New insights into myosin evolution and classification

Abstract

Myosins are eukaryotic actin-dependent molecular motors important for a broad range of functions like muscle contraction, vision, hearing, cell motility, and host cell invasion of apicomplexan parasites. Myosin heavy chains consist of distinct head, neck, and tail domains and have previously been categorized into 18 different classes based on phylogenetic analysis of their conserved heads. Here we describe a comprehensive phylogenetic examination of many previously unclassified myosins, with particular emphasis on sequences from apicomplexan and other chromalveolate protists including the model organism Toxoplasma, the malaria parasite Plasmodium, and the ciliate Tetrahymena. Using different phylogenetic inference methods and taking protein domain architectures, specific amino acid polymorphisms, and organismal distribution into account, we demonstrate a hitherto unrecognized common origin for ciliate and apicomplexan class XIV myosins. Our data also suggest common origins for some apicomplexan myosins and class VI, for classes II and XVIII, for classes XII and XV, and for some microsporidian myosins and class V, thereby reconciling evolutionary history and myosin structure in several cases and corroborating the common coevolution of myosin head, neck, and tail domains. Six novel myosin classes are established to accommodate sequences from chordate metazoans (class XIX), insects (class XX), kinetoplastids (class XXI), and apicomplexans and diatom algae (classes XXII, XXIII, and XXIV). These myosin (sub)-classes include sequences with protein domains (FYVE, WW, UBA, ATS1-like, and WD40) previously unknown to be associated with myosin motors. Regarding the apicomplexan ''myosome,'' we significantly update class XIV classification, propose a systematic naming convention, and discuss possible functions in these parasites.Apicomplexa ͉ Chromalveolata

Powering membrane traffic in endocytosis and recycling

“…Dictyostelium discoideum MyoM contains a Rac guaninenucleotide exchange factor domain that has a PH subdomain 134 and associates with macropinocytic structures 135 . Last, genome mining revealed a human myosin that contains a FYVE domain that is thought to interact with endosomal phosphatidylinositol-3-phosphate 136 .…”

Myosin XI-K Is Required for Rapid Trafficking of Golgi Stacks, Peroxisomes, and Mitochondria in Leaf Cells of Nicotiana benthamiana

“…Evolution of myosins involved a complex history of lineage-specific duplications, such that the myosin superfamily is subdivided into as many as 37 classes (Richards and Cavalier-Smith, 2005;Foth et al, 2006). The angiosperms have two classes of myosins, VIII and XI, with the latter being the largest.…”

Molecular dissection of host cell invasion by the Apicomplexans: the glideosome

“…The T. gondii possesses the largest repertoire for each of the three types of motors found in any apicomplexan to date: 10 genes giving rise to at least 11 myosin heavy chains and 15 and 10 genes encode kinesin and dynein heavy chains, respectively. Phylogenetic analysis of the conserved head domains groups six T. gondii myosins into the alveolate-specific class XIV, two into the wellknown class VI, and one sequence each into the newly described myosin classes XXII, XXIII, and XXIV (Foth et al, 2006). We have showed that TgMyoD exhibits the same kinetics properties as TgMyoA but a conventional knockout has established that this motor does not play a significant role in motility of tachyzoites.…”

“…1). Our recent phylogenetic analysis of the repertoire of myosins in Apicomplexa and in others protozoans led us to postulate that other motors could potentially contribute to gliding motility (Foth et al, 2006) given the fact that T. gondii tachyzoites exhibit three distinct modes of motility (Hakansson et al, 1999). The T. gondii possesses the largest repertoire for each of the three types of motors found in any apicomplexan to date: 10 genes giving rise to at least 11 myosin heavy chains and 15 and 10 genes encode kinesin and dynein heavy chains, respectively.…”

“…TgMyoB and TgMyoC are encoded by two alternatively spliced products of the same gene and are thought to be involved in cell division (Delbac et al, 2001;Gubbels et al, 2006). Other myosins contain protein domains such as a WD40 repeats and ATS1/RCC1-like domains in their tail region that had not been observed before as part of myosin motors (Foth et al, 2006). The biological function of the TgMHCs will await further investigations.…”