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Actin Gene Family Dynamics in Cryptomonads and Red Algae

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Abstract

Here we present evidence for a complex evolutionary history of actin genes in red algae and cryptomonads, a group that acquired photosynthesis secondarily through the engulfment of a red algal endosymbiont. Four actin genes were found in the nuclear genome of the cryptomonad, Guillardia theta, and in the genome of the red alga, Galdieria sulphuraria, a member of the Cyanidiophytina. Phylogenetic analyses reveal that the both organisms possess two distinct sequence types, designated “type-1” and “type-2.” A weak but consistent phylogenetic affinity between the cryptomonad type-2 sequences and the type-2 sequences of G. sulphuraria and red algae belonging to the Rhodophytina was observed. This is consistent with the possibility that the cryptomonad type-2 sequences are derived from the red algal endosymbiont that gave rise to the cryptomonad nucleomorph and plastid. Red algae as a whole possess two very different actin sequence types, with G. sulphuraria being the only organism thus far known to possess both. The common ancestor of Rhodophytina and Cyanidiophytina may have had two actin genes, with differential loss explaining the distribution of these genes in modern-day groups. Our study provides new insight into the evolution and divergence of actin genes in cryptomonads and red algae, and in doing so underscores the challenges associated with heterogeneity in actin sequence evolution and ortholog/paralog detection.

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Acknowledgments

We thank the Joint Genome Institute’s Community Sequencing Program (http://www.jgi.doe.gov/sequencing/why/50026.html) for their ongoing efforts to sequence the nuclear genome of Guillardia theta, K. Barry and E. Lindquist of the JGI for project management and data availability, J. Schmutz for genome assembly, and M. W. Gray, P. Keeling, G. I. McFadden, and C. E. Lane for their contributions to the project. We also thank A. Weber for permission to analyze the Galdieria sulphuraria actin genes, H. Philippe for interesting discussion about actin evolution, and K. Sommerfeld and M. Dlutek for technical assistance. This study was supported in part by a Special Research Opportunities Grant from the Natural Sciences and Engineering Research Council of Canada awarded to JMA and M. W. Gray. GT is supported by a postdoctoral fellowship from the Tula Foundation and the Centre for Comparative Genomics and Evolutionary Bioinformatics at Dalhousie University. JMA is a Fellow of the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, and holder of a New Investigator Award from the Canadian Institutes of Health Research.

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  1. Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia, Canada

    Goro Tanifuji & John M. Archibald

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  1. Goro Tanifuji
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Correspondence to John M. Archibald.

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Supplementary Figure 1

Maximum likelihood phylogenetic tree constructed from an alignment (287 amino acid positions) of 83 actin proteins without Rhodophytina. The tree was produced using RaxML with the RtRev substitution matrix and Gamma + Invar model (4 site rate categories). Bootstrap values were calculated using the rapid bootstrap method and CAT model with 1000 replicates. No numbers are shown where bootstrap support was less than 80%. Scale bar indicates inferred number of amino acid substitutions per site. (EPS 462 kb)

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Tanifuji, G., Archibald, J.M. Actin Gene Family Dynamics in Cryptomonads and Red Algae. J Mol Evol 71, 169–179 (2010). https://doi.org/10.1007/s00239-010-9375-6

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