Myosin repertoire expansion coincides with eukaryotic diversification in the Mesoproterozoic era

Abstract

BackgroundThe last eukaryotic common ancestor already had an amazingly complex cell possessing genomic and cellular features such as spliceosomal introns, mitochondria, cilia-dependent motility, and a cytoskeleton together with several intracellular transport systems. In contrast to the microtubule-based dyneins and kinesins, the actin-filament associated myosins are considerably divergent in extant eukaryotes and a unifying picture of their evolution has not yet emerged.ResultsHere, we manually assembled and annotated 7852 myosins from 929 eukaryotes providing an unprecedented dense sequence and taxonomic sampling. For classification we complemented phylogenetic analyses with gene structure comparisons resulting in 79 distinct myosin classes. The intron pattern analysis and the taxonomic distribution of the classes suggest two myosins in the last eukaryotic common ancestor, a class-1 prototype and another myosin, which is most likely the ancestor of all other myosin classes. The sparse distribution of class-2 and class-4 myosins outside their major lineages contradicts their presence in the last eukaryotic common ancestor but instead strongly suggests early eukaryote-eukaryote horizontal gene transfer.ConclusionsBy correlating the evolution of myosin diversity with the history of Earth we found that myosin innovation occurred in independent major “burst” events in the major eukaryotic lineages. Most myosin inventions happened in the Mesoproterozoic era. In the late Neoproterozoic era, a process of extensive independent myosin loss began simultaneously with further eukaryotic diversification. Since the Cambrian explosion, myosin repertoire expansion is driven by lineage- and species-specific gene and genome duplications leading to subfunctionalization and fine-tuning of myosin functions.Electronic supplementary materialThe online version of this article (10.1186/s12862-017-1056-2) contains supplementary material, which is available to authorized users.

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

“…S5) as well as Myo22 ( Fig. S5, Supplementary Text 1) (Odronitz and Kollmar 2007;Kollmar and Mühlhausen 2017):…”

“…Myo1s are ancient, widely expressed myosins that link membranes to the actin cytoskeleton (McIntosh and Ostap 2016;Kollmar and Mühlhausen 2017). The budding and fission yeast Myo1s recruit activators of the Arp2/3 complex to actin patches to drive internalization of endocytic vesicles (Giblin et al 2011).…”

Animal evolution coincides with a novel degree of freedom in exocytic transport processes

“…4C). Comparing their sequences, the Mb-MYO5 globular tail domain is closely related to the vertebrate MYO5-GTDs (Pylypenko, et al 2013;Kollmar and Muhlhausen 2017) and it remains to be analysed whether Mb-SPIRE contacts Mb-MYO5 in a similar way as it was found in mammals. The strong interaction of Mb-SPIRE and Mb-MYO5, however, indicates that the cooperation of actin nucleation and motor protein activation is conserved between choanoflagellates and mammals.…”

“…SPIRE genes have been identified and annotated using the same approach, with which thousands of tubulins, myosins and dynein heavy chains were annotated and which has been described in exhaustive detail there (Findeisen, et al 2014;Kollmar 2016;Kollmar and Muhlhausen 2017). Shortly, starting with the protein sequences of human and Drosophila melanogaster SPIRE, further homologs were identified in TBLASTN searches of available genome and transcriptome assemblies.…”

Update on Myosin Motors: Molecular Mechanisms and Physiological Functions

“…These cellular functions allow myosins to perform supporting roles in plant growth, environmental responses, and defense against pathogens. Angiosperms typically encode around 15 myosin genes that can be grouped into two families, myosin VIII and myosin XI motors, which are found only in the Archaeplastidae lineage (Reddy and Day, 2001;Odronitz and Kollmar, 2007;Kollmar and Mühlhausen, 2017). Both motor families follow the typical myosin domain organization with an N-terminal motor domain, followed by a neck region that functions as a lever arm, a coiled-coil region for dimerization, and a globular C-terminal tail.…”