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Myosin domain evolution and the primary divergence of eukaryotes

Abstract

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.

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Figure 1: Taxonomic distribution and evolutionary history of myosin paralogues.
Figure 2: Myosin head domain phylogeny (bayesian consensus: 118 myosins; 357 characters).
Figure 3: Section from a myosin sequence alignment, including a representative selection of myosin types.

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Acknowledgements

Preliminary sequence data were obtained from The Institute for Genomic Research website (http://www.tigr.org) and the Department of Energy Joint Genome Institute (JGI) website (http://www.jgi.doe.gov). We thank TIGR and DOE JGI for making data publicly available, A. A. Davies for comments and assistance with data management, and D. Soanes for PSI BLAST assistance. T.A.R. was supported by a BBSRC studentship. T.C.-S. thanks NERC for research grants and NERC and the Canadian Institute for Advanced Research Evolutionary Biology Program for Fellowship support.

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Correspondence to Thomas A. Richards.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Table S1.

Comparative genome survey of myosin genes. Full details of comparative genomic analyses of the myosin gene family displayed as a table with footnotes and an additional table listing details about domain names, definitions and abbreviations. (DOC 185 kb)

Supplementary Figure S1.

Alignment of representatives of myosin class II, V and XI. Annotated amino acid alignment that illustrates sequence synapomorphies and details about protein domain evolution. (PDF 1803 kb)

Supplementary Figure S2.

Alignment of myosins with either MYTH4 and/or FERM domains. Annotated amino acid alignment that illustrates sequence synapomorphies and details about protein domain evolution. (PDF 2115 kb)

Supplementary Figure S3.

Alignment of representatives of myosin class I. Annotated amino acid alignment that illustrates sequence synapomorphies and details about protein domain evolution. (PDF 2638 kb)

Supplementary Figure S4.

Phylogeny of myosin head domains; this is the same tree as in Fig. 2 of the main text of the paper, except that accession numbers replace species names and exact support values are shown. The details of the phylogenetic methods are explained in the figure legend. (PDF 82 kb)

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Richards, T., Cavalier-Smith, T. Myosin domain evolution and the primary divergence of eukaryotes. Nature 436, 1113–1118 (2005). https://doi.org/10.1038/nature03949

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