Skip to main content

The Protistan Origins of Animals and Fungi

  • Chapter
  • First Online:
Evolution of Fungi and Fungal-Like Organisms

Part of the book series: The Mycota ((MYCOTA,volume 14))

  • 748 Accesses

Abstract

Fungi and Metazoa (animals) are two major multicellular kingdoms of life and both are positioned in the eukaryotic Opisthokonta. Within the supergroup Fungi and Metazoa fall into either side of the opisthokont root, in the major sub-groups Holomycota and Holozoa. In this chapter, we cover recent advances in the understanding of opisthokont biology, in particular looking at their diversity and where opisthokonts fall in the eukaryotic tree. Although much uncertainty remains over how different eukaryotic supergroups are related to each other, the closest relatives of Opisthokonta are now widely recognised.

The composition of Opisthokonta has been revised due to the discovery of new species, as well as the reassignment of taxa on the basis of phylogenetic analyses. We consider common traits and characteristics found in opisthokonts. The explosion of genomic and transcriptomic sequencing since the turn of the century has allowed the identification of genes involved in multicellularity in both Metazoa and Fungi; molecular phylogenies show multicellularity has independently evolved in multiple lineages across the opisthokonts. Annotated gene complements from species spanning the group highlight that gene loss and gain is a dynamic process in the opisthokonts.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adl SM, Simpson AGB, Farmer MA et al (2005) The new higher level of classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451

    Article  PubMed  Google Scholar 

  • Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:429–493

    Article  PubMed  PubMed Central  Google Scholar 

  • Adl SM, Bass D, Lane CE et al (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 66:4–119

    Article  PubMed  PubMed Central  Google Scholar 

  • Amaral-Zettler LA, Nerad TA, O’Kelly J, Sogin ML (2001) The nucleariid amoebae: more protists at the animal–fungal boundary. J Eukaryot Microbiol 48:293–297

    Article  Google Scholar 

  • Baker GC, Beebee TJ, Ragan MA (1999) Prototheca richardsi, a pathogen of anuran larvae, is related to a clade of protistan parasites near the animal–fungal divergence. Microbiology 145:1777–1784

    Article  CAS  PubMed  Google Scholar 

  • Balbiani G (1882) Sur les microsporidies ou psorospermies des Articulés. C R Acad Sci 95:1168–1171

    Google Scholar 

  • Baldauf SL, Palmer JD (1993) Animals and fungi are each others closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci U S A 90:11558–11562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bass D, Czech L, Williams BAP et al (2018) Clarifying the relationships between Microsporidia and Cryptomycota. J Eukaryot Microbiol 65:773–782

    Article  PubMed  PubMed Central  Google Scholar 

  • Bauer R, Garnica S, Oberwinkler F et al (2015) Entorrhizomycota: A new fungal phylum reveals new perspectives on the evolution of Fungi. PLoS One 10:e0128183

    Article  PubMed  PubMed Central  Google Scholar 

  • Beebee TJC, Wong AL-C (1992) Prototheca-mediated interference competition between anuran larvae operates by resource diversion. Physiol Zool 65:815–831

    Article  Google Scholar 

  • Benny GL, O’Donnell K (2000) Amoebidium parasiticum is a protozoan, not a Trichomycete. Mycologica 92:1133–1137

    Article  Google Scholar 

  • Berbee ML, Taylor JW (2010) Dating the molecular clock in fungi – how close are we? Fungal Biol Rev 24:1–16

    Article  Google Scholar 

  • Bergsten J (2005) A review of long-branch attraction. Cladistics 21:163–193

    Article  PubMed  Google Scholar 

  • Betancur-R R, Naylor GJP, Ortí G (2014) Conserved genes, sampling error, and phylogenomic inference. Syst Biol 63:257–262

    Article  PubMed  Google Scholar 

  • Betat H, Mede T, Tretbar S et al (2015) The ancestor of modern Holozoa acquired the CCA-adding enzyme from Alphaproteobacteria by horizontal gene transfer. Nucleic Acids Res 43:6739–6746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bojko J, Reinke AW, Stentiford GD et al (2022) Microsporidia: a new taxonomic, evolutionary, and ecological synthesis. Trends Parasitol 38:642–659

    Article  CAS  PubMed  Google Scholar 

  • Bonasoro F, Wilkie IC, Bavestrello G et al (2001) Dynamic structure of the mesohyl in the sponge Chondrosia reniformis (Porifera, Demospongiae). Zoomorphology 121:109–121

    Article  Google Scholar 

  • Booth DS, Szmidt-Middleton H, King N (2018) Transfection of choanoflagellates illuminates their cell biology and the ancestry of animal septins. Mol Biol Cell 29:3026–3038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borteiro C, Baldo D, Maronna MM et al (2018) Amphibian parasite of the Order Dermocystida (Ichthyosporea): current knowledge, taxonomic review and new records from Brazil. Zootaxa 4461:499–518

    Article  PubMed  Google Scholar 

  • Bourlat SJ, Nielsen C, Economou AD, Telford MJ (2008) Testing the new animal phylogeny: a phylum level molecular analysis of the animal kingdom. Mol Phylogenet Evol 49:23–31

    Article  CAS  PubMed  Google Scholar 

  • Bourrelly P (1968) Les algues d’eau douce. Tome II: Les algues jaunes et brunes. N. Boubée et Cie, Paris

    Google Scholar 

  • Brinkmann H, van der Giezen M, Zhou Y et al (2005) An empirical assessment of long-branch attraction artefacts in deep euakaryotic phylogenomics. Syst Biol 54:743–757

    Article  PubMed  Google Scholar 

  • Brown MW, Spiegel FW, Silberman JD (2009) Phylogeny of the “forgotten” cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Mol Biol Evol 26:2699–2709

    Article  CAS  PubMed  Google Scholar 

  • Brown MW, Sharpe SC, Silberman JD et al (2013) Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc R Soc B 280:20131755

    Article  PubMed  PubMed Central  Google Scholar 

  • Brown MW, Heiss AA, Kamikawa R et al (2018) Phylogenomics places orphan protistan lineages in a novel eukaryotic super-group. Genome Biol Evol 10:427–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunet T, King N (2017) The origin of animal multicellularity and cell differentiation. Dev Cell 43:124–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bullerwell CE, Lang BF (2005) Fungal evolution: the case of the vanishing mitochondrion. Curr Opin Microbiol 8:362–369

    Article  CAS  PubMed  Google Scholar 

  • Burger G, Forget L, Zhu Y et al (2003) Unique mitochondrial genome architecture in unicellular relatives of animals. Proc Natl Acad Sci U S A 100:892–897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burkhardt P, Sprecher SG (2017) Evolutionary origin of synapses and neurons – bridging the gap. BioEssays 39:1700024

    Article  Google Scholar 

  • Burki F, Shalchian-Tabrizi K, Minge M et al (2007) Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 8:e790

    Article  Google Scholar 

  • Burki F, Roger AJ, Brown MW, Simpson AGB (2020) The new tree of eukaryotes. Trends Ecol Evol 35:43–55

    Article  PubMed  Google Scholar 

  • Bütschli O (1878) Beiträge zur Kenntnis der Flagellaten und einiger verwandter Organismen. Z Wiss Zool Abt A 30:219–281

    Google Scholar 

  • Cafaro MJ (2005) Eccrinales (Trichomycetes) are not fungi, but a clade of protists at the early divergence of animals and fungi. Mol Phylogenet Evol 35:21–34

    Article  CAS  PubMed  Google Scholar 

  • Cannon JT, Cossermelli Vellutini B, Smith J III et al (2016) Xenacoelomorpha is the sister group to Nephrozoa. Nature 530:89–93

    Article  CAS  PubMed  Google Scholar 

  • Carr M, Leadbeater BSC (2022) Re-evaluating loricate choanoflagellate phylogenetics: molecular evidence points to the paraphyly of tectiform species. Protist 173:125924. https://doi.org/10.1016/j.protis.2022.125924

    Article  CAS  PubMed  Google Scholar 

  • Carr M, Leadbeater BSC, Hassan R et al (2008) Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proc Natl Acad Sci U S A 105:16641–16646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carr M, Leadbeater BSC, Baldauf SL (2010) Conserved meiotic genes point to sex in the choanoflagellates. J Eukaryot Microbiol 57:56–62

    Article  CAS  PubMed  Google Scholar 

  • Carr M, Richter D, Fozouni P et al (2017) A six-gene phylogeny provides new insights into choanoflagellate evolution. Mol Phylogenet Evol 107:166–178

    Article  PubMed  Google Scholar 

  • Cavalier-Smith T (1983) A 6-kingdom classification and a unified phylogeny. In: Schenk HEA, Schwemmler WS (eds) Endocytobiology. II. Intracellular space as oligogenetic. Walter de Gruyter, Berlin, pp 1027–1034

    Chapter  Google Scholar 

  • Cavalier-Smith T (1987) The origin of fungi and pseudofungi. In: Rayner ADM, Brasierand M, Moore D (eds) Evolutionary biology of fungi. Cambridge University Press, Cambridge, pp 339–353

    Google Scholar 

  • Cavalier-Smith T (1993) Kingdom protozoa and its 18 phyla. Microbiol Rev 57:953–994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavalier-Smith T (1997) Amoeboflagellates and mitochondrial cristae in eukaryote evolution: megasystematics of the new protozoan subkingdoms Eozoa and Neozoa. Arch Protistenkd 147:237–258

    Article  Google Scholar 

  • Cavalier-Smith T (1998a) Neomonada and the origin of animals and fungi. In: Coombs GH, Vickerman K, Sleigh MA, Warren A (eds) Evolutionary relationships among Protozoa. Chapman & Hall, London, pp 375–407

    Google Scholar 

  • Cavalier-Smith T (1998b) A revised six kingdom system of life. Biol Rev 73:203–266

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int J Syst Evol Biol 52:297–354

    Article  CAS  Google Scholar 

  • Cavalier-Smith T, Allsopp MTEP (1996) Corallochytrium, an enigmatic non-flagellate protozoan related to choanoflagellates. Eur J Protistol 32:306–310

    Article  Google Scholar 

  • Cavalier-Smith T, Chao EE-Y (2003) Phylogeny of Choanozoa, Apusozoa, and other protozoa and early eukaryote megaevolution. J Mol Evol 56:540–563

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T, Chao EE-Y, Oates B (2004) Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. Eur J Protistol 40:21–48

    Article  Google Scholar 

  • Cavalier-Smith T, Chao EE, Snell EA et al (2014) Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonta (animals, fungi, choanozoans) and Amoebozoa. Mol Phylogenet Evol 81:71–85

    Article  PubMed  Google Scholar 

  • Chadefaud M (1960) Les végétaux non vasulaires (Cryptogamie). In: Chadeauf M, Emberger I (eds) Traité de botanique systématique, vol 3. Masson et Cie, Paris, pp 1–1018

    Google Scholar 

  • Chang Y, Wang S, Sekimoto S et al (2015) Phylogenomic analyses indicate that early fungi evolved digesting cells walls of algal ancestors of land plants. Genome Biol Evol 7:1590–1601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christen R, Ratto A, Baroin A et al (1991) An analysis of the origin of metazoans, using comparisons of partial sequences of the 28S RNA, reveals an early emergence of triploblasts. EMBO J 10:499–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cienkowski L (1865) Beiträge zur Kenntniss der Monaden. Arch mikr Anat 1:203–232

    Article  Google Scholar 

  • Copeland HF (1956) The classification of lower organisms. Pacific Books, Palo Alto, CA

    Book  Google Scholar 

  • Corsaro D, Walochnik J, Venditti D et al (2014) Rediscovery of Nucleophaga amoebae, a novel member of the Rozellomycota. Parasitol Res 113:4491–4498

    Article  PubMed  Google Scholar 

  • Dayel MJ, Alegado RA, Fairclough SR et al (2011) Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev Biol 357:73–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeBry RW (2005) The systematic component of phylogenetic error as a function of taxonomic sampling under parsimony. Syst Biol 54:432–440

    Article  PubMed  Google Scholar 

  • del Campo J, Massana R (2011) Emerging diversity within chrysophytes, choanoflagellates and bicosoecids based upon molecular surveys. Protist 162:435–448

    Article  PubMed  Google Scholar 

  • del Campo J, Ruiz-Trillo I (2013) Environmental survey meta-analysis reveals hidden diversity among unicellular opisthokonts. Mol Biol Evol 30:802–805

    Article  PubMed  PubMed Central  Google Scholar 

  • Denbo S, Aono K, Kai T et al (2018) Revision of the Capsaspora genome using read mating information adjusts the view on premetazoan genome. Dev Growth Differ 61:34–42

    Article  PubMed  Google Scholar 

  • Derelle R, Torruella G, Klimeš V et al (2015) Bacterial proteins pinpoint a single eukaryotic root. Proc Natl Acad Sci U S A 112:E693–E699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derelle R, López-Garcia P, Timpano H, Moreira D (2016) A phylogenomic framework to study the diversity and evolution of stramenopiles. Mol Biol Evol 33:2890–2898

    Article  CAS  PubMed  Google Scholar 

  • Dirren S, Posch T (2016) Promiscuous and specific bacterial symbiont acquisition in the amoeboid genus Nuclearia (Opisthokonta). FEMS Microbiol Ecol 92:fiw105

    Article  PubMed  Google Scholar 

  • Dirren S, Pitsch G, Silva MOD, Posch T (2017) Grazing of Nuclearia thermophila and Nuclearia delicatula (Nucleariidae, Opisthokonta) on the toxic cyanobacterium Planktothrix rubescens. Eur J Protistol 60:87–101

    Article  PubMed  Google Scholar 

  • Dubin A, Chi SI, Emblem Å et al (2019) Deep-water sea anemone with a two-chromosome mitochondrial genome. Gene 692:195–200

    Article  CAS  PubMed  Google Scholar 

  • Dunn CW, Hejnol A, Matus DQ et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749

    Article  CAS  PubMed  Google Scholar 

  • Dyková I, Veverkov M, Fiala I et al (2003) Nuclearia pattersoni sp. n. (Filosea), a new species of amphizoic amoeba isolated from gills of roach (Rutilus rutilus), and its rickettsial endosymbiont. Folia Parasitol 50:161–170

    Article  Google Scholar 

  • Edler D, Klein J, Antonelli A, Silvestro D (2020) raxmlGUI 2.0: a graphical interface and toolkit for phylogenetic analyses using RAxML. Methods Ecol Evol 12:373–377

    Article  Google Scholar 

  • Edlind TD, Li J, Visvesvara GS et al (1996) Phylogenetic analysis of β-tubulin sequences from amitochondrial protozoa. Mol Phylo Evol 5:359–367

    Article  CAS  Google Scholar 

  • Ehrenberg CG (1831) Über die Entwickelung und Lebensdauer der Infusionthiere: nebst ferneren Beiträgen zu einer Vergleichung ihrer organischen Système, vol 1831. Abh Königl Akad Wiss Berlin, pp 1–154

    Google Scholar 

  • Ehrenberg CG (1838) Die Infusionsthierchen als vollkommene Organismen. Voss, Leipzig

    Book  Google Scholar 

  • Embley TM, van der Giezen M, Horner DS et al (2003) Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55:387–395

    Article  CAS  PubMed  Google Scholar 

  • Erwin DH, Valentine JW (2013) The Cambrian explosion: the construction of animal biodiversity. Roberts & Company, Calgary, AB

    Google Scholar 

  • Fairclough SR, Chen Z, Kramer E et al (2013) Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol 14:R15

    Article  PubMed  PubMed Central  Google Scholar 

  • Fast NM, Logsdon JM Jr, Doolittle WF (1999) Phylogenetic analysis of the TATA box binding protein (TBP) gene from Nosema locustae: evidence for a microsporidia-fungi relationship and spliceosomal intron loss. Mol Biol Evol 16:1415–1419

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Biol 27:401–410

    Article  Google Scholar 

  • Ferrier DEK, Holland PWH (2001) Ancient origin of the Hox gene cluster. Nat Rev Genet 2:33–38

    Article  CAS  PubMed  Google Scholar 

  • Franzen C (2005) How do microsporidia invade cells. Folia Parasitol 52:36–40

    Article  Google Scholar 

  • Fraune S, Bosch TCG (2010) Why bacteria matter in animal development and evolution. BioEssays 32:571–580

    Article  CAS  PubMed  Google Scholar 

  • Gabaldón T, Völcker E, Torruella G (2022) On the biology, diversity and evolution of nucleariid amoebae (Amorphea, Obazoa, Opisthokonta). Protist 173:125895

    Article  PubMed  Google Scholar 

  • Galindo LJ, Torruella G, Moreira D et al (2019) Combined cultivation and single-cell approaches to the phylogenomics of nucleariid amoebae, close relatives of fungi. Philos Trans R Soc B 374:20190094

    Article  CAS  Google Scholar 

  • Galindo LJ, López-García P, Torruella G et al (2021) Phylogenomics of a new fungal phylum reveals multiple waves of reductive evolution across Holomycota. Nat Commun 12:4973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galindo LJ, Torruella G, López-García P et al (2022) Phylogenomics supports the monophyly of aphelids and fungi and identifies new molecular synapomorphies. Syst Biol. https://doi.org/10.1093/sysbio/syac054

  • Gams H (1947) Die Protochlorinae als autotrophe Vorfahren von Pilzen und Tieren? Mikroskopie 2:383–387

    Google Scholar 

  • Gawryluk RMR, Tikhonenkov DV, Hehenberger E et al (2019) Non-photosynthetic predators are sister to red algae. Nature 572:241–243

    Article  Google Scholar 

  • Gill EE, Fast NM (2006) Assessing the microsporidia-fungi relationship: combined phylogenetic analysis of eight genes. Gene 375:103–109

    Article  CAS  PubMed  Google Scholar 

  • Glockling SL, Marshall WL, Gleason FH (2013) Phylogenetic interpretations and ecological potentials of the Mesomycetozoae (Ichthyosporea). Fungal Ecol 6:237–247

    Article  Google Scholar 

  • González-Hernández M, Denoël M, Duffus AJL et al (2010) Dermocystid infection and associated skin lesions in free-living palmate newts (Lissotriton helveticus) from Southern France. Parasitol Int 59:344–350

    Article  PubMed  Google Scholar 

  • Gouy M, Li W-H (1989) Molecular phylogeny of the kingdoms Animalia, Plantae and Fungi. Mol Biol Evol 6:109–122

    CAS  PubMed  Google Scholar 

  • Grau-Bové X, Torruella G, Donachie S et al (2017) Dynamics of genomic innovation in the unicellular ancestry of animals. elife 6:e26036

    Article  PubMed  PubMed Central  Google Scholar 

  • Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481

    Article  CAS  PubMed  Google Scholar 

  • Grobben K (1908) Die systematische Einteilung des Tierreiches, vol 58. Verhandlungen der kaiserlich-königlichen zoologisch-botanischen Gesellschaft in Wien, Vienna, pp 491–511

    Google Scholar 

  • Gromov BV (2000) Algal parasites of the genera Aphelidium, Amoeboaphelidium and Pseudoaphelidium from the Cienkovski’s “Monadinea” group as representatives of new class. Zool Zhurn 79:517–525

    Google Scholar 

  • Haag KL, James TY, Pombert J-F, Larsson R, Schaer TMM, Refardt D, Ebert D (2014) Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. Proc Natl Acad Sci U S A 111:15480–15485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hampl V, Hug L, Leigh JW et al (2009) Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups”. Proc Natl Acad Sci U S A 106:3859–3864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa M, Hashimoto T, Adachi J et al (1993) Early branchings in the evolution of eukaryotes: ancient divergence of Entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol 36:380–388

    Article  CAS  PubMed  Google Scholar 

  • Hatschek B (1888) Lehrbuch der Zoologie: eine morphologische Übersicht des Thierreiches zur Einführung in das Studium dieser Wissenschaft. Georg Fischer, Jena

    Google Scholar 

  • He D, Fiz-Palacios O, Fu C-J et al (2014) An alternative root for the eukaryotic tree of life. Curr Biol 24:456–470

    Article  Google Scholar 

  • Hehenberger E, Tikhonenkov DV, Kolisko M et al (2017) Novel predators reshape Holozoan phylogeny and reveal the presence of a two-component signaling system in the ancestor of animals. Curr Biol 27:2043–2050

    Article  CAS  PubMed  Google Scholar 

  • Heiss AA, Kolisko M, Ekelund F et al (2018) Combined morphological and phylogenomic re-examination of malawimonads, a critical taxon for inferring the evolutionary history of eukaryotes. R Soc Open Sci 5:171707

    Article  PubMed  PubMed Central  Google Scholar 

  • Hendy MD, Penny D (1989) A framework for the quantitative study of evolutionary trees. Syst Zool 38:297–309

    Article  Google Scholar 

  • Herman RL (1984) Ichthyophonus-like infection in newts (Notophthalmus viridescens Rafinesque). J Wildl Dis 20:55–56

    Article  CAS  PubMed  Google Scholar 

  • Herr RA, Ajello L, Taylor JW et al (1999) Phylogenetic analysis of Rhinosporidium seeberi’s 18S small-subunit ribosomal DNA groups this pathogen among members of the protoctistan Mesomycetozoa clade. J Clin Microbiol 37:2750–2754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hertel LA, Bayne CJ, Loker ES (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 Mesomycetozoa. Int J Parasitol 32:1183–1191

    Article  CAS  PubMed  Google Scholar 

  • Hirt RP, Logsdon JM Jr, Healy B et al (1999) Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl Acad Sci U S A 96:580–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyman LH (1940) The invertebrates: protozoa through ctenophora. McGraw Hill, New York

    Google Scholar 

  • Ireland EV, Woznica A, King N (2020) Synergistic cues from diverse bacteria enhance multicellular development in a choanoflagellate. Appl Environ Microbiol 86:e02920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James TY, Berbee ML (2012) No jacket required – new fungal lineage defies dress code. BioEssays 34:94–102

    Article  CAS  PubMed  Google Scholar 

  • James TY, Kauff F, Schoch L et al (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443:818–822

    Article  CAS  PubMed  Google Scholar 

  • James TY, Pelin A, Bonen L et al (2013) Shared signatures of parasitism and phylogenomics unite Cryptomycota and Microsporidia. Curr Biol 23:1548–1553

    Article  CAS  PubMed  Google Scholar 

  • James TY, Stajich JE, Hittinger CT, Rokas A (2020) Toward a fully resolved fungal tree of life. Annu Rev Microbiol 74:291–313

    Article  CAS  PubMed  Google Scholar 

  • James-Clark H (1866) Note on the Infusoria Flagellata and the Spongiae Ciliatae. Am Sci 1:113–114

    Google Scholar 

  • James-Clark H (1867) On the Spongiae Ciliatae as Infusoria Flagellata; or observations on the structure, animality and relationship of Leucosolenia botryoides, Bowerbank. Ann Mag Nat Hist 1:133–142

    Article  Google Scholar 

  • Jiménez-Guri E, Philippe H, Okamura B, Holland PWH (2007) Buddenbrockia is a cnidarian worm. Science 317:116–118

    Article  PubMed  Google Scholar 

  • Jones MDM, Forn I, Gadelha C et al (2011) Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474:200–203

    Article  CAS  PubMed  Google Scholar 

  • Kapli P, Telford MJ (2020) Topology-dependent asymmetry in systematic errors affects phylogenetic placement of Ctenophora and Xenacoelomorpha. Sci Adv 6:eabc5162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapli P, Natsidis P, Leite DJ et al (2021) Lack of support for Deuterostomia prompts reinterpretation of the first Bilateria. Sci Adv 7:eabe2741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karpov SA, Mylnikov AP (1989) Biology and ultrastructure of colorless flagellates Apusomonadida ord. n. Zool Zhurn 68:5–17

    Google Scholar 

  • Karpov SA, Mikhailov KV, Mirzaeva GS et al (2013) Obligately phagotrophic aphelids turned out to branch with the earliest-diverging Fungi. Protist 164:195–205

    Article  PubMed  Google Scholar 

  • Karpov SA, Mamkaeva MA, Aleoshin VV et al (2014a) Morphology, phylogeny, and ecology of the aphelids (Aphelidae, Opisthokonta) and proposal for the new superphylum Opisthosporidia. Front Microbiol 5:112

    Article  PubMed  PubMed Central  Google Scholar 

  • Karpov SA, Mamkaeva MA, Benzerara K et al (2014b) Molecular phylogeny and ultrastructure of Aphelidium aff. Melosirae (Aphelida, Opisthosporidia). Protist 165:512–526

    Article  PubMed  PubMed Central  Google Scholar 

  • Karpov SA, López-Garcia P, Mamkaeva MA et al (2018) The chytrid-like parasites of algae Amoeboradix gromovi gen. et sp. nov. and Sanchytrium tribonematis belong to a new fungal lineage. Protist 169:122–140

    Article  PubMed  Google Scholar 

  • Karpov SA, Cvetkova VS, Annenkova NV, Vishnyakov AE (2019a) Kinetid structure of Aphelidium and Paraphelidium (Aphelida) suggests the features of the common ancestor of Fungi and Opisthosporidia. J Eukaryot Microbiol 55:911–924

    Article  Google Scholar 

  • Karpov SA, Vishnyakov AE, Moreira D, López-García P (2019b) The ultrastructure of Sanchytrium tribonematis (Sanchytriaceae, Fungi incertae sedis) confirms its close relationship to Amoeboradix. J Eukaryot Microbiol 66:892–898

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keeling PJ, Doolittle WF (1996) Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol Biol Evol 13:1297–1305

    Article  CAS  PubMed  Google Scholar 

  • Kennedy FA, Buggage RR, Ajello L (1995) Rhinosporidiosis: a description of an unprecedented outbreak in captive swans (Cygnus spp.) and a proposal for revision of the ontogenic nomenclature of Rhinosporidium seeberi. J Med Vet Mycol 33:157–165

    Article  CAS  PubMed  Google Scholar 

  • Kent WS (1878) A new field for the microscopist. Pop Sci Rev 2:113–132

    Google Scholar 

  • Kent WS (1880–1882) A manual of the Infusoria, vol 1–3. D Bogue, London

    Google Scholar 

  • Kerk D, Gee A, Standish M, Wainwright PO 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 122:187–192

    Article  Google Scholar 

  • Kim E, Simpson AGB, Graham LE (2006) Evolutionary relationships of apusomonads inferred from taxon-rich analyses of 6 nuclear encoded genes. Mol Biol Evol 23:2455–2466

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi M, Wada H, Satoh N (1996) Early evolution of the Metazoa and phylogenetic status of diploblasts as inferred from amino acid sequence of Elongation Factor-1. Mol Phylo Evol 5:414–422

    Article  CAS  Google Scholar 

  • Koźyczkowska A, Najle S, Ocaña-Pallarès E et al (2021) Stable transfection in protist Corallochytrium limacisporum identifies novel cellular features among unicellular animals relatives. Curr Biol 31:1–7

    Article  Google Scholar 

  • Lang BF, O’Kelly C, Nerad T et al (2002) The closest unicellular relatives of Animals. Curr Biol 12:1773–1778

    Article  CAS  PubMed  Google Scholar 

  • Lapage G (1925) Notes on the choanoflagellate, Codosiga botrytis, Ehrbg. Q J Microsc Sci 69:471–508

    Google Scholar 

  • Lara E, Moreira D, López-Garcia P (2009) The environmental clade LKM11 and Rozella form the deepest branching clade of Fungi. Protist 161:116–121

    Article  PubMed  Google Scholar 

  • Laumer CE, Fernández R, Lemer S et al (2019) Revisiting metazoan phylogeny with genomic sampling of all phyla. Proc R Soc B 286:20190831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laundon D, Larson BT, McDonald K et al (2019) The architecture of cell differentiation in choanoflagellates and sponge choanocytes. PLoS Biol 17:e3000226

    Article  PubMed  PubMed Central  Google Scholar 

  • Lax G, Eglit Y, Eme L et al (2018) Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes. Nature 564:410–414

    Article  CAS  PubMed  Google Scholar 

  • Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320

    Article  CAS  PubMed  Google Scholar 

  • Leadbeater BSC (1983) Distribution and chemistry of microfilaments in choanoflagellates, with special reference to the collar and other tentacle systems. Protistologica 19:157–166

    CAS  Google Scholar 

  • Leadbeater BSC (2008a) Choanoflagellate evolution: the morphological perspective. Protistology 5:256–267

    Google Scholar 

  • Leadbeater BSC (2008b) Choanoflagellate lorica construction and assembly: The nudiform condition. I. Savillea species. Protist 159:259–268

    Article  PubMed  Google Scholar 

  • Leadbeater BSC (2010) Choanoflagellate lorica construction and assembly: The tectiform condition. Volkanus costatus (=Diplotheca costata). Protist 161:160–176

    Article  PubMed  Google Scholar 

  • Leadbeater BSC (2015) The Choanoflagellates: evolution, biology and ecology. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Leadbeater BSC, Hassan R, Nelson M et al (2008) A new genus, Helgoeca gen. nov., for a nudiform choanoflagellate. Eur J Protistol 44:227–237

    Article  PubMed  Google Scholar 

  • Leadbeater BSC, Yu QB, Kent J, Stekel DJ (2009) Three-dimensional images of choanoflagellate loricae. Proc R Soc B 276:3–11

    Article  PubMed  Google Scholar 

  • Letcher PM, Powell MJ (2018) A taxonomic summary and revision of Rozella (Cryptomycota). IMA Fungus 9:383–399

    Article  PubMed  PubMed Central  Google Scholar 

  • Letcher PM, Powell MJ (2019) A taxonomic summary of Aphelidiaceae. IMA Fungus 10:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Letcher PM, Lopez S, Schmieder R et al (2013) Characterization of Amoeboaphelidium protococcarum, an algal parasite new to the Cryptomycota isolated from an outdoor algal pond used for the production of biofuel. PLoS One 8:e56232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lichtwardt RW (1986) The Trichomycetes: Fungal associates of arthropods. Springer, New York

    Book  Google Scholar 

  • Lighthill J (1976) Flagellar hydrodynamics. SIAM Rev 18:161–230

    Article  Google Scholar 

  • Logares R, Bråte J, Bertilsson S et al (2009) Infrequent marine-freshwater transitions in the microbial world. Trends Microbiol 17:414–422

    Article  CAS  PubMed  Google Scholar 

  • Lohr JN, Laforsch C, Koerner H, Wolinsk J (2010) A Daphnia parasite (Caullerya mesnili) constitutes a new member of the Ichthyosporea, a group of protists near the animal-fungi divergence. J Eukaryot Microbiol 57:328–336

    Article  CAS  PubMed  Google Scholar 

  • López-Escardó D, López-García P, Moreira D et al (2017) Parvularia atlantis gen. et sp. nov., a nucleariid filose amoeba (Holomycota, Opisthokonta). J Eukaryot Microbiol 65:170–179

    Article  PubMed  Google Scholar 

  • López-Escardó D, Grau-Bové X, Guillaumet-Adkins A et al (2019) Reconstruction of protein domain evolution using single-cell amplified genomes of uncultured choanoflagellates sheds light on the origin of animals. Philos Trans R Soc B 374:20190088

    Article  Google Scholar 

  • Lord JC, Hartzer KL, Kambhampati S (2012) A nuptially transmitted ichthyosporean symbiont of Tenebrio molitor (Coleoptera: Tenebrionidae). J Eukaryot Microbiol 59:246–250

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Ocaña-Pallarès E, López-Escardó D et al. (2020) Revisiting the phylogenetics position of Caullerya mesnili (Ichthyosporea), a common Daphnia parasite, based on 22 protein-coding genes. Mol Phylogenet Evol 151:106891

    Google Scholar 

  • Mah JL, Christensen-Dalsgaard C, Leys SP (2014) Choanoflagellate and choanocyte collar-flagellar systems and the assumption of homology. Evol Dev 16:25–37

    Article  CAS  PubMed  Google Scholar 

  • Malakhov VV (2016) Symmetry and the tentacular apparatus in Cnidaria. Russ J Mar Biol 42:287–298

    Article  Google Scholar 

  • Maldonado M (2004) Choanoflagellates, choanocytes, and animal multicellularity. Invert Biol 123:1–22

    Article  Google Scholar 

  • Manton I, Bremer G, Oates K (1981) Problems of structure and biology in a large collared flagellate (Diaphanoeca grandis Ellis) from Arctic Seas. Proc R Soc B 213:15–26

    Google Scholar 

  • Marshall WL, Berbee ML (2011) Facing unknowns: living cultures (Pirum gemmate 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 162:33–57

    Article  PubMed  Google Scholar 

  • Marshall WL, Berbee ML (2013) Comparative morphology and genealogical delimitation of cryptic species of sympatric isolates of Sphaeroforma (Ichthyosporea, Opisthokonta). Protist 164:287–311

    Article  PubMed  Google Scholar 

  • Matriano DM, Alegado RA, Conaco C (2021) Detection of horizontal gene transfer in the genome of the choanoflagellate Salpingoeca rosetta. Sci Rep UK 11:5993

    Article  CAS  Google Scholar 

  • Matus DQ, Pang K, Marlow H et al (2006) Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc Natl Acad Sci U S A 103:11195–11200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 2:203–211

    Article  Google Scholar 

  • Medlin L, Elwood HJ, Stickel S et al (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499

    Article  CAS  PubMed  Google Scholar 

  • Mendoza L, Ajello L, Taylor JW (2001) The taxonomic status of Lacazia loboi and Rhinosporidium seeberi has been finally resolved with the use of molecular tools. Rev Iberoam Micol 18:95–98

    CAS  PubMed  Google Scholar 

  • Mendoza L, Taylor JW, Ajello L (2002) The Class Mesomycetozoa: a heterogeneous group of microorganisms at the animal–fungal boundary. Annu Rev Microbiol 56:315–344

    Article  CAS  PubMed  Google Scholar 

  • Mikrjukov KA (1999) Taxonomic revision of scale- bearing Heliozoon-like amoebae (Pompholyxophryidae, Rotosphaerida). Acta Potozool 38:119–131

    Google Scholar 

  • Minge MA, Silberman JD, Orr RJS et al (2009) Evolutionary position of breviate amoebae and the primary eukaryote divergence. Proc R Soc B 276:597–604

    Article  CAS  PubMed  Google Scholar 

  • Moroz LL, Halanych KM (2016) A sisterly dispute. Nature 529:286–287

    Article  PubMed  Google Scholar 

  • Moroz LL, Kocot KM, Citarella MR et al (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510:109–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mylnikov AP, Tikhonenkov DV, Karpov SA, Wylezich C (2019) Microscopical studies on Ministeria vibrans Tong, 1997 (Filasterea) highlight the cytoskeletal structure of the common ancestor Filasterea, Metazoa and Choanoflagellata. Protist 170:385–396

    Article  PubMed  Google Scholar 

  • Nitsche F, Carr M, Arndt H, Leadbeater BSC (2011) Higher level taxonomy and molecular phylogenetics of the Choanoflagellatea. J Eukaryot Microbiol 58:452–462

    Article  PubMed  Google Scholar 

  • Nitsche F, Thomsen HA, Richter DJ (2017) Bridging the gap between morphological species and molecular barcodes – exemplified by loricate choanoflagellates. Eur J Protistol 57:26–37

    Article  PubMed  Google Scholar 

  • Norris RE (1965) Neustonic marine Craspedomonadales (Choanoflagellata) from Washington and California. J Protozool 12:589–612

    Article  Google Scholar 

  • Ocaña-Pallarès E, Williams TA, López-Escardó D et al (2022) Divergent genomic trajectories predate the origin of animals and fungi. Nature 609:747–753

    Article  PubMed  PubMed Central  Google Scholar 

  • Owczarzak A, Stibbs HH, Bayne CJ (1980) The destruction of Schistosoma mansoni mother sporocysts in vitro by amoebae isolated from Biomphalaria glabrata: an ultrastructural study. J Invertebr Pathol 35:26–33

    Article  CAS  PubMed  Google Scholar 

  • Page FC (1987) The classification of ‘naked’ amoebae (phylum rhizopoda). Arch Protistenkd 133:199–217

    Article  Google Scholar 

  • Paps J, Medina-Chacón LA, Marshall W, Suga H, Ruiz-Trillo I (2013) Molecular phylogeny of unikonts: new insights into the position of apusomonads and ancyromoands and the internal relationships of opisthokonts. Protist 164:2–12

    Article  PubMed  Google Scholar 

  • Parfrey LW, Lahr DJG, Knoll AH, Katz LA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci U S A 108:13624–13629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parra-Acero H, Ros-Rocher N, Perez-Posada A et al (2018) Transfection of Capsaspora owczarzaki, a close unicellular relative of animals. Development 145:dev162107

    Article  PubMed  PubMed Central  Google Scholar 

  • Pastrana CC, DeBiasse MB, Ryan JF (2019) Sponges lack ParaHox genes. Genome Bio Evol 11:1250–1257

    Article  CAS  Google Scholar 

  • Patterson DJ (1985) On the organization and affinities of the amoeba, Pompholyxophrys punicea Archer, based on ultrastructural examination of individual cells from wild material. J Eukaryot Microbiol 32:241–246

    Google Scholar 

  • Patterson DJ (1999) The diversity of eukaryotes. Am Nat 154(Suppl):S86–S124

    Google Scholar 

  • Patterson DJ, Surek B, Melkonian M (1987) The ultrastructure of Vampyrellidium perforans Surek & Melkonian and its taxonomic position among the naked filose Amoebae. J Protozool 34:63–67

    Article  Google Scholar 

  • Patterson DJ, Nygaard K, Steinberg G, Turley CM (1993) Heterotrophic flagellates and other protists associated with oceanic detritus throughout the water column in the mid North Atlantic. J Mar Biol Assoc UK 73:67–95

    Article  Google Scholar 

  • Paul M (2012) Acanthocorbis mongolica nov. spec. – description of the first freshwater loricate choanoflagellate (Acanthoecida) from a Mongolian lake. Eur J Protistol 48:1–8

    Google Scholar 

  • Pereira CN, Di Rosa I, Fagotti A et al (2005) The pathogen of frogs Amphibiocystidium ranae is a member of the order Dermocystida in the class Mesomycetozoea. J Clin Microbiol 43:192–198

    Article  PubMed  PubMed Central  Google Scholar 

  • Pettitt ME (2001) Prey capture and ingestion in choanoflagellates. PhD thesis, University of Birmingham

    Google Scholar 

  • Pettitt ME, Orme BAA, Blake JR, Leadbeater BSC (2002) The hydrodynamics of filter feeding in choanoflagellates. Eur J Protistol 38:313–332

    Article  Google Scholar 

  • Philippe H, Brinkmann H, Lavrov DV et al (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9:e1000602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philippe H, Poustka AJ, Chiodin M et al (2019) Mitigating anticipated effects of systematic errors supports sister-group relationship between Xenacoelomorpha and Amubulacraria. Curr Biol 29:1818–1826

    Article  CAS  PubMed  Google Scholar 

  • Pick KS, Philippe H, Schreiber F et al (2010) Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27:1983–1987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pisani D, Pett W, Dohrmann M et al (2015) Genomic data do not support comb jellies as the sister group to all other animals. Proc Natl Acad Sci U S A 112:15402–15407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Posada D (2003) Using Modeltest and PAUP* to select a model of nucleotide substitution, current protocols in bioinformatics. Wiley, New York

    Google Scholar 

  • Powell MJ (1984) Fine structure of the unwalled thallus of Rozella polyphagia in its host Polyphagus euglenae. Mycologia 76:1039–1048

    Article  Google Scholar 

  • Quandt CA, Beaudet D, Corsaro D et al (2017) The genome of an intracellular parasite, Paramicrosporidium saccamoebae, reveals alternative adaptations to obligate intracellular parasitism. eLife 6:e29594

    Article  PubMed  PubMed Central  Google Scholar 

  • Raffel TR, Dillard JR, Hudson PJ (2006) Field evidence for leech-borne transmission of amphibian Ichthyophonus sp. J Parasitol 92:1256–1264

    Article  PubMed  Google Scholar 

  • Ragan MA, Goggins CL, Cawthorn RJ et al (1996) A novel clade of protistan parasites near the animal–fungal divergence. Proc Natl Acad Sci U S A 93:11907–11912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghu-kumar S (1987) Occurrence of the thraustochytrid, Corallochytrium limacisporum gen. et sp. nov. in the coral reef lagoons of the Lakshadweep Islands in the Arabian Sea. Bot Mar 30:83–89

    Article  Google Scholar 

  • Rainer H (1968) Urtiere, Protozoa, Wurzelfu ̈ßler, Rhizopoda, Sonnentierchen, Heliozoa. Systematik und Taxonomie, Biologie, Verbreitung und Ökologie der Arten der Erde. In: Dahl M, Peus F (eds) Die Tierwelt Deutschlands und der angrenzenden Meeresteile, vol 56. VEB Gustav Fischer Verlag, Jena

    Google Scholar 

  • Ramaiah N (2006) A review on fungal diseases of algae, marine fishes, shrimps and corals. Indian J Mar Sci 35:380–387

    Google Scholar 

  • Ramos OM, Barker D, Ferrier DEK (2012) Ghost loci imply Hox and ParaHox existence in the last common ancestor of animals. Curr Biol 22:1951–1956

    Article  Google Scholar 

  • Reinke AW, Balla KM, Bennett EJ et al (2017) Identification of microsporidia host-exposed proteins reveals a repertoire of rapidly evolving proteins. Nat Commun 8:14023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds NK, Smith ME, Tretter ED et al (2017) Resolving relationships at the animal-fungal divergence: a molecular phylogenetic study of the protist trichomycetes (Ichthyosporea, Eccrinida). Mol Phylogenet Evol 109:447–464

    Article  CAS  PubMed  Google Scholar 

  • Richards TA, Leonard G, Wideman JG (2017) What defines the “kingdom” Fungi. Microbiol Spectr 5. https://doi.org/10.1128/microbiolspec.FUNK-0044-2017

  • Richter DJ, Fozouni P, Eisen MB, King N (2018) Gene family innovation, conversation and loss on the animal stem lineage. eLife 7:e34226

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Rouse GW, Wilson NG, Carvajal JI et al (2016) New deep-sea species of Xenoturbella and the position of Xenacoelomorpha. Nature 530:94–97

    Article  CAS  PubMed  Google Scholar 

  • Rowley JJL, Gleason FH, Andreou D et al (2013) Impacts of mesomycetozoean parasites on amphibian and freshwater fish populations. Fungal Biol Rev 27:100–111

    Article  Google Scholar 

  • Ruiz-Trillo I, Inagaki Y, Davis LA et al (2004) Capsaspora owczarzaki is an independent opisthokont lineage. Curr Biol 14:R946–R947

    Article  CAS  PubMed  Google Scholar 

  • 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 53:379–384

    Article  CAS  PubMed  Google Scholar 

  • Ryan JF, Pang K, Schnitzler CE et al (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342:1242592

    Article  PubMed  PubMed Central  Google Scholar 

  • Schilde C, Schaap P (2013) The Amoebozoa. Methods Mol Biol 983:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schiwitza S, Nitsche F (2021) A needle in the haystack – mapping sequences to morphology exemplified by the loricate choanoflagellate Enibas thessalia sp. nov. (Acanthoecida, Acanthoecidae). Protist 172:125782

    Google Scholar 

  • Sebé-Pedrós A, Irimia M, del Campo J et al (2013) Regulated aggregative multicellularity in a close unicellular relative of metazoa. eLife 2:e01287

    Article  PubMed  PubMed Central  Google Scholar 

  • Seeber GR (1900) Un nuevo esporozoario parásito del hombre. Dos casos encontrados en pólipos nasales. Graduation thesis, Facultad de Ciencias Médicas, Universidad Nacional de Buenos Aires, Buenos Aires

    Google Scholar 

  • Shalchian-Tabrizi K, Minge MA, Espelund M et al (2008) Multigene phylogeny of Choanozoa and the origin of animals. PLoS One 3:e2098

    Article  PubMed  PubMed Central  Google Scholar 

  • Simion P, Philipe H, Baurain D et al (2017) A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr Biol 27:958–967

    Article  CAS  PubMed  Google Scholar 

  • Smith DR, Kayal E, Yanagihara AA et al (2011) First complete mitochondrial genome sequence from a box jellyfish reveals a highly fragmented linear architecture and insights into telomere evolution. Genome Biol Evol 4:52–58

    Article  PubMed  PubMed Central  Google Scholar 

  • Sogabe S, Hatleberg WL, Kocot KM et al (2019) Pluripotency and the origin of animal multicellularity. Nature 570:519–522

    Article  CAS  PubMed  Google Scholar 

  • Sogin ML, Elwood HJ, Gunderson JH (1986) Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci U S A 83:1383–1387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Southworth JS, Armitage P, Fallon B et al (2018) Patterns of ancestral animal codon usage bias revealed through holozoan protists. Mol Biol Evol 35:2499–2511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Southworth JS, Grace CA, Marron AO et al (2019) A genomic survey of transposable elements in the choanoflagellate Salpingoeca rosetta reveals selection on codon usage. Mob DNA 10:44

    Article  PubMed  PubMed Central  Google Scholar 

  • Spanggaard B, Skouboe P, Rossen L et al (1996) Phylogenetic relationships of the intercellular fish pathogen Ichthyophonus hoferi, and fungi, choanoflagellates and the rosette agent. Mar Biol 126:109–115

    Article  CAS  Google Scholar 

  • Spatafora JW, Chang Y, Benny GL et al (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava M, Simakov O, Chapman J et al (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Fresenius G (1858) Beiträge zur Kenntnis mikroskopischer Organismen. Abh Senckenb Naturforsch Ges 2:211–242

    Google Scholar 

  • Stechmann A, Cavalier-Smith T (2003a) The root of the eukaryote tree pinpointed. Curr Biol 13:R665–R666

    Article  CAS  PubMed  Google Scholar 

  • Stechmann A, Cavalier-Smith T (2003b) Phylogenetic analysis of eukaryotes using heat-shock protein Hsp90. J Mol Evol 57:408–419

    Article  CAS  PubMed  Google Scholar 

  • Stampar SN, Broe MB, Macrander J et al (2019) Linear mitochondrial genoe in Anthozoa (Cnidaria): a case study in Ceriantharia. Sci Rep UK 9:6094

    Article  Google Scholar 

  • Strassert JFH, Jamy M, Mylnikov AP et al (2019) New phylogenomic analysis of the enigmatic phylum Telonemia further resolves the eukaryote tree of life. Mol Biol Evol 36:757–765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steenkamp ET, Wright J, Baldauf SL (2006) The protistan origins of animals and fungi. Mol Biol Evol 23:93–106

    Article  CAS  PubMed  Google Scholar 

  • von Stein FR (1878) Der Organismus der Infusionthiere. W. Engelmann, Leipzig

    Google Scholar 

  • Steinert M, Novikoff AB (1960) The existence of a cytostome and the occurrence of pinocytosis in the trypanosome, Trypanosoma mega. J Biophys Biochem Cytol 8:563–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stibbs HH, Owczarzak A, Bayne CJ, DeWan P (1979) Schistosome sporocyst-killing amoebae isolated from Biomphalaria glabrata. J Invertebr Pathol 33:159–170

    Article  CAS  PubMed  Google Scholar 

  • Suga H, Chen Z, de Mendoza A et al (2013) The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun 4:2325

    Article  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Tedersoo L, Sánchez-Ramírez S, Köljalg U et al (2018) High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Divers 90:135–159

    Article  Google Scholar 

  • Telford MJ (2016) Fighting over a comb. Nature 529:286

    Article  CAS  PubMed  Google Scholar 

  • Thompson LD (2016) Rhinosporidiosis. Ear Nose Throat J 95:101

    Article  PubMed  Google Scholar 

  • Thomsen HA (1982) Planktonic choanoflagellates from Disco Bugt, West Greenland, with a survey of the marine nanoplankton of the area. Meddelelser om Gronland Bioscience 8:3–35

    Google Scholar 

  • Tikhonenkov DV, Mikhailov KV, Hehenberger E et al (2020) New lineage of microbial predators adds complexity to reconstructing the evolutionary origin of animals. Curr Biol 30:4500–4509

    Article  CAS  PubMed  Google Scholar 

  • Tong SM (1997) Heterotrophic flagellates and other protists from Southampton Water, U.K. Ophelia 47:71–131

    Article  Google Scholar 

  • Toret C, Picco A, Boiero-Sanders M et al (2022) The cellular slime mold Fonticula alba forms a dynamic, multicellular collective while feeding on bacteria. Curr Biol 32:1961–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 29:531–544

    Article  CAS  PubMed  Google Scholar 

  • Torruella G, Grau-Bové X, Moreira D et al (2018) Global transcriptome analysis of the aphelid Paraphelidium tribonemae supports the phagotrophic origin of fungi. Commun Biol 1:231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torruella G, Mendoza A, Grau-Bové X et al (2015) Phylogenomics reveals convergent evolution of lifestyles in close relatives of animals and fungi. Curr Biol 25:2404–2410

    Article  CAS  PubMed  Google Scholar 

  • Trotter MJ, Whisler HC (1965) Chemical composition of the cell wall of Amoebidium parasiticum. Can J Bot 43:869e876

    Article  Google Scholar 

  • Urrutia A, Mitsi K, Foster R et al (2022) Txikispora philomaios n. sp., n. g., a micro-eukaryotic pathogen of amphipods, reveals parasitism and hidden diversity in Class Filasterea. J Eukaryot Microbiol 69:e12875

    Article  PubMed  Google Scholar 

  • Ustinova I, Krienitz L, Huss VA (2000) Hyaloraphidium curvatum is not a green alga, but a lower fungus; Amoebidium parasiticum is not a fungus, but a member of the DRIPs. Protist 151:253–262

    Article  CAS  PubMed  Google Scholar 

  • Verni F, Gualtieri P (1997) Feeding behaviour in ciliated protists. Micron 28:487–504

    Article  Google Scholar 

  • Vickerman K, Darbyshire JF, Ogden CG (1974) Apusomonas proboscidae Aléxéieff 1924, an unusual phagotrophic flagellate from soil. Arch Protistenkd 116:254–269

    Google Scholar 

  • Vischer W (1945) Über einen pilzähnlichen, autotrophen Mikroorganismus, Chlorochytridion, einige neue Protococcales und die systematische Bedeutun der Chloroplasten. Verhandlungen der Naturforschenden Gesellschaft in Basel 6:41–49

    Google Scholar 

  • Vossbrinck CR, Maddox JV, Friedman S et al (1987) Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326:411–414

    Article  CAS  PubMed  Google Scholar 

  • Wadi L, Reinke AW (2020) Evolution of microsporidia: An extremely successful group of eukaryotic intracellular parasites. PLoS Pathog 16:e1008276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wainright PO, Hinkle G, Sogin ML, Stickel SK (1993) Monophyletic origins of the Metazoa: an evolutionary link with fungi. Science 260:340–342

    Article  CAS  PubMed  Google Scholar 

  • Whelan NV, Kocot KM, Moroz LL, Halanych KM (2015) Error, signal, and the placement of Ctenophora sister to all other animals. Proc Natl Acad Sci U S A 112:5773–5578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams TA, Embley TM (2014) Archaeal “Dark Matter” and the origin of eukaryotes. Genome Biol Evol 6:474–481

    Article  PubMed  PubMed Central  Google Scholar 

  • Worley AC, Raper KB, Hohl M (1979) Fonticula alba: a new cellular slime mold (Acrasiomycetes). Mycologia 71:746–760

    Article  Google Scholar 

  • Wylezich C, Karpov SA, Mylnikov AP et al (2012) Ecologically relevant choanoflagellates collected from hypoxic water masses of the Baltic Sea have untypical mitochondrial cristae. BMC Microbiol 12:271

    Article  PubMed  PubMed Central  Google Scholar 

  • Yahalomi D, Atkinson SD, Neuhof M et al (2020) A cnidarian parasite of salmon (Myxozoa: Henneguya) lacks a mitochondrial genome. Proc Natl Acad Sci U S A 117:5358–5363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida M, Nakayama T, Inouye I (2009) Nuclearia thermophila sp. nov. (Nucleariidae), a new nucleariid species isolated from Yunoko Lake in Nikko (Japan). Eur J Protistol 45:147–155

    Article  PubMed  Google Scholar 

  • Young AD, Gillung JP (2020) Phylogenomics – principles, opportunities and pitfalls of big-data phylogenetics. Syst Entomol 45:225–247

    Article  Google Scholar 

  • Yue J, Sun G, Hu X, Huang J (2013) The scale and evolutionary significance of horizontal gene transfer in the choanoflagellate Monosiga brevicollis. BMC Genomics 14:729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaremba-Niedzwiedzka K, Caceres EF, Saw JH et al (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–358

    Article  CAS  PubMed  Google Scholar 

  • Zopf W (1885) Zur Morphologie und Biologie der niederen Pilztiere (Monadinen). University of Strasbourg, Leipzig

    Google Scholar 

  • Zwickl DJ, Hillis DM (2002) Increased taxon sampling greatly reduces phylogenetic error. Syst Biol 51:588–598

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Carr .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Carr, M., Hopkins, K., Ginger, M.L. (2023). The Protistan Origins of Animals and Fungi. In: Pöggeler, S., James, T. (eds) Evolution of Fungi and Fungal-Like Organisms. The Mycota, vol 14. Springer, Cham. https://doi.org/10.1007/978-3-031-29199-9_1

Download citation

Publish with us

Policies and ethics