Root of the Eukaryotic Tree of Life

While it has become quite clear that the last eukaryotic common ancestor (LECA) was a bikont, i.e. had two anterior cilia to move around (as I wrote previously), it now seems that the LECA wasn't only a bikont, but also an excavate. Excavates are one of the five main groups of eukaryotes (Adl et al.2012) having ancestrally two cilia and a ventral feeding groove. Excavates include for example Trichomonas (Parabasalia), Giardia (Fornicata), Euglenozoa (e.g. Euglena, Trypanosoma), Heterolobosea, Jakobida (latter three belonging to Discoba), and Malawimonas, but it has turned out that they might not form a monophyletic group that seemed quite likely in 2009 (Hampl et al. 2009). In my previous post I treated excavates as monophyletic and avoided discussing them, although I was aware of some problems. Particularly, Malawimonas, which is structurally a typical excavate (possessing two cilia with a characteristic ciliary apparatus and a ventral feeding groove; Simpson, 2003) did not want to group very well with other excavates in phylogenomic analyses (Rodríguez-Ezpeletaet al. 2007; Derelle & Lang, 2012; Zhao et al. 2013; Brown et al. 2013). I thought perhaps the data was incomplete to make a big deal about this. Now it looks pretty clear (Cavalier-Smith et al. 2014; 2015; Derelle et al. 2015) that Malawimonas is more closely related to unikont/Opimoda branch (amoebae, animals, fungi and others; Fig. 1) than to (most) other excavates. Interestingly, phylogenomic analyses by Cavalier-Smith et al. (2014; 2015) reveal that excavate groups Parabasalia, Fornicata, and Preaxostyla might also be more closely related to unikonts than to Discoba (Euglenozoa, Heterolobosoa, and Jakobida). Parabasalia, Fornicata, and Preaxostyla are classified under Metamonada, who are all anaerobic or microaerophilic and lack typical respiratory mitochondria. Many of them are parasites or symbionts of animals. Unfortunately most of them are fast evolving, making it difficult to place them in phylogenetic analyses, particularly Trichomonas and Giardia for which full genomes are available. It would be necessary to obtain additional genome scale data for more slowly evolving free-living species from groups like Dysnectes and Carpediemonas (Takishita et al. 2012) to place representatives of Metamonada among eukaryotes more reliably.

Figure 1. Phylogeny of eukaryotes updated from my previous post mainly on the basis of Cavalier-Smith et al. (2014; 2015) and Derelle et al. (2015) papers. Although since 2010, Cavalier-Smith prefers to root the tree between Euglenozoa (member of Discoba) and other eukaryotes, the rooting found by Derelle et al. (2015) is more reliable, because it is based on large number of mitochondrial and other bacterial genes for which there are closer out-groups available than for genes of archaeal origin (see for example the rooting found by Lasek-Nesselquist& Gogarten, 2013 which fits Cavalier-Smith's scenario). Cavalier-Smith (2010; 2013) lists some genomic characters that appear to be ancestral (i.e. shared with prokaryotes) in Euglenozoa but derived in other eukaryotes. The problem is that full genome sequences are available only for few fast evolving and mostly parasitic Euglenozoa and other excavates, which makes these kinds of lists highly speculative.

If the rooting of the eukoryote tree (Fig. 1) is correct, then it really seems that the LECA might have been quite similar to a typical excavate like Malawimonas or a jakobid (e.g. Jakoba, Reclinomonas, Andalucia). This scenario finds support also from some alveolates (e.g. Colponema) that are structurally quite similar to excavates (Tikhonenkov et al. 2014; Cavalier-Smith et al. 2014). Apparently, Colponema, Acavomonas and many other similar undescribed groups (Janouškovecet al. 2013; Tikhonenkov et al. 2014) are phylogenetically diverse bunch that are variously related to, but clearly outside of the three main groups of alveolates (ciliates, apicomplexans, and dinoflagellates).

References

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Brown MW, Sharpe SC, Silberman JD, Heiss AA, Lang BF, Simpson AGB, Roger AJ (2013) Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proceedings. Biological sciences / The Royal Society 280 (1769): 20131755. doi: 10.1098/rspb.2013.1755

Cavalier-Smith T (2010) Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biology letters 6: 342–345. doi: 10.1098/rsbl.2009.0948

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Cavalier-Smith T, Chao EE, Lewis R (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. doi: 10.1016/j.ympev.2015.07.004

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