amoeba exemplar, however, is that as unicellular protists go, Amoeba is actually (a) apparently not that common, and (b) seriously wierd*.

*Euglena and Paramecium aren’t that typical either.

What makes Amoeba so odd? For a start, Amoeba is amoeboid* (kind of by definition, really). This might not seem so unusual at a glance (many micro-organisms are amoeboid), but the thing is that Amoeba is always amoeboid. It never possesses cilia. Many (if not most) other amoeboid eukaryotes transform into amoeboflagellates or flagellates for at least part of their life-cycle, or possess flagellated gametes, while the majority of unicellular eukaryotes are permanently flagellated**. Even among amoebozoans, cilia are not that unusual; they’re still present in Breviata, Multicilia, Phalansterium, Mastigamoebidae, Pelomyxa and many Mycetozoa, though cilia have been entirely lost among amoebozoans at least nine times (Cavalier-Smith et al. 2004).

*Simply for the sake of avoiding confusion, I prefer to avoid the common use of the name “amoeba” to refer to any organism with an Amoeba-like morphology.

**A brief explanation about the terms “cilium” and “flagellum”. Originally, the term “cilium” was used for small hair-like locomotory structures, usually present in large numbers, while “flagellum” referred to larger whip-like structures of which a cell would usually only have one or a few. As our knowledge of unicellular diversity broadened, the boundary between the two became increasingly blurred, and fundamentally they’re all the same structure. On the other hand, “flagella” in bacteria, though superficially resembling flagella in eukaryotes, are structurally very different (eukaryote flagella are organelles formed of membrane-bound microtubules, while bacterial flagella are formed of a single protein strand). As a result, recent authors have tended to restrict the term “flagellum” to bacteria, and expand the term “cilium” to cover all eukaryote locomotory structures (a replacement term “undulipodium” never caught on [thankfully]). However, terms such as “flagellate” are still pretty well entrenched in their old sense.

Amoeba ‘radiosa’, photo by David Patterson & Aimlee Laderman. Despite the use of the name, there is not really such a species as ‘Amoeba radiosa’. Rather, the name is used to indicate amoebae that have become detached from the substrate and are free-floating in the water column, where they abandon their usual flattened form and adopt a form with slender pseudopodia radiating from a spherical centre. Once they come back into contact with a solid surface, they will return to their normal morphology.

The second unusual thing about Amoeba (which is perhaps not unconnected to the first thing) is its reproductive habits. Most people are aware that Amoeba reproduce by division. That happens to be the only way that Amoeba reproduce (Chapman-Andresen 1971); they are (so far as anyone knows) entirely asexual. While asexual reproduction is normal for many organisms, exclusively asexual lineages are something of a rarity. Most asexually reproducing organisms have more aphid-like life cycles – they reproduce asexually as long as conditions are favourable for doing so, but convert to sexual reproduction when times get tough. Even bacteria, which mostly don’t engage in sexual reproduction per se, are able to engage in processes such as conjugation that still allow for gene flow.

And the third wierd thing about Amoeba has to be its genetics. Amoeba genomes are simply huge—the largest genomes known to exist, in fact. We humans have a genome that clocks in at a little under three billion base pairs of DNA. Amoeba proteus, the best-known species of Amoeba, has a genome containing closer to three hundred billion base pairs. And even that effort pales in comparison to Amoeba dubia, which carries around a whopping six hundred and seventy billion base pairs. That’s right—the difference in genome size alone between the two species is larger than the total genome size of any other organism! The actual genetic structure of Amoeba, however, appears to be little-known. The genome of A. proteus is divided between more than five hundred chromosomes, which is hardly surprising considering its size. By means unknown, however, this enormous genome can be reduced to nearly a third of its normal size over the course of cell division (Parfrey et al. 2008). Presumably the normally polyploid amoeba jettisons excess chromosomes prior to division then recreates them from the remainder afterwards.

Amoeba proteus on the move (towards the top left of the photo). Note the knobbly bit at the bottom right corner. This is the uroid, and represents the trailing end of the cell. The form of the uroid has turned out to be surprisingly useful in identifying amoeboids. Another photo by David Patterson.

One other feature of the Amoeba nucleus is worth mentioning. The nucleus contains a number of stellate aggregations of condensed helical structures just inside the nuclear envelope that, when first observed, were not unreasonably thought to represent condensed chromosomes. However, further study showed that the nuclear helices were composed of a mixture of proteins and RNA (not DNA) and seemed to be able to be transported out of the nucleus into the surrounding cytoplasm (Minassian & Bell 1976). The helices disappear over the course of cell division, but are regenerated afterwards. The exact function of these helices is still unknown. Minassian & Bell (1976) seem to have suggested (in a rather cagy way that would have allowed for ready back-tracking if they turned out to be wrong, and which I may have easily misinterpreted) that they could be related to ribosome formation. Gągola et al. (2003), in contrast, note the attachment of actin filaments to the helices, and imply that they may play a role in cell motility (Amoeba with removed nuclei are unable to move*, while amoeboid animals cells can continue to move even without their nuclei).

*Removing the nucleus from an Amoeba is as simple as slicing it in half.

Tubulinea: the paragons of amoeboids
Published 9 September 2009
The basal tubulinean Echinamoeba. If you look very closely at the lower end of the cell, you can see the filaments of the adhesive uroid. Photo by David Patterson et al.

Due to popular demand (does two count as popular?), I’m continuing with the Amoebozoa series. The two major classifications of Amoebozoa that have been published in recent years are those of Cavalier-Smith et al. (2004) and Smirnov et al. (2005). While at first glance the two systems appear quite different, there are few real significant differences between them. Mostly it’s a matter of different names being used for similar concepts, plus the Cavalier-Smith et al. classification assigns positions to a number of taxa that the more conservative Smirnov et al. classification is content to list as Amoebozoa incertae sedis. The Cavalier-Smith et al. classification divides amoebozoans between seven ‘classes’, which offers a good basis for dividing my posts. One of Cavalier-Smith et al.‘s classes currently includes a single species, the strange (and not necessarily amoebozoan) Breviata anathema, which has previously been covered here, while the two classes of their infraphylum Mycetozoa (slime moulds) are described here. So that leaves four classes that I haven’t yet covered in detail. In the coming posts, I’ll start with the Tubulinea, move to the Discosea, waft through the ‘Variosea’ and finish with the Archamoebae. And if that seems like a lot to you, just be glad I didn’t choose to do my amoeboid series on Foraminifera—we could have been here well into the next century.

The “Tubulinea” of Smirnov et al. (2005) are the same grouping as the “Lobosea” of Cavalier-Smith et al. (2004). I prefer to use the name Tubulinea because Lobosea has been used in the past for a much larger grouping, effectively all amoebozoans except Mycetozoa and (sometimes) Archamoebae. Also, the name Tubulinea refers to one of the characteristic features of this group, the production of tubular rather than flattened pseudopodia, with cytoplasmic flow within the pseudopodia or entire cell along a single axis. All Tubulinea lack cilia at all stages of the life cycle. The Tubulinea include the Tubulinida (Amoeboidea of Cavalier-Smith et al.), Arcellinida, Copromyxidae, Leptomyxida and Echinamoeba, and both the papers cited above produced identical phylogenies for this class.

Leptomyxa, type genus of the Leptomyxida. Note the branched morphology. Don’t ask me to tell you which way this one’s going—I think that might be the uroid towards the bottom right, but I’m not sure. Photo by David Patterson et al.

Echinamoeba forms the basalmost clade within the Tubulinea, together with the species ‘Hartmannella’ vermiformis (erroneous comments on the relationships of the family Hartmannellidae in Cavalier-Smith et al., 2004, are due to the use of H. vermiformis to represent Hartmannella; it wasn’t until later that Smirnov et al., 2005, showed that H. vermiformis is not closely related to other Hartmannella species. The normal cell shape of Echinamoeba is “acanthopodian”—flattened with short, spinelike subpseudopodia (Smirnov & Goodkov 1999); it only produces a more typically tubulinean cylindrical, monopodial form under particular conditions. The form it takes in these conditions is one produced by many amoeboids called the ‘limax’ form. Limax is a genus of slugs, and a microscopic slug is exactly what this form looks like. ‘Hartmannella’ vermiformis, on the other hand, is habitually worm-like, and has gained a certain notoriety as an unwitting vector for bacteria causing respiratory diseases in humans, particularly Legionnaire’s disease (Brieland et al. 1997).

The Leptomyxida are the next group to branch off. The four genera of leptomyxidans—Leptomyxa, Rhizamoeba, Flabellula and Paraflabellula—resemble Echinamoeba by normally being flattened, and only adopting a tubular limax-like form occasionally. The normal form of Leptomyxa is reticulate, with a anastomosing net of pseudopodia. In the other three genera, the uroid (the trailing end of the moving cell) is adhesive, so when the cell is moving the posterior end is drawn out into smeared streaks. Rhizamoeba is monopodial, while the other two genera are fan-shaped. Paraflabellula produces short subpseudopodia from the anterior edge of the cell, Flabellula doesn’t.

The fruiting body of Copromyxa arborescens, which grows up to 2.5 mm in height. Figure from Nesom & Olive (1972).

The Copromyxidae were placed by Cavalier-Smith et al. (2004) among the Tubulinea on the basis of their morphology (but were not represented in the molecular analysis), but were not even mentioned by Smirnov et al. (2005). Copromyxids include two little-studied genera, Copromyxa and Copromyxella. Cavalier-Smith et al. suggested that they are closer to Arcellinida and Tubulinida than other Tubulinea as these three groups are habitually rather than only intermittently tubular. Copromyxids differ from other Tubulinea in having a slime-mould type life cycle (I overlooked them in my earlier slime mould post). Life for copromyxids really is a pile of crap—their chosen habitat is animal dung. Fruiting bodies are produced by previously separate cells aggregating together to form a mound. Newly-arriving cells clamber over their confederates to reach the top of the pile, and the eventual result is a small, vaguely tree-like fruiting body (Bonner 1982). Copromyxids are very similar in appearance to the non-amoebozoan acrasid slime moulds, and many earlier references combine the two.

The Arcellinida are the most speciose subgroup of Tubulinea (at least, as far as we know). Arcellinida are the testate Amoebozoa—they possess are hardened test of either secreted proteinaceous material or agglutinated mineral grains. The test is roughly vase-shaped, with a single opening through which the organism extends its pseudopodia. Phylogenetic studies (Nikolaev et al. 2005) confirm that the testate Amoebozoa form a monophyletic group (which, as I noted earlier, forms an interesting contrast to the polyphyletic testate Rhizaria), but the same cannot be said for proteinaceous- versus agglutinated-test formers, with lineages apparently switching between the two a number of times.

Nebela tubulosa, a member of the Arcellinida. Photo by Antonio Guillen.

Finally, the Tubulinida includes Amoeba itself and its nearest and dearest (such as Chaos, Saccamoeba and true Hartmannella). Tubulinida differ from Echinamoeba and Leptomyxida in being permanently tubular, never flattened. The cell may move limax-wise as a single pseudopodium (Saccamoeba, Hartmannella, sometimes Amoeba) or may form multiple pseudopodia (Chaos, other times Amoeba). Both Cavalier-Smith et al. and Smirnov et al. placed Chaos and Amoeba closest to one another, and indeed phylogenetically mixed together. As the only difference between the two seems to be the number of nuclei (one in Amoeba, more in Chaos) it would perhaps not be surprising if one or the other, or both, turned out to be polyphyletic.

Finally, I’d like to end this post on a bit of speculation. Above, I described the ridiculously large genome of Tubulinida species (thanks to commentor George X for pointing out that the species I referred to as Amoeba dubia is now known as Polychaos dubium). I tried to find if any studies had been done on the detailed genetic structure of these species, to see if there was any clue as to just why Tubulinida have such enormous genomes, but I couldn’t find any. Indeed, when searching on Amoeba in Google Scholar, I was struck by the dates shown for most of the results—a significant proportion dating back to the period from the 1940s to the 1960s. It looks like Amoeba proteus, so popular as a model organism in the early days of cell biology due to its large size making it easy to observe and manipulate, may have since fallen in popularity. I can guess at some reasons why that might be—I get the impression that Amoeba‘s rarity makes it tricky to find, that it is difficult to maintain in culture once you do find it, and I wonder if, in a time when electron microscopy has become almost routine, Amoeba is large enough that its size has become a positive disadvantage rather than advantage.

In the absence of much information about Amoeba‘s genome beyond its size, speculation becomes ill-founded. The large size of the genome doesn’t necessarily indicate a proportionally large number of genes—it could be that Amoeba is carrying a particularly heavy load of non-coding DNA. Also, the previously-mentioned cyclic nature of the Amoeba genome, with the amount of DNA increasing and decreasing over the course of the division cycle by a factor of nearly three (Parfrey et al. 1998), suggests that Amoeba proteus is at least hexaploid. Again, it might not be—perhaps instead of the entire genome being replicated three times, a smaller number of chromosomes are replicated many times (as we know happens with such things as B chromosomes in animals). But, with all those caveats, I still can’t help wondering if the cyclic Amoeba genome is related to its unusual success as an asexual organism. Let us assume that the entire genome is replicated in the cell cycle, and that it is random which of the resulting replicate chromosomes gets retained and which disposed of prior to division. The result would be that the effective mutation rate of Amoeba would probably be noticeably higher than in organisms with more straightforward genetic cycles. Could this be what has allowed Amoeba to survive for so long seemingly without the benefit of recombination?

Systematics of Tubulinea

Characters (from Smirnov et al. 2005): Naked or testate amoebae producing tubular, subcylindrical pseudopodia or capable of altering locomotive form from flattened, expanded one to subcylindrical one. Monoaxial flow of cytoplasm in every pseudopodium or in entire cell. No cytoplasmic microtubule-organising centres; no flagellate stage in life cycle.

<==Tubulinea [Arcellina, Hartmannellina, Lobosea, Neolobosia, Tubulina]
    |--CorycidaAB19
    |    |--MicrocoryciidaeAB19
    |    `--Trichosphaeriidae [Trichosia, Trichosida, Trichosidae]C-SCL16
    |         |--Pontifex marinusC-SCL16
    |         |--Atrichosa Cavalier-Smith in Cavalier-Smith, Chao & Lewis 2016C-SCL16
    |         |    `--*A. algivora Cavalier-Smith in Cavalier-Smith, Chao & Lewis 2016C-SCL16
    |         `--Trichosphaerium Schaudinn 1899AB19, AS12
    |              |--T. platyxyrumC-SCL16
    |              `--T. sieboldiC-SCL16 [incl. Pachymyxa hystrixG84]
    |--Echinamoebida [Echinamoebia]C-SCL16
    |    |  i. s.: ‘Hartmannella’ vermiformisBY03
    |    |--Vermamoeba [Vermamoebidae]C-SCL16
    |    |    `--V. vermiformisC-SCL15
    |    `--Echinamoebidae [Echinamoeboidea]C-SCL16
    |         |--Micriamoeba tesserisC-SCL16, AB19
    |         `--EchinamoebaAS12
    |              |--E. exundansBY03
    |              |--E. gingivalisC-SC03
    |              |--E. silvestrisBY03
    |              `--E. thermarum Baumgartner, Yapi et al. 2003BY03
    `--ElardiaAB19
         |--Leptomyxida [Leptomyxia, Leptomyxoidea]C-SCL16
         |    |--Gephyramoeba [Gephyramoebidae]C-SCL16
         |    |    `--G. delicatulaLB90
         |    `--LeptomyxidaeC-SCL16
         |         |--Leptomyxa reticulataSN05
         |         `--+--Rhizamoeba saxonicaSN05
         |            `--Flabellulidae [Flabellulina]C-SCO04
         |                 |--FlabellulaSN05
         |                 `--ParaflabellulaSN05
         |                      |--P. hoguaeSN05
         |                      `--P. reniformisSN05
         `--EulobosiaC-SCL16
              |--ArcellinidaC-SCL16
              `--EuamoebidaAS12
                   |--Nolandella Page 1980C-SCL16, AS12 [Nolandellidae, Nolandina, Poseidonida]
                   |    `--N. abertawensis [=Hartmannella abertawensis]C-SCL16
                   `--Amoebina [Amoeboidea, Chaidae, Chaosidae, Hartmannellinae, Tubulinida]C-SCL16
                        |--Hartmannellidae [Copromyxaceae, Copromyxida, Copromyxidae]C-SCL16
                        |    |  i. s.: CashiaC-SCL16
                        |    |         Copromyxella Raper. Worley & Kurzynski 1978KC01
                        |    |--PtolemebaC-SCL16
                        |    `--+--+--Hartmannella cantabrigiensisC-SCL16
                        |       |  `--Copromyxa Zopf 1884C-SCL16, KC01
                        |       |       `--C. proteaC-SCL16
                        |       `--+--Glaeseria miraC-SCL16
                        |          `--SaccamoebaC-SCL16
                        |               |--S. limaxSN05
                        |               `--S. stagnicolaLB90
                        `--AmoebidaeC-SCL16
                             |  i. s.: PolychaosC-SCL16
                             |         ParachaosC-SCL16
                             |         Trichamoeba villosaC-SCL16, LB90
                             |         DeuteramoebaC-SCL16
                             |         HydramoebaC-SCL16
                             |--Chaos Linné 1767C-SCL16, LT64 [Chaosina]
                             |    |--C. diffluensLT64
                             |    `--C. nobileSN05
                             `--+--‘Amoeba’ leningradensisC-SCL16
                                `--+--‘Chaos’ carolinenseC-SCL16
                                   `--Amoeba Ehrenberg 1830C-SCL16, LT64 [=Amiba Bory de St. Vincent 1822LT64]
                                        |--A. albidaV63
                                        |--A. berylliferaV63
                                        |--A. botryllisV63
                                        |--A. cavicola Varga 1963V63
                                        |--A. dubiaLG91
                                        |--A. flavescensG89
                                        |--A. fluidaG89
                                        |--A. gorgoniaV63
                                        |--A. guttulaG84
                                        |--A. limaxSX97
                                        |--A. primaG89
                                        |--A. proteusSN05
                                        |--A. quadrilineataG84
                                        |--A. radiosa Ehrenberg 1838W86
                                        |--A. tentaculata (Gruber 1881)C-SCL16
                                        |--A. verrucosa Ehrenberg 1838W86
                                        |--A. vespertilisSX97
                                        `--A. villosa Wallich 1863W86

*Type species of generic name indicated

References

[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.

[BY03] Baumgartner, M., A. Yapi, R. Gröbner-Ferreira & K. O. Stetter. 2003. Cultivation and properties of Echinamoeba thermarum n. sp., an extremely thermophilic amoeba thriving in hot springs. Extremophiles 7: 267–274.

Bonner, J. T. 1982. Evolutionary strategies and developmental constraints in the cellular slime molds. American Naturalist 119 (4): 530–552.

Brieland, J. K., J. C. Fantone, D. G. Remick, M. LeGendre, M. McClain & N. C. Engleberg. 1997. The role of Legionella pneumophila-infected Hartmannella vermiformis as an infectious particle in a murine model of Legionnaire’s disease. Infection and Immunity 65 (12): 5330–5333.

[C-SC03] Cavalier-Smith, T., & E. E.-Y. Chao. 2003. Phylogeny of Choanozoa, Apusozoa, and other Protozoa and early eukaryote megaevolution. Journal of Molecular Evolution 56: 540–563.

[C-SCL15] Cavalier-Smith, T., E. E. Chao & R. Lewis. 2015. Multiple origins of Heliozoa from flagellate ancestors: new cryptist subphylum Corbihelia, superclass Corbistoma, and monophyly of Haptista, Cryptista, Hacrobia and Chromista. Molecular Phylogenetics and Evolution 93: 331–362.

[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.

Chapman-Andresen, C. 1971. Biology of the large amoebae. Annual Review of Microbiology 25: 27–48.

Gągola, M., W. Kłopocka, A. Grębecki & R. Makuch. 2003. Immunodetection and intracellular localization of caldesmon-like proteins in Amoeba proteus. Protoplasma 222: 75–83.

[G84] Gruber, A. 1884. Die Protozoen des Hafens von Genua. Verhandlungen der Kaiserlichen Leopoldinisch-Carolinischen Deutschen Akademie der Naturforscher [Nova Acta Academiae Caesareae Leopoldino-Carolinae Germanicae Naturae Curiosorum] 46 (4): 473–539, pls 7–11.

[G89] Gruber, A. 1889. Ueber einige Rhizopoden aus dem Genueser Hafen. Berichte der Naturforschenden Gesellschaft zu Freiburg I. B. 4: 33–44, pl. 31.

[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).

[LG91] Li, W.-H., & D. Graur. 1991. Fundamentals of Molecular Evolution. Sinauer: Sunderland (MA).

[LT64] Loeblich, A. R., Jr & H. Tappan. 1964. Sarcodina: chiefly “thecamoebians” and Foraminiferida. In: Moore, R. C. (ed.) Treatise on Invertebrate Paleontology pt C. Protista 2 vol. 1. The Geological Society of America and The University of Kansas Press.

[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.

Minassian, I., & L. G. E. Bell. 1976. Studies on changes in the nuclear helices of Amoeba proteus during the cell cycle. J. Cell Sci. 20: 273–287.

Nesom, M., & L. S. Olive. 1972. Copromyxa arborescens, a new cellular slime mold. Mycologia 64 (6): 1359–1362.

Nikolaev, S. I., E. A. D. Mitchell, N. B. Petrov, C. Berney, J. Fahrni & J. Pawlowski. 2005. The testate lobose amoebae (order Arcellinida Kent, 1880) finally find their home within Amoebozoa. Protist 156: 191–202.

Parfrey, L. W., D. J. G. Lahr & L. A. Katz. 2008. The dynamic nature of eukaryotic genomes. Molecular Biology and Evolution 25 (4): 787–794.

Smirnov, A. V., & A. V. Goodkov. 1999. An illustrated list of basic morphotypes of Gymnamoebia (Rhizopoda, Lobosea). Protistology 1: 20–29.

[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.

[SX97] Song B. & Xie P. 1997. Preliminary studies on the community structure of the planktonic protozoa from the outlet of Lake Dongting. Acta Hydrobiologica Sinica 21 (Suppl): 60–68.

[V63] Varga, L. 1963. Weitere Untersuchungen über die aquatile Mikrofauna der Baradla-Höhle bei Aggtelek (Ungarn) (Biospeologica Hungarica, XVII). Acta Zoologica Academiae Scientiarum Hungaricae 9 (3–4): 439–458.

[W86] Whitelegge, T. 1886. List of the freshwater Rhizopoda of N. S. Wales. Part I. Proceedings of the Linnean Society of New South Wales, series 2, 1 (2): 497–504.

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