Archamoebae: The Apogee (or Nadir) of Amoebozoan Evolution

Mastigamoeba aspera, the type species of the mastigamoebids. Photo by Josef Brief.

There's just one group of amoebozoans left for me to cover: the Archamoebae. Among Amoebozoa, the Archamoebae are easily distinguishable by one significant feature - they lack mitochondria. Mitochondria are also absent in Breviata (which was initially identified as an archamoeba as a result), but Breviata has double basal bodies attached to the cilium unlike the single basal body of Archamoebae (Walker et al., 2006). Members of the Archamoebae are either freshwater amoeboflagellates or non-ciliate animal endosymbionts. Because the Archamoebae are primarily defined by a character absence some authors have suggested that their monophyly is suspect, but molecular analyses support their recognition. The lack of mitochondria also lead to Archamoebae being one of the four groups of protists (along with the Diplomonadida, Microsporidia and Parabasalia) that were grouped together as the "Archezoa", and suggested to have diverged from other eukaryotes prior to the origin of mitochondria. The archezoan hypothesis began to fall from favour in the latter half of the 1990s as relationships were proposed between various 'archezoans' and specific groups of mitochondriate protists, such as between Archamoebae and other amoebozoans. Putative mitochondrion-derived organelles such as mitosomes and/or hydrogenosomes have now been identified from most Archamoebae (Walker et al., 2001; Gill et al., 2007).

Molecular data supports the division of Archamoebae into two clades, the Mastigamoebida and Pelobiontida (Cavalier-Smith et al., 2004). Production of pseudopodia in Mastigamoebida is eruptive (Walker et al., 2001), which you may recall is not the usual condition for amoebozoans (other than Archamoebae, eruptive pseudopodium is also found in Leptomyxida). Free-living mastigamoebids are ciliate for at least part of their life cycle, and movement is generally by means of the cilium or by gliding rather than by pseudopodium production. Mastigamoebids may or may not be multinucleate, and the cilium is usually connected to the nucleus. Taxonomy of the free-living amoeboflagellate mastigamoebids is in something of a state of flux - three genera have been distinguished, Mastigamoeba, Phreatamoeba and Mastigella, but opinions differ as to whether the latter two should be distinguished from the first. Phreatamoeba balamuthi has been placed as a separate genus because of its more complex life-cycle alternating between amoeboid and amoeboflagellate stages, with the amoeboid stage predominant, but the flagellate stage is otherwise not distinguishable from Mastigamoeba. Mastigella has been distinguished based on the absence of a connection between the cilium and the nucleus, but the presence or absence of such a connection can be difficult to distinguish in taxa where the connection is very fine (Walker et al., 2001). Part of the problem lies in the genus Mastigamoeba itself - Mastigamoeba contains about forty species of which some are very distinct from each other but many (including the type species) are insufficiently studied. When more of the Mastigamoeba species are studied it may lead to the genus' subdivision.


The giant micro-aerobic amoeboid Pelomyxa palustris, with the larger cell nearly three millimetres in length. The flecks of green inside it are endosymbiotic algae. Photo from here.

The Pelobiontida contain three distinct genera, Pelomyxa, Mastigina and Entamoeba, united by molecular data. Mastigina and Pelomyxa are both free-living amoeboflagellates. Mastigina setosa has one or a few nuclei and a single long cilium; however, movement is by pseudopodia while the cilium contributes little if any propulsion. Pelomyxa palustris is a gigantic amoeboid, up to five millimetres long and often with hundreds of nuclei in a single cell. It possesses small cilia, but it almost goes without saying that they do not contribute to moving the cell's massive bulk. Cytoplasmic movement in Pelomyxa has been described as "fountain streaming" - a wave of cytoplasm moves across the dorsal surface of the cell and spills over the front. Like Trichosphaerium, Pelomyxa can reproduce by budding off a piece of the cell with a few nuclei (Hickson, 1909) - indeed, at one point it was thought that Pelomyxa never underwent mitosis, an error that lead to its brief elevation to the status of an independent phylum, Caryoblastea.

Both of the two archamoebaen clades have given rise to non-ciliate lineages - the Endolimacidae (Endolimax and Endamoeba) among mastigamoebids, and Entamoeba among pelobionts. Both of these taxa are animal endosymbionts, living inside the gut of their host (the name Endolimax means "inner slug") - Endolimax and Entamoeba inhabit vertebrates (including humans), while Endamoeba is found in cockroaches (including termites). Endolimacidae are generally innocuous, but a few species of Entamoeba can cause great trouble for their hosts - among humans, E. histolytica causes dysentery, while E. gingivalis lives in the mouth and can cause gum disease.


Endamoeba blattae, an inhabitant of the digestive system of cockroaches. Photo from here.

Even with the downfall of the idea that Archamoebae are among the most archaic of eukaryotes (which kind of makes the name of clade a bit misleading, but we're stuck with it now), the relationships of this group are still interesting. Archamoebae possess a distinct conical arrangement of microtubules at the base of the cilium; in turn, this cone sits on top of the nucleus like a Vietnamese farmer's hat. The presence of a similar structure in many slime moulds lead Cavalier-Smith to unite Archamoebae and Mycetozoa in a clade called Conosa (or Conosea, depending on which paper you're reading and what rank Cavalier-Smith felt like putting it at at the time). Molecular data generally supports placing the two close together, but not always as an exclusive clade - often various examples of the taxa described in the last post muscle their way in. Many of these other amoebozoans, such as Phalansterium and Multicilia, possess similar (but not identical) microtubular cones, and Cavalier-Smith (2009) recently extended the Conosa to include these taxa as well. This extended Conosa is supported by most molecular analyses, but it has to be noted that all of the taxa involved show elevated rates of evolution - Pelomyxa and Trichosphaerium, in particular, show rates going through the roof - and the possibility of long-branch attraction cannot be entirely ruled out. If I may be allowed a somewhat strained analogy, it's a bit like when an election is held in a culturally diverse area between candidates of various backgrounds and both sexes, and all the winning candidates end up belonging to one particular subgroup. It's entirely possible that this was the valid result, and nothing untoward occurred in the ballot-counting process, but still, you can't help wondering.

And with that, I reach the end of the Amoebozoa (at least for now). If you want to look back on the other amoebozoan posts:

General Amoebozoa: Putting the Formless in Formation.
Breviata anathema: TAFKAMI; TAFKAMI Walks.
Tubulinea: The Paragons of Amoeboids; Amoeba: Much Wierder than You Think.
Discosea: Keeping a Low Profile.
Mycetozoa: The Diversity of Slime Moulds.
Various Amoebozoa incertae sedis ('Variosea'): Amoebozoan Oddments.

Now if only someone would do the same for Heterolobosea...

REFERENCES

Cavalier-Smith, T. 2009. Megaphylogeny, cell body plans, adaptive zones: causes and timing of eukaryote basal radiations. Journal of Eukaryotic Microbiology 56 (1): 26-33.

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 (1): 21-48.

Gill, E. E., S. Diaz-Triviño, M. J. Barberà, J. D. Silberman, A. Stechmann, D. Gaston, I. Tamas & A. J. Roger. 2007. Novel mitochondrion-related organelles in the anaerobic amoeba Mastigamoeba balamuthi. Molecular Microbiology 66 (6): 1306–1320

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

Walker, G., A. G. B. Simpson, V. Edgcomb, M. L. Sogin & D. J. Patterson. 2001. Ultrastructural identities of Mastigamoeba punctachora, Mastigamoeba simplex and Mastigella commutans and assessment of hypotheses of relatedness of the pelobionts (Protista). European Journal of Protistology 37 (1): 25-49.