Eukaryotic systematics: a user's guide for cell biologists and parasitologists

Abstract

Single-celled parasites like Entamoeba, Trypanosoma, Phytophthora and Plasmodium wreak untold havoc on human habitat and health. Understanding the position of the various protistan pathogens in the larger context of eukaryotic diversity informs our study of how these parasites operate on a cellular level, as well as how they have evolved. Here, we review the literature that has brought our understanding of eukaryotic relationships from an idea of parasites as primitive cells to a crystallized view of diversity that encompasses 6 major divisions, or supergroups, of eukaryotes. We provide an updated taxonomic scheme (for 2011), based on extensive genomic, ultrastructural and phylogenetic evidence, with three differing levels of taxonomic detail for ease of referencing and accessibility (see supplementary material at Cambridge Journals On-line). Two of the most pressing issues in cellular evolution, the root of the eukaryotic tree and the evolution of photosynthesis in complex algae, are also discussed along with ideas about what the new generation of genome sequencing technologies may contribute to the field of eukaryotic systematics. We hope that, armed with this user's guide, cell biologists and parasitologists will be encouraged about taking an increasingly evolutionary point of view in the battle against parasites representing real dangers to our livelihoods and lives.

A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates

“…putative SITs in two different eukaryotic supergroups, opisthokonts and stramenopiles [37]. These SIT domains are not present in any of the sequenced non-siliceous choanoflagellate species [15,17,38,39], implying a correlation between their presence and lorica biomineralization.…”

“…This organism would be equivalent to the last common ancestor of all eukaryotic supergroups [37], and therefore this hypothesis would involve the loss of all SIT homologues from all other sequenced eukaryotes. The convergent evolution of SITs in loricate choanoflagellates and siliceous stramenopiles would require not only parallel evolution of multiple SIT-specific features, but also the loss of all related or ancestral genes in all other opisthokonts and non-siliceous stramenopiles.…”

“…Biosilicification is found in isolated species or small groups in each of the eukaryotic supergroups [37]. However, current molecular evidence of differing mechanisms points towards multiple independent origins of biosilica, rather than biosilicification being present in the last common ancestor of all eukaryotes.…”

The mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae

“…Excavates are subdivided into two subgroups, Metamonada and Discoba, the latter consistently recovered in phylogenomic analyses (Hampl et al, 2009;Zhao et al, 2012). Within Metamonada, most lineages lack typical mitochondria and instead possess hydrogenosomes (e.g., Trichomonas in parabasalids) or mitosomes (e.g., Giardia in diplomonads) (Adl et al, 2012;Walker et al, 2011). In contrast, the three lineages comprising Discoba are mostly mitochondriate: Heterolobosea have a regular mitochondrion with a very gene-rich genome (e.g., Naegleria gruberi) (Gray et al, 2004), Jakobids harbour mitochondria retaining one of the highest gene complements known to date (e.g., Reclinomonas and Andalucia) (Burger et al, 2013;Lang et al, 1997), and, finally, Euglenozoa are a very diverse collection of protists, some of which are parasitic (e.g., Trypanosomatidae in kinetoplastids), others photosynthetic (e.g., euglenophytes in euglenids) or free-living heterotrophs (e.g., diplonemids).…”

“…In two recent syntheses of the phylogenetic literature, eukaryotes are considered as composed of about 6-9 major lineages, of which well-studied green plants, fungi and animals only correspond to a very small fraction (Adl et al, 2012;Walker et al, 2011). Among these major lineages excavates are a putative assemblage of (often heterotrophic) flagellates, proposed on the basis of shared morphological characters (e.g., the ventral feeding groove and associated cytoskeletal structures) and molecular data.…”