Capsaspora owczarzaki

Capsaspora cellsThe amoeboid protist Capsaspora owczarzaki occupies a key position to understand animal origins. It is a member of the Filasterea, that is the sister-group to Choanoflagellatea and Metazoa (Torruella et al.2012 and 2015).

 

Capsaspora was originally described as an amoeba-like “symbiont” of the fresh-water mollusc Biomphalaria glabrata (Stibbs and Owczarzak 1979; Owczarzak et al. 1980). The amoebae were obtained from the pericardial explants and mantle swabs of snails originally sampled in Puerto Rico. Capsaspora was originally described as nucleariids (Owczarzak et al. 1980). However, later molecular ribosomal phylogenies placed Capsaspora somewhere closer to animals than the rest of nucleariids (Zettler et al. 2001; Hertel et al. 2002; Medina et al. 2003). Finally, a multi-gene phylogenetic analysis with several opisthokont taxa clearly showed that Capsaspora is not a nucleariid, but part of the Holozoa (Ruiz-Trillo et al. 2004; Ruiz-Trillo et al. 2006). This was later on corroborated by phylogenomic analyses (Ruiz-Trillo et al. 2008, Shalchian-Tabrizi 2008), one of which (Shalchian-Tabrizi) situated it as sister-group to Ministeria forming the Filasterea clade.

 

The  life cycle of Capsaspora has recently been reported (Sebé-Pedrós et al. 2013). Under culture conditions, Capsaspora cells crawls attached at the substrate, with active replication until the end of the exponential growth phase. Then cells start to detach retracting the branching filopodia and encysting. During this cystic phase, division is stopped. Alternatively, amoebae can actively aggregate to each other by unknown factors, forming a multicellular, aggregative structure and secreting an unstructured extracellular material that seems to prevent direct cell-cell contact.

 

Due to its important phylogenetic position as close unicellular relative of animals, the genome, transcriptome, proteome and phosphoproteome of Capsaspora has been obtained and analyzed (Suga et al. 2013, Sebe-Pedrós et al. 2103,  Sebe-Pedrós et al. 2106a,b). Overall Capsaspora has resulted pivotal to unravel the nature of the unicellular ancestor of animal, which was genetically much more complex than previously thought.
References
-Hertel, L. A., Bayne, C. J., & Loker, E. S. (2002). The symbiontCapsaspora owczarzaki, nov. gen. nov. sp., isolated from three strains of the pulmonate snailBiomphalaria glabratais related to members of the Mesomycetozoea. Int J Parasitol, 32(9), 1183–1191.
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-Owczarzak, A., Stibbs, H. H., & Bayne, C. J. (1980). The destruction ofSchistosoma mansonimother sporocysts in vitro by amoebae isolated fromBiomphalaria glabrata: an ultrastructural study. J Invertebr Pathol, 35(1), 26–33.
-Stibbs, H. H., Owczarzak, A., Bayne, C. J., & DeWan, P. (1979). Schistosome sporocyst-killing Amoebae isolated from Biomphalaria glabrata. Journal of Invertebrate Pathology, 33(2), 159–170.
-Torruella, G., Derelle, R., Paps, J., Lang, B. F., Roger, A. J., Shalchian-Tabrizi, K., & Ruiz-Trillo, I. (2012). Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single-copy protein domains. Mol Biol Evol, 29(2), 531–544. http://doi.org/10.1093/molbev/msr185
-Torruella, G., de Mendoza, A., Grau-Bové, X., Antó, M., Chaplin, M. A., del Campo, J., et al. (2015). Phylogenomics Reveals Convergent Evolution of Lifestyles in Close Relatives of Animals and Fungi. Current Biology : CB, 25(18), 2404–2410. http://doi.org/10.1016/j.cub.2015.07.053
-Ruiz-Trillo, I., Inagaki, Y., Davis, L. A., Sperstad, S., Landfald, B., & Roger, A. J. (2004). Capsaspora owczarzakiis an independent opisthokont lineage. Curr Biol, 14(22), R946–947.
-Ruiz-Trillo, I., Lane, C. E., M, A. J., & Roger, A. J. (2006). Insights into the evolutionary origin and genome architecture of the unicellular opisthokontsCapsaspora owczarzakiandSphaeroforma arctica. Journal of Eukaryotic Microbiology, 53(5), 1–6.
-Ruiz-Trillo, I., Roger, A. J., Burger, G., Gray, M. W., & Lang, B. F. (2008). A phylogenomic investigation into the origin of metazoa. Mol Biol Evol, 25(4), 664–672.
-Sebe-Pedros, A., Irimia, M., del Campo, J., Parra-Acero, H., Russ, C., Nusbaum, C., et al. (2013). Regulated aggregative multicellularity in a close unicellular relative of metazoa. Elife, 2, e01287. http://doi.org/10.7554/eLife.01287
-Shalchian-Tabrizi, K., Minge, M. A., Espelund, M., Orr, R., Ruden, T., Jakobsen, K. S., & Cavalier-Smith, T. (2008). Multigene phylogeny of choanozoa and the origin of animals. PLoS ONE, 3(5), e2098.
-Sebé-Pedrós, A., Ballaré, C., Parra-Acero, H., Chiva, C., Tena, J. J., Sabidó, E., et al. (2016). The Dynamic Regulatory Genome of Capsaspora and the Origin of Animal Multicellularity. Cell, 165(5), 1224–1237. http://doi.org/10.1016/j.cell.2016.03.034
-Sebé-Pedrós, Arnau, Marcia Ivonne Peña, Salvador Capella-Gutiérrez, Meritxell Antó, Toni Gabaldón, Iñaki Ruiz-Trillo & Eduard Sabidó. (2016). High-Throughput Proteomics Reveals the Unicellular Roots of Animal Phosphosignaling and Cell Differentiation. Developmental Cell 39 (2): p186–197.
-Suga, H., Chen, Z., de Mendoza, A., Sebe-Pedros, A., Brown, M. W., Kramer, E., et al. (2013). The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun, 4, 2325. http://doi.org/10.1038/ncomms3325
-Zettler, L., Nerad, T. A., O’Kelly, C. J., & Sogin, M. L. (2001). The nucleariid amoebae: more protists at the animal-fungal boundary. J Eukaryot Microbiol, 48(3), 293–297.