Evolution and Classification of Myosins, a Paneukaryotic Whole-Genome Approach

Abstract

Myosins are key components of the eukaryotic cytoskeleton, providing motility for a broad diversity of cargoes. Therefore, understanding the origin and evolutionary history of myosin classes is crucial to address the evolution of eukaryote cell biology. Here, we revise the classification of myosins using an updated taxon sampling that includes newly or recently sequenced genomes and transcriptomes from key taxa. We performed a survey of eukaryotic genomes and phylogenetic analyses of the myosin gene family, reconstructing the myosin toolkit at different key nodes in the eukaryotic tree of life. We also identified the phylogenetic distribution of myosin diversity in terms of number of genes, associated protein domains and number of classes in each taxa. Our analyses show that new classes (i.e., paralogs) and domain architectures were continuously generated throughout eukaryote evolution, with a significant expansion of myosin abundance and domain architectural diversity at the stem of Holozoa, predating the origin of animal multicellularity. Indeed, single-celled holozoans have the most complex myosin complement among eukaryotes, with paralogs of most myosins previously considered animal specific. We recover a dynamic evolutionary history, with several lineage-specific expansions (e.g., the myosin III-like gene family diversification in choanoflagellates), convergence in protein domain architectures (e.g., fungal and animal chitin synthase myosins), and important secondary losses. Overall, our evolutionary scheme demonstrates that the ancestral eukaryote likely had a complex myosin repertoire that included six genes with different protein domain architectures. Finally, we provide an integrative and robust classification, useful for future genomic and functional studies on this crucial eukaryotic gene family.

Functions of myosin motors tailored for parasitism

“…Initially, TgMyoJ and TgMyoK were grouped in the class of retrograde myosin VI [3]. A more recent phylogenetic analysis has reclassified these two proteins into class XXIII [5]. However this finding is not supported by the phylogenetic analysis presented here, in which class VI clearly groups outside of the class XXIII/ XXIV cluster (Figure 3).…”

“…Several phylogenetic analyses of myosin motors have led to their classification and the reconstruction of their evolutionary diversification [3][4][5]. The apicomplexan myosins were placed into several distinct classes encompassing myosins from other systematic lineages (classes VI, XXII, XXIII, XXIV).…”

Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites

“…Among the known chitin synthase genes, one is restricted to fungi, known as the division II chitin synthases (25). Moreover, only fungi possess a chitin synthase gene with a myosin domain-the class V, division II chitin synthases (26)-with the exception of the choanozoan Corallochytrium limacisporum (27). The myosin motor domain of the chitin synthase is believed to function by depositing chitin at particular regions of the plasma membrane via the cytoskeletal highway and is associated with polarized secretion and apical growth in fungi (28).…”

Myosin-independent cytokinesis in Giardia utilizes flagella to coordinate force generation and direct membrane trafficking

“…Hence, the use of myosin II may be implemented on top of a more ancient mechanism that is dependent on cortical tension and a Laplace-like pressure property of cells that serves to minimize the surface area-to-volume ratio (18,19). Moreover, phylogenetic distribution of myosin II is limited to Unikonts with one known exception that may be an example of horizontal gene transfer (20,21); thus, three of the five eukaryotic supergroups use an alternative to the canonical "purse-string" mechanism of cytokinesis, as is the case in plants (22). The number and types of alternative mechanisms remain understudied (23), especially in cells that have been difficult to culture and for which molecular and imaging methodologies are lacking.…”