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Capsaspora

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Capsaspora
Scientific classification
Domain:
Eukaryota
(unranked):
Opisthokonta
(unranked):
Holozoa
(unranked):
Filozoa
Class:
Filasterea
Order:
Ministeriida
Family:
Capsasporidae

Cavalier-Smith, 2008[1]
Genus:
Capsaspora

Hertel, Bayne & Loker, 2002[2]
Species:
C. owczarzaki
Binomial name
Capsaspora owczarzaki
Hertel, Bayne & Loker, 2002[2]

Capsaspora is a monotypic genus 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 (see “Taxonomy” below). This amoeboid protist has been pivotal to unravel 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 only recently.[when?] 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-cell contact.

C. owczarzaki cells, in the filopodial stage, were described as 3 to 5 μm amoebas with a nucleus ⅓ - ½ 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.[8]

Taxonomy

C. owczarzaki is together with Ministeria vibrans a member of the Filasterea clade.[9][1] This group is the sister group to a clade comprising Metazoa and Choanoflagellata, which together form the Filozoa[9][1][10] (See Figure 1). 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.[11][12][13] Finally, a multi-gene phylogenetic analysis with several opisthokont taxa clearly showed that C. owczarzaki is not a nucleariid, but part of the Holozoa.[14][15] This was later on corroborated by phylogenomic analyses,[16][17] one of which [17] situated it as sister-group to Ministeria forming the Filasterea clade, which is the sister-group to Choanoflagellatea and Metazoa.[18][19]

Figure 1: Capsaspora's phylogenetic tree

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,[20] metazoan transcription factors,[21] and protein tyrosine kinases.[22] 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.[23]

References

  1. ^ a b c 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. ^ a b 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. ^ 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. ^ 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. ^ 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. PMID 27746046.
  6. ^ a b 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 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. ^ Sebe-Pedros, A. (2013) The origin of metazoan multicellularity, a genomic and functionalapproach. PhD UB, Facultat de Biologia, Departament de Genètica
  9. ^ a b Torruella, G; Derelle, R; Paps, J; Lang, F; Roger, A; Shalchian-Tabrizi, K; Ruiz-Trillo, I (2012). "Phylogenetic relationships within theOpisthokonta based on phylogenomic analyses of conserved single copy proteindomains". Molecular Biology and Evolution. 29 (2): 531–544. doi:10.1093/molbev/msr185. PMC 3350318. PMID 21771718.
  10. ^ Paps, J; Medina-Chacon, L; Marshall, W; Suga, H; Ruiz-Trillo, I (2013). "Molecular phylogeny of Unikonts: new insightsinto the position of apusomonads and ancyromonads and the internalrelationships of opisthokonts". Protist. 164 (1): 2–12. doi:10.1016/j.protis.2012.09.002. PMC 4342546. PMID 23083534.
  11. ^ 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.
  12. ^ Zettler LAA, null; 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.
  13. ^ 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.
  14. ^ 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.
  15. ^ Ruiz-Trillo, Inaki; Lane, Christopher E.; Archibald, John M.; Roger, Andrew J. (2006-09-01). "Insights into the evolutionary origin and genome architecture of the unicellular opisthokonts Capsaspora owczarzaki and Sphaeroforma arctica". The Journal of Eukaryotic Microbiology. 53 (5): 379–384. doi:10.1111/j.1550-7408.2006.00118.x. ISSN 1066-5234. PMID 16968456. S2CID 24862220.
  16. ^ 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.
  17. ^ a b 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.
  18. ^ 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.
  19. ^ 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.
  20. ^ 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.
  21. ^ Sebe-Pedros, A; de Mendoza, A; Lang, F; Degnan, B; Ruiz-Trillo, I (2011). "Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki". Molecular Biology and Evolution. 28 (3): 1241–54. doi:10.1093/molbev/msq309. PMC 4342549. PMID 21087945.
  22. ^ Suga, H; DacreM; de Mendoza, A; Shalchian-Tabrizi, K; Manning, G; Ruiz-TrilloI (2012). "Genomic Survey of Premetazoans Shows Deep Conservation of Cytoplasmic Tyrosine Kinases and Multiple Radiations of Receptor Tyrosine Kinases". Science Signaling. 5 (222): ra35. doi:10.1126/scisignal.2002733. hdl:10261/112779. PMID 22550341. S2CID 27205070.
  23. ^ 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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