Amastigomonas cf. mutabilis, from Mindolina et al. (2023). Scale bar = 10 µm.

Belongs within: Amorphea.

The Apusozoa are a clade of gliding unicellular eukaryotes.

Published 5 June 2007

The organism I want to tell you about here has had rather a complicated history. Prior to its formal description, it was long present in the literature under something of a pseudonym. As a result, I’m going to dub it TAFKAMI—The Amoeba Formally Known As Mastigamoeba invertens. TAFKAMI is an anaerobic amoeboflagellate with a cilium shorter than the body.

A little backgroud, first. Protist phylogeny has always been a contentious, uncertain world – compared to multicellular organisms, unicells have relatively few obvious characters to unite various groups of taxa. However, the availability of better and better electron microscopy and the continued improvements in molecular phylogenies mean that in recent years, a growing consensus has developed that the majority of eukaryotes fall into a few large “supergroups” (Simpson & Roger, 2004)—the opisthokonts (including fungi and animals), amoebozoans, excavates (mostly flagellates), rhizarians (including radiolarians and foraminiferans), chromalveolates (including ciliates, brown algae and dinoflagellates) and plants (including green and red algae). There are still a few random taxa that don’t necessarily fall into any of these groups.

The supergroup Amoebozoa includes the majority of amoebae with lobose pseudopodia, as well as most slime moulds and the Archamoebae, a group of amitochondriate anaerobic amoebae (take a moment to appreciate the assonance). The Archaemoebae include Mastigamoeba proper (as well as Entamoeba, the causative organism of amoebic dysentery).

According to Walker et al. (2006), TAFKAMI was first isolated back in 1992. Since then, it has been what is technically referred to as a right pain in the khyber. Comparisons using both microscope and molecular techniques between TAFKAMI and other supposedly related organisms increasingly indicated that it was not Mastigamoeba or any other known amoeba. In molecular studies (such as Cavalier-Smith & Chao 2003a) TAFKAMI leapt about madly, sometimes with amoebozoans, sometimes with apusomonads (another small group that doesn’t fit into any of the supergroups), sometimes entirely elsewhere.

Walker et al. (2006) recently established TAFKAMI as a new taxon, Breviata anathema* (the real Mastigamoeba invertens is known only from an undiagnostic description published in 1892, and, short of someone inventing a time machine so that they can look over its original describer’s shoulder, will probably never be identifiable). They also presented a detailed comparison of Breviata with the main contenders for close relationship.

*Tragically, Walker et al. (2006) gave no etymology for the new name. I have always wondered what exactly is so anathematic about Breviata anathema.

As explained above, Breviata has proven to be an obscenely difficult organism to place phylogenetically. Its position in phylogenetic analyses has been very unstable, and it jumps wildly about depending on the analysis parameters. The earliest division in eukaryotes appears to be between unikonts (animals, fungi and amoebozoans, which have a single flagellum with a single basal body) and bikonts (including plants, algae and excavates, with flagella in doublets or with double basal bodies), and it has not even been conclusively established whether Breviata is a unikont or a bikont. It has a single flagellum like a unikont, but two basal bodies attached to that flagellum like a bikont*, and sturdy branching filose pseudopodia like nothing else. Whatever its position, it seems likely that the divergence of Breviata from other eukaryotes happened not long after the the origin of crown eukaryotes in total.

**Just to confuse matters, there are unikonts with double basal bodies, and bikonts with single flagella. However, bikonts with single flagella always retain two basal bodies. The anterior basal body in bikonts is always the younger of the two, and when the posterior basal body dies off the anterior body moves to the back and a new basal body grows in front of it. Those unikonts with two basal bodies still lack this distinctive growth pattern. Unfortunately, the flagellar growth pattern has not yet been studied for Breviata.

Cavalier-Smith et al. (2004) felt that TAFKAMI was the basalmost member of the Amoebozoa, placing it in its own class Breviatea. The main reason for doing so was that TAFKAMI was supposed to possess a single ciliary basal body (the organelle that the flagellum emerges from). However, Walker et al. found that Breviata actually had double basal bodies. There is reasonably good evidence (Cavalier-Smith, 2002; Simpson & Rogers, 2004) that eukaryotes with double basal bodies form a single über-clade, the bikonts (including the excavates, rhizarians, chromalveolates and plants). It seems quite believable that Breviata is a member of this clade. Breviata also lacks the molecular markers of Amoebozoa proper (Cavalier-Smith et al., 2004).

Under certain parameters, molecular phylogenies supported an association of Breviata with the afore-mentioned apusomonads, which are also bikonts. Breviata also has similar pseudopodia to apusomonads. However, I would be just as sceptical of a direct apusomonad-Breviata connection. At the present, I don’t feel that Breviata can be placed as anything more that “basal bikont”. (It is worth noting, too, that one amoebozoan group, the Myxogastrea, has independently evolved double basal bodies.)

Perhaps most interestingly, Walker et al. identified a large organelle overlying the nucleus that they suggested as a possible hydrogenosome. Hydrogenosomes are respiratory organelles that are generally regarded as having been independently derived from mitochondria in a number of anaerobic groups. As such, Breviata potentially joins the growing list of supposedly amitochondriate taxa retaining mitochondrial remnants.

Published 16 January 2009
Various individuals of the amoeboflagellate Breviata anathema. Note particularly the extended anterior and posterior pseudopodia on numbers 13, 14 and 18. Figure from Walker et al. (2006).

A more recent paper by Minge et al. (2009) presented a new phylogenetic analysis incorporating Breviata anathema that drew on 17,283 nucleotide sites from no less than 78 genes (for contrast, the analysis of Breviata by Walker et al. used 1274 sites). The results of this analysis place Breviata with the amoebozoans, the clade including the majority of amoeboids with lobose pseudopodia. The support for this result is actually not too bad for this high a level of evolutionary divergence. Under certain analytical parameters, Breviata fell within other amoebozoans as sister to the other amitochondriate amoeboids Entamoeba and Mastigamoeba proper, but in the majority of cases it was the sister group to all other amoebozoans. This seems the more likely option as Breviata lacks certain sequence signatures (including a small insertion) characteristic of other Amoebozoa.

Sadly, as interesting as this result is, and as impressive as the amount of data used is, the analysis of Minge et al. (2009) suffers a fatal flaw. Though the analysis by Walker et al. did not give a conclusive result, the position they suggested to be most likely for Breviata was as sister to the Apusozoa. Apusozoans are a small group of flagellates with doubled flagella, and have been suggested to represent the basalmost divergence in the bikont lineage. As well as the double basal bodies, Apusozoa also produce filose pseudopodia like Breviata. Unfortunately, due to lack of data, the analysis by Minge et al. (2009) doesn’t include a single apusozoan. While I’m personally sceptical of an apusozoan-Breviata relationship, I do think that without their inclusion the results of Minge et al. can’t really be taken as conclusive.

Even if the phylogenetic results can’t be entirely trusted, Minge et al. (2009) do have some interesting things to say. One of the interesting results from Walker et al. (2006) was the identification in Breviata of what appeared to be a hydrogenosome. Hydrogenosomes are hydrogen-processing organelles found in a number of anaerobic eukaryotes that have been shown to be altered mitochondria (Akhmanova et al., 1998). If Breviata did have a hydrogenosome, that would add to an increasing amount of evidence that all of the various ‘amitochondriate’ eukaryotes living today actually descend from ancestors that once had mitochondria (in contrast to previous opinions that they diverged from other eukaryotes prior to the origin of mitochondria). Among the genes possessed by Breviata, Minge et al. identify a number of genes derived from the pre-mitochondrial endosymbiont, confirming that Breviata‘s lack of mitochondria is a secondary feature.

Finally, there is the way Breviata moves. Amoeboids move, of course, by the extension of pseudopodia, but the exact method by which pseudopodia are produced can differ significantly between taxa. Indeed, in organisms with few permanent morphological features, the mode of pseudopodium formation has turned out to have a fair amount of phylogenetic significance (Smirnov et al., 2005). With its unique phylogenetic position, it seems only fitting that Breviata should have a unique mode of movement—it walks. A pseudopodium is protruded from the front of the cell and attached to the substrate. The rest of the cell body then rolls forward over the attached pseudopodium (like a tractor on treads, is Minge et al.‘s analogy), until the pseudopodium is left trailing behind before being retracted and another pseudopod is extended from the front to repeat the process. No other organism has a mode of movement like Breviata—always twirling, twirling, twirling towards the future!

Systematics of Apusozoa
Apusozoa [Thecomonadea]
| |--Subulatomonas tetrasporaAS12, C-SCL15
| |--Pygsuia biforma Brown et al. 2013AB19
| |--LenisiaAB19
| `--Breviata Walker, Dacks & Embley 2006C-SCL15, WDE06 [Breviatida]
| `--*B. anathema Walker, Dacks & Embley 2006WDE06
| i. s.: PodomonasAS12
| ChelonemonasAB19
|--Multimonas mediaC-SCL15
|--Apusomonas Alexieff 1924 [incl. Rostromonas Karpov & Zhukov 1980]C-S93
| `--A. proboscideaC-SC03
|--Thecamonas Larsen & Patterson 1990C-S93
| |--T. oxoniensisC-SCL15
| `--+--T. trahens Larsen & Patterson 1990C-SCL15, AB19 [=Amastigomonas trahensC-SC03]
| `--Manchomonas bermudensisC-SCL15
`--Amastigomonas de Saedeleer 1931C-S93
|--A. bermudensisC-SC03
|--A. debruyneiC-SC03
|--A. filosaC-SC03
|--A. marinaS-TE06
`--A. mutabilisC-SC03

*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.

Akhmanova, A., F. Voncken, T. van Alen, A. van Hoek, B. Boxma, G. Vogels, M. Veenhuis & J. H. P. Hackstein. 1998. A hydrogenosome with a genome. Nature 396: 527-528.

[C-S93] Cavalier-Smith, T. 1993. The protozoan phylum Opalozoa. Journal of Eukaryotic Microbiology 40 (5): 609–615.

Cavalier-Smith, T., & E. E.-Y. Chao. 2003a. Molecular phylogeny of centrohelid Heliozoa, a novel lineage of bikont eukaryotes that arose by ciliary loss. Journal of Molecular Evolution 56 (4): 387–396.

[C-SC03] Cavalier-Smith, T., & E. E.-Y. Chao. 2003b. 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-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.

Minge, M. A., J. D. Silberman, R. J. S. Orr, T. Cavalier-Smith, K. Shalchian-Tabrizi, F. Burki, Å. Skjæveland & K. S. Jakobsen. 2009. Evolutionary position of breviate amoebae and the primary eukaryote divergence. Proceedings of the Royal Society of London B 276: 597–604.

[S-TE06] Shalchian-Tabrizi, K., W. Eikren, D. Klaveness, D. Vaulot, M. A. Minge, F. Le Gall, K. Romari, J. Throndsen, A. Botnen, R. Massana, H. A. Thomsen & K. S. Jakobsen. 2006. Telonemia, a new protist phylum with affinity to chromist lineages. Proceedings of the Royal Society of London Series B—Biological Sciences 273: 1833–1842.

Simpson, A. G. B., & A. J. Roger. 2004. The real ‘kingdoms’ of eukaryotes. Current Biology 14 (17): R693–R696.

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.

[WDE06] Walker, G., J. B. Dacks & T. M. Embley. 2006. Ultrastructural description of Breviata anathema n. gen., n. sp., the organism previously studied as “Mastigamoeba invertens”. Journal of Eukaryotic Microbiology 53: 65–78.

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