TAFKAMI Walks

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).

There's been a couple of really interesting things come through the pipeline lately. For this post, I'm not going to talk (yet) about yesterday's publication of an analysis of acanthodians that suggests that they are not a monophyletic grouping. If you want to know what that's all about, ask Adam Yates (and if you don't know what an acanthodian is, I've briefly discussed them previously). Today, I'm going to discuss another recent publication.

One of the first posts I wrote for this site (in fact, the sixth) was on an organism that I dubbed TAFKAMI, or The Amoeboid Formerly Known As Mastigamoeba invertens. This organism had been originally identified as 'Mastigamoeba invertens' when isolated in 1992, and was eventually properly described by Walker et al. (2006) as 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). Breviata is an amitochondriate, microaerobic amoeboid or amoeboflagellate (depending on life cycle stage). As explained in the previous post, 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.

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

**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.

A new paper published by Minge et al. (2009) presents a new phylogenetic analysis incorporating Breviata anathema that draws 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!

REFERENCES

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.

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.

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.

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 (2): 65-78.