Eukaryote Evolution

The study of microbial fossils involves a broad array of disciplines and covers a vast diversity of topics, of which we review a select few, summarizing the state of the art. Microbes are found as body fossils preserved in different modes and have also produced recognizable structures in the rock record (microbialites, microborings). Study of the microbial fossil record and controversies arising from it have provided the impetus for the assembly and refining of powerful sets of criteria for recognition of bona fide microbial fossils. Different types of fossil evidence concur in demonstrating that microbial life was present in the Archean, close to 3.5 billion years ago. Early eukaryotes also fall within the microbial realm and criteria developed for their recognition date the oldest unequivocal evidence close to 2.0 billion years ago (Paleoproterozoic), but Archean microfossils >3 billion years old are strong contenders for earliest eukaryotes. In another dimension of their contribution to the fossil record, microbes play ubiquitous roles in fossil preservation, from facilitating authigenic mineralization to replicating soft tissue with extracellular polymeric substances, forming biofilms that inhibit decay of biological material, or stabilizing sediment interfaces. Finally, studies of the microbial fossil record are relevant to profound, perennial questions that have puzzled humanity and science—they provide the only direct window onto the beginnings and early evolution of life; and the methods and criteria developed for recognizing ancient, inconspicuous traces of life have yielded an approach directly applicable to the search for traces of life on other worlds.

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.