Filastereans and Ichthyosporeans: Models to Understand the Origin of Metazoan Multicellularity

  • Hiroshi SugaEmail author
  • Iñaki Ruiz-Trillo
Part of the Advances in Marine Genomics book series (AMGE, volume 2)


The origin of animals or metazoans from their unicellular ancestors is one of the most important evolutionary transitions in the history of life. To decipher the molecular mechanisms involved in this transition, it is crucial to understand both the early evolution of animals and their unicellular prehistory. Recent phylogenomic analyses have shown that there are at least three distinct unicellular or colonial lineages closely related to metazoans: choanoflagellates, ichthyosporeans and filastereans. However, until recently, choanoflagellates had been the only lineage for which an entire genome sequence was available. Moreover, the lack of transgenesis tools in any of these unicellular lineages had precluded the possibility of performing functional analyses. To better understand the unicellular prehistory of animals, we have recently obtained the genome sequences of both filastereans and ichthyosporeans. Analyses of their genomes identified many important genes for metazoan multicellularity and development, some of which are absent from the choanoflagellate genomes and thus were thought to be metazoan-specific. We have also established methods for transgenesis and gene silencing in ichthyosporeans. The combination of genomic information and molecular tools in filastereans and ichthyosporeans facilitate efficient functional analyses to understand how the key genes in the evolution of multicellularity were co-opted during the unicellular-tomulticellular transition that gave rise to metazoans. We propose that filastereans and ichthyosporeans are ideal model organisms for investigating the origin of metazoan multicellularity.


Filastereans Ichthyosporeans Evolution of multicellularity Genome sequencing Transgenesis 



We thank theUNICORNproject for the genome sequencing. Figures reprinted from Developmental Biology, vol 377, Issue 1, H. Suga and I Ruiz-Trillo, Development of ichthyosporeans sheds light on the origin of metazoan multicellularity, © Elsevier Inc. (2013), with permission from Elsevier. This work is supported by the Marie Curie Intra-European Fellowship (H. S.), a European Research Council Starting Grant (ERC-2007-StG- 206883), and a grant (BFU2011–23434) from the Ministerio de Economía y Competitividad (MINECO) to I. R.-T.


  1. Abedin M, King N (2008) The premetazoan ancestry of cadherins. Science 319:946–948CrossRefGoogle Scholar
  2. Arkush KD, Mendoza L, AdkisonMAet al (2003) Observations on the life stages of Sphaerothecum destruens n. g., n. sp., a mesomycetozoean fish pathogen formerly referred to as the rosette agent. J Eukaryot Microbiol 50:430–438CrossRefGoogle Scholar
  3. Bonner J (1998) The origins of multicellularity. Integr Biol 1:27–36CrossRefGoogle Scholar
  4. Cavalier-Smith T (1987) The origin of fungi and pseudofungi. In: RaynerADM, Brasier CM, Moore D (eds) Evolutionary biology of fungi. Cambridge University Press, Cambridge, pp 339–353Google Scholar
  5. Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev 73:203–266CrossRefGoogle Scholar
  6. Cavalier-Smith T, Allsopp MTEP (1996) Corallochytrium, an enigmatic non-flagellate protozoan related to choanoflagel-lates. Eur J Protistol 32:306–310CrossRefGoogle Scholar
  7. Cavalier-Smith T, Chao EE (2003) Phylogeny of choanozoa, apusozoa, and other protozoa and early eukaryote megaevolution. J Mol Evol 56:540–563CrossRefGoogle Scholar
  8. Del Campo J, Ruiz-Trillo I (2013) Environmental survey meta-analysis reveals hidden diversity among unicellular opisthokonts. Mol Biol Evol 30:802–805Google Scholar
  9. Elston RA, Harrell LW, Wilkinson MT (1986) Isolation and in vitro characteristics of chinook salmon (Oncorhynchus tshawytscha) rosette agent. Aquaculture 56:1–21CrossRefGoogle Scholar
  10. Fairclough SR, Dayel MJ, King N (2010) Multicellular development in a choanoflagellate. Curr Biol 20:R875–R876CrossRefGoogle Scholar
  11. Grosberg EK, Strathmann RR (2007) The evolution of multicellularity: a minor major transition? Annu Rev Ecol Evol Syst 38:621–654CrossRefGoogle Scholar
  12. Harrell LW, Elston RA, Scott TM et al (1986) A significant new systemic disease of net-pen reared chinook salmon (Oncorhynchus tshawytscha) brood stock. Aquaculture 55:249–262CrossRefGoogle Scholar
  13. James-ClarkH (1866) Note on the infusoria flagellata and the spongiae ciliatae. AmJ Sci 1:113–114Google Scholar
  14. Jøstensen J-P, Sperstad S, Johansen S et al (2002) Molecular-phylogenetic, structural and biochemical features of a cold-adapted, marine ichthyosporean near animal-fungal divergence, described from in vitro cultures. Eur J Protistol 38:93–104CrossRefGoogle Scholar
  15. Kerk D, Gee A, Standish M et al (1995) The rosette agent of chinook salmon (Oncorhynchus tshawytscha) is closely related to choanoflagellates, as determined by the phylogenetic analyses of its small ribosomal subunit RNA. Mar Biol 122:187–192Google Scholar
  16. Kim JA, Cho K, ShinMSet al (2008) Anovel electroporation method using a capillary and wire-type electrode. Biosens Bioelectron 23:1353–1360CrossRefGoogle Scholar
  17. King N (2004) The unicellular ancestry of animal development. Dev. Cell 7:313–325Google Scholar
  18. King N, Westbrook MJ, Young SL et al (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783–788CrossRefGoogle Scholar
  19. Knoll AH (2011) The multiple origins of complex multicellularity. Annu Rev Earth Planet Sci 39:217–239CrossRefGoogle Scholar
  20. MarshallWL, BerbeeML (2003) Methods for introducing morpholinos into the chicken embryo. Dev Dyn 226:470–477CrossRefGoogle Scholar
  21. Lang BF, O’Kelly C, Nerad T et al (2002) The closest unicellular relatives of animals. Curr Biol 12:1773–1778CrossRefGoogle Scholar
  22. Manning G, Young SL, Miller WT et al (2008) The protist, Monosiga brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan. Proc Natl Acad Sci U S A 105:9674–9679CrossRefGoogle Scholar
  23. Marshall WL, Berbee ML (2010) Facing unknowns: living cultures (Pirum gemmata gen. nov., sp. nov., and Abeoforma whisleri, gen. nov., sp. nov.) from invertebrate digestive tracts represent an undescribed clade within the unicellular Opisthokont lineage ichthyosporea (Mesomycetozoea). Protist 162:33–57CrossRefGoogle Scholar
  24. Marshall WL, Berbee ML (2013) Comparative morphology and genealogical delimitation of cryptic species of sympatric isolates of Sphaeroforma (Ichthyosporea, Opisthokonta). Protist 164:287–311CrossRefGoogle Scholar
  25. Marshall WL, Celio G, McLaughlin DJ et al (2008) Multiple isolations of a culturable, motile Ichthyosporean (Mesomycetozoa, Opisthokonta), Creolimax fragrantissima n. gen., n. sp., from marine invertebrate digestive tracts. Protist 159:415–433CrossRefGoogle Scholar
  26. McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10:13–26Google Scholar
  27. McVigar AH (1982) Ichthyophonus infections of fish. In: Roberts RJ (eds) Microbial diseases of fish. Academic Press, London, p 243–269Google Scholar
  28. Medina M, Collins AG, Taylor JW et al (2003) Phylogeny of opisthokonta and the evolution of multicellularity and complexity in fungi and metazoa. Int J Astrobiol 2:203–211CrossRefGoogle Scholar
  29. Mendoza L, Taylor JW, Ajello L (2002) The class Mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. Annu Rev Microbiol 56:315–344CrossRefGoogle Scholar
  30. Moya A, Pereto J, GilRet al (2008) Learning howto live together: genomic insights into prokaryoteanimal symbioses. Nat Rev Genet 9:218–229CrossRefGoogle Scholar
  31. Paps J, Medina-Chacón LA, Marshall WL et al (2013) Molecular phylogeny of unikonts: new insights into the position of apusomonads and ancyromonads and the internal relationships of opisthokonts. Protist 164:2–12CrossRefGoogle Scholar
  32. Pekkarinen M, Lom J, Murphy CA et al (2003) Phylogenetic position and ultrastructure of two dermocystidium species (Ichthyosporea) from the common perch (Perca fluviatilis). Acta Protozool 42:287–307Google Scholar
  33. Ragan MA, Goggin CL, Cawthorn RJ et al (1996) A novel clade of protistan parasites near the animal-fungal divergence. Proc Natl Acad Sci U S A 93:11907–11912CrossRefGoogle Scholar
  34. Rokas A (2008a) The molecular origins of multicellular transitions. Curr Opin Genet Dev 18:472–478CrossRefGoogle Scholar
  35. Rokas A (2008b) The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu Rev Genet 42:235–251CrossRefGoogle Scholar
  36. Ruiz-Trillo I, InagakiY, DavisLAet al (2004) Capsaspora owczarzaki is an independent opisthokont lineage. Curr Biol 14:R946–R947CrossRefGoogle Scholar
  37. Ruiz-Trillo I, Lane CE, Archibald JM et al (2006) Insights into the evolutionary origin and genome architecture of the unicellular opisthokonts Capsaspora owczarzaki and Sphaeroforma arctica. J Eukaryot Microbiol 53:379–384CrossRefGoogle Scholar
  38. Ruiz-Trillo I, Burger G, Holland PW et al (2007) The origins of multicellularity: a multi-taxon genome initiative. Trends Genet 23:113–118CrossRefGoogle Scholar
  39. Sebé-Pedrós A, Ruiz-Trillo I (2010) Integrin-mediated adhesion complex: cooption of signaling systems at the dawn of Metazoa. Commun Integr Biol 3:475–477CrossRefGoogle Scholar
  40. Sebé-Pedrós A, Roger AJ, Lang FB et al (2010) Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc Natl Acad Sci U S A 107:10142–10147CrossRefGoogle Scholar
  41. Sebé-Pedrós A, de Mendoza A, Lang BF et al (2011) Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28:1241–1254CrossRefGoogle Scholar
  42. Sebé-Pedrós A, Zheng Y, Ruiz-Trillo I et al (2012) Premetazoan origin of the Hippo signaling pathway. Cell Rep 1:13–20CrossRefGoogle Scholar
  43. Sebé-Pedrós A, Irimia M, Del Campo J et al (2013) Regulated aggregative multicellularity in a close unicellular relative of metazoa. eLife 2:e01287CrossRefGoogle Scholar
  44. Seeber GR (1900) Un nuevo sporozuario parasito del hombre: dos casos encontrados en polypos nasals. Dissertation, Universidad Nacional de Buenos AiresGoogle Scholar
  45. Shalchian-Tabrizi K, Minge MA, Espelund M et al (2008) Multigene phylogeny of choanozoa and the origin of animals. PLoS One 3:e2098CrossRefGoogle Scholar
  46. Steenkamp ET, Wright J, Baldauf SL (2006) The protistan origins of animals and fungi. Mol Biol Evol 23:93–106CrossRefGoogle Scholar
  47. Stibbs HH, Owczarzak A, Bayne CJ et al (1979) Schistosome sporocyst-killing amoebae isolated from Biomphalaria glabrata. J Invertebr Pathol 33:159–170CrossRefGoogle Scholar
  48. Suga H, Ruiz-Trillo I (2013) Development of ichthyosporeans sheds light on the origin of metazoan multicellularity. Dev Biol 377:284–292CrossRefGoogle Scholar
  49. Suga H, Dacre M, de Mendoza A et al (2012) Genomic survey of pre-metazoans shows deep conservation of cytoplasmic tyrosine kinases and multiple radiations of receptor tyrosine kinases. Sci Signal 5:ra35CrossRefGoogle Scholar
  50. Suga H, Chen Z, De Mendoza A et al (2013) The genome of Capsaspora reveals a complex unicellular prehistory of animals. Nat Commun 4:2325CrossRefGoogle Scholar
  51. Suga H, Torruella G, Burger G et al (2014) Earliest holozoan expansion of phosphotyrosine signaling. Mol Biol Evol 31:517–528Google Scholar
  52. TongSM (1997) Heterotrophic flagellates and other protists from SouthamptonWater, U.K. Ophelia 47:71–131CrossRefGoogle Scholar
  53. Torruella G, Derelle R, Paps J et al (2012) Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single copy protein domains. Mol Biol Evol 20:531–544Google Scholar
  54. van Hannen EJ, Mooij W, van Agterveld MP et al (1999) Detritus-dependent development of the microbial community in an experimental system: qualitative analysis by denaturing gradient gel electrophoresis. Appl Environ Microbiol 65:2478–2484Google Scholar
  55. Wainright PO, Hinkle G, Sogin ML et al (1993) Monophyletic origins of the metazoa: an evolutionary link with fungi. Science 260:340–342CrossRefGoogle Scholar
  56. Willmer P (1990) The origin of the Metazoa. In: Invertebrate relationships: pattern in animal evolution. Cambridge University Press, Cambridge, pp 163–198Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Faculty of Life and Environmental SciencesPrefectural University of HiroshimaShobaraJapan
  2. 2.Institut de Biologia Evolutiva (CSIC—Universitat Pompeu Fabra)BarcelonaSpain
  3. 3.Departament de GenèticaUniversitat de BarcelonaBarcelonaSpain
  4. 4.Institució Catalana de Recerca i Estudis Avançats (ICREA)BarcelonaSpain

Personalised recommendations