Evidence of taxa-, clone-, and kin-discrimination in protists: ecological and evolutionary implications

Abstract

Unicellular eukaryotes, or protists, are among the most ancient organisms on Earth. Protists belong to multiple taxonomic groups; they are widely distributed geographically and in all environments. Their ability to discriminate among con- and heterospecifics has been documented during the past decade. Here we discuss exemplar cases of taxa-, clone-, and possible kin-discrimination in five major lineages: Mycetozoa (Dictyostelium, Polysphondylium), Dikarya (Saccharomyces), Ciliophora (Tetrahymena), Apicomplexa (Plasmodium) and Archamoebae (Entamoeba). We summarize the proposed genetic mechanisms involved in discrimination-mediated aggregation (self versus different), including the csA, FLO and trg (formerly lag) genes, and the Proliferation Activation Factors (PAFs), which facilitate clustering in some protistan taxa. We caution about the experimental challenges intrinsic to studying recognition in protists, and highlight the opportunities for exploring the ecology and evolution of complex forms of cell-cell communication, including social behavior, in a polyphyletic, still superficially understood group of organisms. Because unicellular eukaryotes are the evolutionary precursors of multicellular life, we infer that their mechanisms of taxa-, clone-, and possible kin-discrimination gave origin to the complex diversification and sophistication of traits associated with species and kin recognition in plants, fungi, invertebrates and vertebrates.

Kin Discrimination in Protists: From Many Cells to Single Cells and Backwards

“…). This single‐gene‐mediated example of behavioral modulation, among only those carrying FLO1 , is consistent with the recognition alleles model (above) in which a single gene promotes cooperation toward other carriers of the gene even if they are non‐kin (Espinosa and Paz‐y‐Miño‐C ).…”

“…Recent studies with unicellular eukaryotes (protists) have uniquely enriched the field of kin recognition, particularly after characterizing the genes involved in discrimination‐mediated aggregation (mostly for flocculation or biofilm‐like formation, starvation‐triggered dormancy, or reproduction; below) or in clone‐versus‐clone competition to colonize hosts in parasitic taxa (Espinosa and Paz‐y‐Miño‐C ). The last decade of kin recognition studies with protists has focused on the molecular biology and genetics of cell–cell discrimination and kin recognition abilities in Saccharomyces , Dictyostelium , Polysphondylium , Tetrahymena , Entamoeba and Plasmodium (Table ; Espinosa and Paz‐y‐Miño‐C ). Here we review these studies succinctly and remark on the type of scientific progress (i.e.…”

“… Entamoeba Proliferation Activating Factors EPAFs; Espinosa and Paz‐y‐Miño‐C (,b). Our lab has identified six putative cell‐signals excreted by the amebas (RasGap/Ankyrin, coronin‐WD40, actin, protein kinases, heat shock 70, and ubiquitin) and which known functions in Entamoeba spp.…”

“…Direct substantiation of specific genes involved in cell–cell discrimination or kin recognition came during the 2000s, from experiments with protists, particularly the common yeast Saccharomyces cerevisiae (Dikarya) and the social ameba Dictyostelium discoideum (Mycetozoa; Table ; Espinosa and Paz‐y‐Miño‐C ). As follows:…”

A Combinatorial Kin Discrimination System in Bacillus subtilis

“…Cooperation is inherent to multicellularity, and kin discrimination has been reported in a variety of multicellular eukaryotes [3]. Bacteria also exhibit kin discrimination-like behavior, in particular while engaged in swarming, a form of multicellularity in which cells hyperflagellate and group together to rapidly spread across surfaces [4].…”