Choanoflagellata

Salpingoeca amphoridium growing on Oedogonium filaments, copyright Proyecto Agua.

Belongs within: Opisthokonta.

The Choanoflagellata are solitary or colonial protists with a collar of microvilli surrounding the base of the single flagellum (Adl et al. 2019).

Collaring choanoflagellates
Published 24 September 2022

Almost any body of water around the world is going to be home to choanoflagellates. These are small protozoans, up to about 10 µm in size, with a more or less ovoid cell crowned by a single elongate flagellum. Around the base of the flagellum is a collar of tentacle-like microvilli. Bacteria and other minute particles drawn in by the beating flagellum are captured by the microvilli and carried down to be engulfed by the cell. The outer surface of the cell is covered by a jacket of carbohydrates called the glycocalyx or by a siliceous lorica. Choanoflagellates can be found in both marine and fresh water, may be attached to the substrate or planktonic, may occur as individual cells or massed colonies. In motile cells, the flagellum extends behind the cell to provide propulsion in the same manner as an animalian sperm cell. In attached forms, the glycocalyx or lorica is extended opposite the flagellum to form a pedicel. Within colonial forms, individual cells may be held together by an extracellular matrix, filopodia or cytoplasmic bridges (Koehl 2019). Life cycles in choanoflagellates remain little known. Cells have mostly been observed to multiply via asexual division but circumstantial evidence (such as the existence of both haploid and diploid cells of a single species) indicates that sexual reproduction must happen somewhere.

Codosiga sp., copyright Daniel Stoupin.

Choanoflagellates have historically received the most attention for their close resemblance to the feeding cells of sponges. Indeed, so close is the resemblance that one genus of colonial choanoflagellates has been awarded the name Proterospongia. As a result, choanoflagellates have long been considered candidates for the closest relatives of animals among unicellular organisms*. Molecular studies have confirmed this relationship in recent years (Carr et al. 2008). Though choanoflagellates were not directly ancestral to animals, they still present a useful model for understanding how multicellularity in animals evolved.

*A competing theory was briefly touted in the 1960s that choanoflagellates were non-photosynthetic relatives of the unicellular chrysophytes (golden algae). Some authors then referred to choanoflagellates by the alternative label of ‘craspedophytes’. This proposition has now been thoroughly abandoned.

Close to 250 species of choanoflagellate have been described to date (Carr et al. 2008). However, it is questionable how accurately this reflects their diversity. Because the cellular morphology of choanoflagellates remains pretty consistent across the clade, their classification is largely based on features such as the form of the external covering or colonial configuration. However, recent studies have found that such features do not necessarily correlate with actual relationships. Colonial and solitary forms previously regarded as distinct may represent stages in the life cycle of a single species. In the species Salpingoeca rosetta, attached solitary cells release motile swimming cells that produce planktonic colonies (Koehl 2019).

Life cycle of Salpingoeca rosetta, from Koehl (2019).

Historically, choanoflagellates have been divided between three families on the basis of the cells’ external coat (Leadbeater & Thomsen 2002). In members of the Codonosigidae, the external glycocalyx was very thin, often not visible under light microscopy. In the Salpingoecidae, the glycocalyx was thickened into a sheath-like theca.  Members of the third family, the Acanthoecidae, possessed a basket-like lorica constructed of strips of silica. The Acanthoecidae were only found in marine and brackish water habitats whereas the other two families could be recognized in both marine and fresh water.

A molecular phylogenetic analysis of the choanoflagellates by Carr et al. (2008) did identify three major clades within the class but did not support the earlier classification. One of the clades did indeed correspond to the Acanthoecidae but representatives of the other two families were intermingled through the other two clades. Basal relationships between the three clades were not strongly supported so it is still uncertain whether the organic-walled choanoflagellates form a single clade relative to the siliceous group. No morphological features were identified that could separate the two organic-walled clades from each other though it is notable that only one of the clades included freshwater representatives. Adl et al. (2019) included all organic-walled choanoflagellates in a single family Salpingoecidae.

Shadowcast mount of Acanthoeca spectabilis, from Leadbeater & Thomsen (2002).

Within the Acanthoecidae, Carr et al. (2008) supported a division between two subclades that had previously been recognized as the nudiform and tectiform groups. In Adl et al. (2019), these clades are recognised respectively as separate families Acanthoecidae and Stephanoecidae. As well as certain differences in the configuration of the lorica, these subgroups can be separated by their manner of cell division. In nudiform species, new cells are expelled from the parent as naked swimmers, constructing their lorica after release. In the tectiform clade, the daughter cell is surrounded by a bundle of lorica strips as it emerges. Diversity counts suggest that the latter approach comes with advantages: though only five or six species are known from the nudiform clade, over 150 species have been described of tectiforms. It helps to give your kids a leg up if you want them to make a good start in life.

Systematics of Choanoflagellata

Characters (from Adl et al. 2019): Phagotrophic with collar of actin-supported microvilli around a single cilium; radial symmetry; solitary or colonial; flat mitochondrial cristae; ciliated basal body associated with ring or multiple arcs of cytoskeletal (cortical) microtubules, with second aciliated basal body located at an angle; fibrillar root, if present, minor and without obvious banding; central filament in kinetosome transition zone.

<==Choanoflagellata (see below for synonymy)AB19
|--AcanthoecidaAS12
| |--Acanthoecidae [Nudiformes]AB19
| | | i. s.: PolyoecaAB19
| | |--Helgoeca nana [incl. Acanthoecopsis unguiculata]CL08
| | `--+--Savillea microporaCL08
| | `--Acanthoeca Ellis 1929CL08, AB19
| | `--A. spectabilisCL08
| `--Stephanoecidae [Tectiformes]AB19
| | i. s.: AcanthocorbisAB19
| | AmoenoscopaAB19
| | ApheloecionAB19
| | Calliacantha simplexAB19, C-SC03
| | CampanoecaAB19
| | CampyloacanthaAB19
| | ConionAB19
| | CosmoecaAB19
| | CrinolinaAB19
| | CrucispinaAB19
| | DidymoecaAB19
| | KakoecaAB19
| | MonocostaAB19
| | NannoecaAB19
| | ParvicorbiculaAB19
| | PleurasigaAB19
| | PolyfibulaAB19
| | SaepiculaAB19
| | SaroecaAB19
| | SpinoecaAB19
| | SpiraloecionAB19
| | StephanacanthaAB19
| | SyndetophyllumAB19
| |--Stephanoeca Ellis 1929CL08, AB19
| | `--S. diplocostataCL08
| `--+--Diaphanoeca grandisCL08
| `--Diplotheca costataCL08
`--Salpingoecidae [Craspedida, Discostomata]AB19
| i. s.: AstrosigaAS12
| AulomonasAS12
| CladospongiaAS12
| Codonocladium candelabrumAS12, H04
| CodonosigopsisAS12
| DicraspedellaAS12
| DiploecaAS12
| DiplosigaAS12
| DiplosigopsisAS12
| LagenoecaAS12
| PachysoecaAS12
| SalpingorhizaAS12
| Sphaeroeca volvoxAS12, C-SC03
| StelexomonasAS12
| Stylochromonas minutaAS12, TS87
| HartaetosigaAB19
| MicrostomoecaAB19
| MylnosigaAB19
| StagondoecaAB19
| Desmarella [incl. Codonodesmus, Kentrosiga]AS12
| `--D. moniliformisF79
|--Salpingoeca James-Clark 1867AB19
| | i. s.: S. balatonisSX97
| | S. lagenellaSX97
| | S. oblongaSX97
| | S. rosettaPP15
| |--+--S. pyxidiumCL08
| | `--S. urceolataCL08
| `--+--S. napiformisCL08
| `--+--S. amphoridiumCL08
| `--‘Monosiga’ ovataCL08
`--+--+--Monosiga brevicollis Ruinen 1938CL08, AB19
| `--Choanoeca perplexa [incl. Proterospongia choanojuncta]CL08
`--+--+--Proterospongia haeckeliCL08, F79
| `--‘Salpingoeca’ infusionumCL08
`--CodosigaCL08 [incl. CodonosigaAS12; Codosigidae]
|--C. botrytisSX97 [=Codonosiga botrytisH04]
|--C. furcataSX97
|--C. gracilisCL08
|--C. pyriformisG84
|--C. umbellataSX97
`--C. utriculusSX97

Choanoflagellata [Choanoflagellatea, Choanoflagellea, Choanoflagellida, Choanomonada, Choanomonadea, Craspedomonadaceae, Craspedomonadina, Craspedomonadophyceae, Craspedophyceae]AB19

*Type species of generic name indicated

References

[AB19] Adl, S. M., D. Bass, C. E. Lane, J. Lukeš, C. L. Schoch, A. Smirnov, S. Agatha, C. Berney, M. W. Brown, F. Burki, P. Cárdenas, I. Čepička, L. Chistyakova, J. del Campo, M. Dunthorn, B. Edvardsen, Y. Eglit, L. Guillou, V. Hampl, A. A. Heiss, M. Hoppenrath, T. Y. James, A. Karnkowska, S. Karpov, E. Kim, M. Kolisko, A. Kudryavtsev, D. J. G. Lahr, E. Lara, L. Le Gall, D. H. Lynn, D. G. Mann, R. Massana, E. A. D. Mitchell, C. Morrow, J. S. Park, J. W. Pawlowski, M. J. Powell, D. J. Richter, S. Rueckert, L. Shadwick, S. Shimano, F. W. Spiegel, G. Torruella, N. Youssef, V. Zlatogursky & Q. Zhang. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66: 4–119.

[AS12] Adl, S. M., A. G. B. Simpson, C. E. Lane, J. Lukeš, D. Bass, S. S. Bowser, M. W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, E. Le Gall, D. H. Lynn, H. McManus, E. A. D. Mitchell, S. E. Mozley-Stanridge, L. W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C. L. Schoch, A. Smirnov & F. W. Spiegel. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59 (5): 429–493.

[CL08] Carr, M., B. S. C. Leadbeater, R. Hassan, M. Nelson & S. L. Baldauf. 2008. Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proceedings of the National Academy of Sciences of the USA 105 (43): 16641–16646.

[C-SC03] Cavalier-Smith, T., & E. E.-Y. Chao. 2003. Phylogeny of Choanozoa, Apusozoa, and other Protozoa and early eukaryote megaevolution. Journal of Molecular Evolution 56: 540–563.

[F79] Fry, W. G. 1979. Taxonomy, the individual and the sponge. In: Larwood, G., & B. R. Rosen (eds) Biology and Systematics of Colonial Organisms pp. 49–80. Academic Press: London.

[G84] Gruber, A. 1884. Die Protozoen des Hafens von Genua. Verhandlungen der Kaiserlichen Leopoldinisch-Carolinischen Deutschen Akademie der Naturforscher [Nova Acta Academiae Caesareae Leopoldino-Carolinae Germanicae Naturae Curiosorum] 46 (4): 473–539, pls 7–11.

[H04] Haeckel, E. 1899–1904. Kunstformen der Natur. Bibliographisches Institut: Leipzig und Wien.

Koehl, M. A. R. 2019. Selective factors in the evolution of multicellularity in choanoflagellates. Journal of Experimental Zoology (Molecular and Developmental Evolution) 336: 315–326.

Leadbeater, B. S. C., & H. A. Thomsen. 2002. Order Choanoflagellida Kent, 1880. In: Lee, J. J., G. F. Leedale & P. Bradbury (eds) 2002 An Illustrated Guide to the Protozoa: Organisms traditionally referred to as Protozoa, or newly discovered groups 2nd ed. vol. 1 pp. 14–38. Society of Protozoologists: Lawrence (Kansas).

[PP5] Pisani, D., W. Pett, M. Dohrmann, R. Feuda, O. Rota-Stabelli, H. Philippe, N. Lartillot & G. Wörheide. 2015. Genomic data do not support comb jellies as the sister group to all other animals. Proceedings of the National Academy of Sciences of the USA 112 (50): 15402–15407.

[SX97] Song B. & Xie P. 1997. Preliminary studies on the community structure of the planktonic protozoa from the outlet of Lake Dongting. Acta Hydrobiologica Sinica 21 (Suppl.): 60–68.

[TS87] Taylor, F. J. R., W. A. S. Sarjeant, R. A. Fensome & G. L. Williams. 1987. Standardisation of nomenclature in flagellate groups treated by both the botanical and zoological codes of nomenclature. Systematic Zoology 36 (1): 79–85.

Leave a comment

Your email address will not be published. Required fields are marked *