Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa

Abstract

Animals and fungi independently evolved from the protozoan phylum Choanozoa, these three groups constituting a major branch of the eukaryotic evolutionary tree known as opisthokonts. Opisthokonts and the protozoan phylum Amoebozoa (amoebae plus slime moulds) were previously argued to have evolved independently from the little-studied, largely flagellate, protozoan phylum, Sulcozoa. Sulcozoa are a likely evolutionary link between opisthokonts and the more primitive excavate flagellates that have ventral feeding grooves and the most primitive known mitochondria. To extend earlier sparse evidence for the ancestral (paraphyletic) nature of Sulcozoa, we sequenced transcriptomes from six gliding flagellates (two apusomonads; three planomonads; Mantamonas). Phylogenetic analyses of 173-192 genes and 73-122 eukaryote-wide taxa show Sulcozoa as deeply paraphyletic, confirming that opisthokonts and Amoebozoa independently evolved from sulcozoans by losing their ancestral ventral groove and dorsal pellicle: Apusozoa (apusomonads plus anaerobic breviate amoebae) are robustly sisters to opisthokonts and probably paraphyletic, breviates diverging before apusomonads; Varisulca (planomonads, Mantamonas, and non-gliding flagellate Collodictyon) are sisters to opisthokonts plus Apusozoa and Amoebozoa, and possibly holophyletic; Glissodiscea (planomonads, Mantamonas) may be holophyletic, but Mantamonas sometimes groups with Collodictyon instead. Taxon and gene sampling slightly affects tree topology; for the closest branches in Sulcozoa and opisthokonts, proportionally reducing missing data eliminates conflicts between homogeneous-model maximum-likelihood trees and evolutionarily more realistic site-heterogeneous trees. Sulcozoa, opisthokonts, and Amoebozoa constitute an often-pseudopodial 'podiate' clade, one of only three eukaryotic 'supergroups'. Our trees indicate that evolution of sulcozoan dorsal pellicle, ventral pseudopodia, and ciliary gliding (probably simultaneously) generated podiate eukaryotes from Malawimonas-like excavate flagellates.

Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus?

“…In one of them, glaucophytes formed a separate clade, whereas red algae and green plants grouped significantly with cryptophytes, haptophytes and katablepharids [78] (see also [74] for another interpretation). In other studies, a clade with the three Archaeplastida lineages was indeed recovered, but they still clustered significantly with haptophytes [79], cryptophytes and katablepharids [80], Palpitomonas [68], as well as with picozoans [81]. The latter study was based on the most sequence-rich data set to date, 258 nuclear-encoded proteins with 55 881 sites in total.…”

“…One way to overcome this problem is to increase the number of genes analyzed and use phylogenomic approaches based on huge data sets on a genomic scale [92]. However, even consideration of more than 40 000 sites does not always result in deep robust phylogenies for the Archaeplastida [80,87,93]. Moreover, analyses of many genetic markers are vulnerable to systematic errors, which can lead to false phylogenetic reconstructions, reflecting unreal evolutionary relationships but with high statistical support.…”

“…Some of the discrepancies observed in above-described phylogenies likely result from such missing data [96]. For example, the exclusion of missing data and a more distant excavate outgroup changed the polyphyly of Archaeplastida (grouped with a katablepharid and a cryptophyte) to monophyly [80]. However, further removing missing data resulted in weak or lack of support for the clade.…”

“…2). It should be emphasized, however, that many other phylogenies based on both smaller [84] and much larger data sets [67,80,81,[85][86][87] have high or very high support values for monophyly of glaucophytes, red algae and green algae/land plants.…”

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

“…In addition to those mentioned (the different Hacrobia), the microkingdoms include Apusomonadida and Breviatea (recently united with Opisthokonta as a new major eukaryotic grouping dubbed Obazoa) (125), Ancyromonadida (=Planomonadida), Mantamonadida, Rigifilida, and Collodictyonida (=Diphyllatea). The latter four groups appear to be deeply diverged lineages branching close to Obazoa and the supergroup Amoebozoa (126)(127)(128)(129), but their exact position is not known. Other such minor deep groups will surely be described, as their existence is suggested by culturing-independent environmental surveys of small subunit rRNA genes, such as the NAMAKO-1 and -2 lineages found in anoxic habitats (130).…”