Capsaspora

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Scientific classification Edit this classification
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Binomial name
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Hertel, Bayne & Loker 2002
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Capsaspora is a monotypic genus of protists containing the single species Capsaspora owczarzaki. C. owczarzaki is a single-celled eukaryote that occupies a key phylogenetic position in our understanding of the origin of animal multicellularity, as one of the closest unicellular relatives to animals. It is, together with Ministeria vibrans, a member of the Filasterea clade. This amoeboid protist has been pivotal to unraveling the nature of the unicellular ancestor of animals, which has been proved to be much more complex than previously thought.[3][4][5]

Description

C. owczarzaki was originally described as an amoeba-like "symbiont" of the fresh-water snail Biomphalaria glabrata.[6][7] The amoebae were obtained from the haemolymph of snails originally sampled in Puerto Rico.

C. owczarzaki's life cycle comprises 3 different stages with three different cell types, which was reported in 2017.[8] Under culture conditions, C. owczarzaki's filopodial cells crawl attached to 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-to-cell contact.

C. owczarzaki cells, in the filopodial stage, were described as 3 to 5 μm amoebas with a nucleus Page Template:Fraction/styles.css has no content.1⁄3 - Page Template:Fraction/styles.css has no content.1⁄2 of the diameter of the cell (containing a central nucleolus), long branched filopodia, mitochondria with flattened cristae, numerous phagosomes, lipid vacuoles, glycogen granules and a Golgi apparatus.[6][7] Cystic cells measure 4 to 5 μm with a double wall: the outer thin, irregular and loosely attached; and the inner thicker, smooth.[9]

Taxonomy

Phylogenetic position of Capsaspora

C. owczarzaki is together with Ministeria vibrans a member of the Filasterea clade.[10][1] This group is the sister group to a clade comprising Metazoa and Choanoflagellata, which together form the Filozoa.[10][1][11] C. owczarzaki was originally described as nucleariids.[7] However, later molecular ribosomal phylogenies placed C. owczarzaki somewhere closer to animals than the rest of nucleariids.[12][13][14] Finally, a multi-gene phylogenetic analysis with several opisthokont taxa clearly showed that C. owczarzaki is not a nucleariid, but part of the Holozoa.[15][16] This was later on corroborated by phylogenomic analyses,[17][18] one of which [18] situated it as sister-group to Ministeria forming the Filasterea clade, which is the sister-group to Choanoflagellatea and Metazoa.[19][20]

Applications

C. owczarzaki is of scientific interest because it is one of the closest unicellular relatives of multicellular animals. Its genome has recently been sequenced and shows several genes involved in metazoan multicellularity, such as integrins,[21] metazoan transcription factors,[22] and protein tyrosine kinases.[23] Moreover, it has relevance to human health because its host, the snail Biomphalaria glabrata, is also the intermediate host of the digenean flatworm Schistosoma mansoni, the causative agent of widespread schistosomiasis in humans. C. owczarzaki not only parasitizes the intermediate host of S. mansoni but also attacks and kills the sporocysts of the flatworm living inside the snail.[24]

References

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  1. ^ a b c Page Module:Citation/CS1/styles.css has no content.Shalchian-Tabrizi, K; Minge, MA; Espelund, M; Orr, R; Ruden, T; Jakobsen, KS; Cavalier-Smith, T (2008). "Multigene phylogeny of choanozoa and the origin of animals". PLOS ONE. 3 (5) e2098. Bibcode:2008PLoSO...3.2098S. doi:10.1371/journal.pone.0002098. PMC 2346548. PMID 18461162.
  2. ^ Page Module:Citation/CS1/styles.css has no content.Hertel L. A.; Bayne C. J.; Loker, E. S. (August 2002), "The symbiont Capsaspora owczarzaki, nov. gen. nov. sp., isolated from three strains of the pulmonate snail Biomphalaria glabrata is related to members of the Mesomycetozoea", International Journal for Parasitology, 32 (9): 1183–91, doi:10.1016/S0020-7519(02)00066-8, PMID 12117501
  3. ^ Page Module:Citation/CS1/styles.css has no content.Suga, Hiroshi; Chen, Zehua; Mendoza, Alex de; Sebé-Pedrós, Arnau; Brown, Matthew W.; Kramer, Eric; Carr, Martin; Kerner, Pierre; Vervoort, Michel (2013-08-14). "The Capsaspora genome reveals a complex unicellular prehistory of animals". Nature Communications. 4: 2325. Bibcode:2013NatCo...4.2325S. doi:10.1038/ncomms3325. ISSN 2041-1723. PMC 3753549. PMID 23942320.
  4. ^ Page Module:Citation/CS1/styles.css has no content.Sebé-Pedrós, Arnau; Ballaré, Cecilia; Parra-Acero, Helena; Chiva, Cristina; Tena, Juan J.; Sabidó, Eduard; Gómez-Skarmeta, José Luis; Croce, Luciano Di; Ruiz-Trillo, Iñaki (2016). "The Dynamic Regulatory Genome of Capsaspora and the Origin of Animal Multicellularity". Cell. 165 (5): 1224–1237. doi:10.1016/j.cell.2016.03.034. PMC 4877666. PMID 27114036.
  5. ^ Page Module:Citation/CS1/styles.css has no content.Sebé-Pedrós, Arnau; Peña, Marcia Ivonne; Capella-Gutiérrez, Salvador; Antó, Meritxell; Gabaldón, Toni; Ruiz-Trillo, Iñaki; Sabidó, Eduard (2016). "High-Throughput Proteomics Reveals the Unicellular Roots of Animal Phosphosignaling and Cell Differentiation". Developmental Cell. 39 (2): 186–197. doi:10.1016/j.devcel.2016.09.019. hdl:10230/32237. PMID 27746046.
  6. ^ a b Page Module:Citation/CS1/styles.css has no content.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. doi:10.1016/0022-2011(79)90149-6. PMID 501126.
  7. ^ a b c Page Module:Citation/CS1/styles.css has no content.Owczarzak, A.; Stibbs, H. H.; Bayne, C. J. (1980). "The destruction of Schistosoma mansonimother sporocysts in vitro by amoebae isolated fromBiomphalaria glabrata: an ultrastructural study". J Invertebr Pathol. 35 (1): 26–33. doi:10.1016/0022-2011(80)90079-8. PMID 7365267.
  8. ^ Page Module:Citation/CS1/styles.css has no content.Ferrer-Bonet M, Ruiz-Trillo I (2017-09-11). "Capsaspora owczarzaki". Curr Biol. 27 (17): R829–R830. ISSN 0960-9822. Retrieved 2024-09-06.
  9. ^ Sebe-Pedros, A. (2013) The origin of metazoan multicellularity, a genomic and functionalapproach. PhD UB, Facultat de Biologia, Departament de Genètica
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  12. ^ Page Module:Citation/CS1/styles.css has no content.Hertel, Lynn A.; Bayne, Christopher J.; Loker, Eric S. (2002-08-01). "The symbiont Capsaspora owczarzaki, nov. gen. nov. sp., isolated from three strains of the pulmonate snail Biomphalaria glabrata is related to members of the Mesomycetozoea". International Journal for Parasitology. 32 (9): 1183–1191. doi:10.1016/s0020-7519(02)00066-8. ISSN 0020-7519. PMID 12117501.
  13. ^ Page Module:Citation/CS1/styles.css has no content.Zettler, L. A. A.; Nerad, T. A.; O'Kelly, C. J.; Sogin, M. L. (2001-05-01). "The nucleariid amoebae: more protists at the animal-fungal boundary". The Journal of Eukaryotic Microbiology. 48 (3): 293–297. doi:10.1111/j.1550-7408.2001.tb00317.x. ISSN 1066-5234. PMID 11411837. S2CID 44548329.
  14. ^ Page Module:Citation/CS1/styles.css has no content.Medina, Mónica; Collins, Allen G.; Taylor, John W.; Valentine, James W.; Lipps, Jere H.; Amaral-Zettler, Linda; Sogin, Mitchell L. (2003-07-01). "Phylogeny of Opisthokonta and the evolution of multicellularity and complexity in Fungi and Metazoa". International Journal of Astrobiology. 2 (3): 203–211. Bibcode:2003IJAsB...2..203M. doi:10.1017/S1473550403001551. ISSN 1475-3006.
  15. ^ Page Module:Citation/CS1/styles.css has no content.Ruiz-Trillo, Iñaki; Inagaki, Yuji; Davis, Lesley A.; Sperstad, Sigmund; Landfald, Bjarne; Roger, Andrew J. (2004). "Capsaspora owczarzaki is an independent opisthokont lineage". Current Biology. 14 (22): R946–R947. doi:10.1016/j.cub.2004.10.037. PMID 15556849.
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  17. ^ Page Module:Citation/CS1/styles.css has no content.Ruiz-Trillo, Iñaki; Roger, Andrew J.; Burger, Gertraud; Gray, Michael W.; Lang, B. Franz (2008-04-01). "A phylogenomic investigation into the origin of metazoa". Molecular Biology and Evolution. 25 (4): 664–672. doi:10.1093/molbev/msn006. ISSN 1537-1719. PMID 18184723.
  18. ^ a b Page Module:Citation/CS1/styles.css has no content.Shalchian-Tabrizi, Kamran; Minge, Marianne A.; Espelund, Mari; Orr, Russell; Ruden, Torgeir; Jakobsen, Kjetill S.; Cavalier-Smith, Thomas (2008-05-07). "Multigene Phylogeny of Choanozoa and the Origin of Animals". PLOS ONE. 3 (5) e2098. Bibcode:2008PLoSO...3.2098S. doi:10.1371/journal.pone.0002098. ISSN 1932-6203. PMC 2346548. PMID 18461162.
  19. ^ Page Module:Citation/CS1/styles.css has no content.Torruella, G.; Derelle, R.; Paps, J.; Lang, B. F.; Roger, A. J.; Shalchian-Tabrizi, K.; Ruiz-Trillo, I. (2012-02-01). "Phylogenetic Relationships within the Opisthokonta Based on Phylogenomic Analyses of Conserved Single-Copy Protein Domains". Molecular Biology and Evolution. 29 (2): 531–544. doi:10.1093/molbev/msr185. ISSN 0737-4038. PMC 3350318. PMID 21771718.
  20. ^ Page Module:Citation/CS1/styles.css has no content.Torruella, Guifré; Mendoza, Alex de; Grau-Bové, Xavier; Antó, Meritxell; Chaplin, Mark A.; Campo, Javier del; Eme, Laura; Pérez-Cordón, Gregorio; Whipps, Christopher M. (2015). "Phylogenomics Reveals Convergent Evolution of Lifestyles in Close Relatives of Animals and Fungi". Current Biology. 25 (18): 2404–2410. doi:10.1016/j.cub.2015.07.053. PMID 26365255.
  21. ^ Page Module:Citation/CS1/styles.css has no content.Sebe-Pedros, A; RogerA, Lang F; King, N; Ruiz-Trillo, I (2010). "Ancient origin of integrin-mediated adhesion and signaling machinery". Proceedings of the National Academy of Sciences USA. 107 (22): 10142–7. doi:10.1073/pnas.1002257107. PMC 2890464. PMID 20479219.
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  24. ^ Page Module:Citation/CS1/styles.css has no content.Owczarzak, A; Stibbs, HH; Bayne, CJ (January 1980). "The destruction of Schistosoma mansoni mother sporocystsin vitro by amoebae isolated from Biomphalaria glabrata: an ultrastructuralstudy". J. Invertebr. Pathol. 35 (1): 26–33. doi:10.1016/0022-2011(80)90079-8. PMID 7365267.

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