Myosin domain evolution and the primary divergence of eukaryotes

Eukaryotic cells have two contrasting cytoskeletal and ciliary organizations. The simplest involves a single cilium-bearing centriole, nucleating a cone of individual microtubules (probably ancestral for unikonts: animals, fungi, Choanozoa and Amoebozoa). In contrast, bikonts (plants, chromists and all other protozoa) were ancestrally biciliate with a younger anterior cilium, converted every cell cycle into a dissimilar posterior cilium and multiple ciliary roots of microtubule bands. Here we show by comparative genomic analysis that this fundamental cellular dichotomy also involves different myosin molecular motors. We found 37 different protein domain combinations, often lineage-specific, and many previously unidentified. The sequence phylogeny and taxonomic distribution of myosin domain combinations identified five innovations that strongly support unikont monophyly and the primary bikont/unikont bifurcation. We conclude that the eukaryotic cenancestor (last common ancestor) had a cilium, mitochondria, pseudopodia, and myosins with three contrasting domain combinations and putative functions. A parting of the ways Myosin is fundamentally important for muscle and much other cell motility in eukaryotes, so it goes back a long way. A survey of myosin types in 23 complete or near-complete genomes throws new light on the evolution of the eukaryote lineage. The probable last common ancestor is identified as a cell with a single cilium, mitochondria and pseudopodia, and myosins with three different domain combinations and functions. From there the eukaryotes diverged into bikonts and unikonts, named for the number of cilia- or flagella-like structures they possess.