Holozoa (from Ancient Greek ὅλος (holos)'whole' and ζῷον (zoion)'animal') is aclade of organisms that includesanimals and their closestsingle-celled relatives, but excludesfungi and all other organisms. Together they amount to more than 1.5 million species of purelyheterotrophic organisms, including around 300unicellular species. It consists of various subgroups, namelyMetazoa (or animals) and theprotistsChoanoflagellata,Filasterea,Pluriformea andIchthyosporea. Along with fungi and some other groups, Holozoa is part of theOpisthokonta, asupergroup ofeukaryotes.Choanofila was previously used as the name for a group similar in composition to Holozoa, but its usage is discouraged now because it excludes animals and is thereforeparaphyletic.
The holozoan protists play a crucial role in understanding the evolutionary steps leading to the emergence ofmulticellular animals from single-celled ancestors. Recentgenomic studies have shed light on the evolutionary relationships between the various holozoanlineages, revealing insights into the origins ofmulticellularity. Somefossils of possible metazoans have been reinterpreted as holozoan protists.
Choanoflagellata, with around 250 species,[7] are the closest living relatives of animals. They are free-livingunicellular orcolonialflagellates that feed onbacteria using a characteristic "collar" ofmicrovilli. The collar of choanoflagellates closely resembles spongecollar cells,[8] leading to theories since the 19th century about their relatedness tosponges.[9] The mysteriousProterospongia is an example of a colonial choanoflagellate that was thought to be related to the origin of sponges.[10] The affinities of the other single-celled holozoans only began to be recognized in the 1990s.[11]
Tunicaraptor unikontum is the newest discovered clade, whose position within Holozoa has yet to be resolved. It is a flagellate with a specialized "mouth" structure absent in other holozoans.[2]
Metazoa, known as animals, are multicellular organisms that sum more than 1.5 million living species.[14] They are characterized by ablastula phase during theirembryonic development and, except for the amorphoussponges, the formation ofgerm layers and differentiatedtissues.[4]
Holozoa, along with a clade that containsfungi and theirprotist relatives (Holomycota), are part of the largersupergroup of eukaryotes known asOpisthokonta. Holozoadiverged from their opisthokont ancestor around 1070 million years ago (Mya).[16] The choanoflagellates, animals and filastereans group together as the cladeFilozoa. Within Filozoa, the choanoflagellates and animals group together as the cladeChoanozoa.[13] Based onphylogenetic andphylogenomic analyses, thecladogram of Holozoa is shown below:[17][18][6][2]
Uncertainty remains around the relationship of the two mostbasal groups,Ichthyosporea andPluriformea.[4] They may besister to each other, forming the putative cladeTeretosporea.[19] Alternatively, Ichthyosporea may be the earliest-branching of the two, while Pluriformea is sister to theFilozoa clade comprising filastereans, choanoflagellates and animals. This second outcome is morestrongly supported after the discovery ofSyssomonas.[2][6]
The position ofTunicaraptor, the newest holozoan member, is still unresolved. Three different phylogenetic positions ofTunicaraptor have been obtained from analyses: as the sister group toFilasterea, as sister toFilozoa, or as the most basal group of all Holozoa.[2][20]
Environmental DNA surveys of oceans have revealed new diverse lineages of Holozoa. Most of them nest within known groups, mainlyIchthyosporea andChoanoflagellata. However, one environmental clade does not nest within any known group and is a potential new holozoan lineage. It has been tentatively named MASHOL (for 'marine small Holozoa').[21]
The quest to elucidate theevolutionary origins of animals from a unicellular ancestor requires an examination of the transition tomulticellularity. In the absence of afossil record documenting this evolution, insights into the unicellular ancestor of animals are obtained from theanalysis of sharedgenes andgenetic pathways between animals and their closest living unicellular relatives. The genetic content of these single-celled holozoans has revealed a significant discovery: many genetic characteristics previously thought as unique to animals can also be found in these unicellular relatives. This suggests that the origin of multicellular animals did not happen solely because of the appearance of new genes (i.e. innovation), but because of pre-existing genes that were adapted or utilized in new ways (i.e. co-option).[7][6] For example:
A considerable portion of animaltranscription factors (TF) is already present in unicellular holozoans, including some TF classes previously thought to be animal-specific (e.g.p53 andT-box).[7]
A fossilized sample ofBicellum brasieri, a billion-year-old potential holozoan.
Abillion-year-oldfreshwater microscopicfossil namedBicellum brasieri is possibly the earliest known holozoan. It shows two differentiatedcell types orlife cycle stages. It consists of a spherical ball of tightly packed cells (stereoblasts) enclosed in a single layer of elongatedcells. There are also two populations of stereoblasts with mixed shapes, which have been interpreted ascellular migration to the periphery, a movement that could be explained by differentialcell-cell adhesion. These occurrences are consistent with extant unicellular holozoans, which are known to form multicellular stages in complex life cycles.[3]
Prior to 2002, a relationship betweenChoanoflagellata,Ichthyosporea and theanimal-fungi divergence was considered on the basis ofmorphology andultrastructure. Early phylogenetic analyses gave contradicting results, because the amount of available DNA sequences was insufficient to yield unambiguous results. The taxonomic uncertainty was such that, for example, some Ichthyosporea were traditionally treated astrichomycete fungi.[1]
Holozoa was first recognized as a clade in 2002 through aphylogenomic analysis by Franz Bernd Lang, Charles J. O'Kelly and other collaborators, as part of apaper published in the journalCurrent Biology. The study used completemitochondrial genomes of a choanoflagellate (Monosiga brevicollis) and an ichthyosporean (Amoebidium parasiticum) to firmly resolve the position of Ichthyosporea as the sister group to Choanoflagellata+Metazoa. This clade was named Holozoa (from Ancient Greek ὅλος (holos)'whole' and ζῷον (zoion)'animal'), meaning 'whole animal', referencing the wider animal ancestry that it contains.[1]
Holozoa has since been supported as a robust clade by every posterior analysis,[20] even after the discovery of more taxa nested within it (namelyFilasterea since 2008,[13] and thepluriformean speciesCorallochytrium andSyssomonas since 2014[25] and 2017[6] respectively). As of 2019, the clade is accepted by the International Society of Protistologists, which revises the classification of eukaryotes.[4]
In classifications that use traditionaltaxonomic ranks (e.g. kingdom, phylum, class), all holozoan protists are classified as subphylumChoanofila (phylumChoanozoa,[a] kingdomProtozoa) while the animals are classified as a separate kingdomMetazoa or Animalia.[26] This classification excludes animals, even though they descend from the same common ancestor as choanofilan protists, making it aparaphyletic group rather than a true clade. Moderncladistic approaches toeukaryotic classification prioritisemonophyletic groupings over traditional ranks, which are increasingly perceived as redundant and superfluous. Because Holozoa is a clade, its use is preferred over the paraphyletic taxon Choanofila.[4]
^abThe term "Choanozoa" has been used since 1991 byCavalier-Smith as a paraphyletic phylum of opisthokont protists,[27] and the terms "Apoikozoa" and "choanimal" were proposed as names for the cladeMetazoa+Choanoflagellata. However, these terms have not been formally described or adopted, and were rejected in favor of a renamedChoanozoa to fit the clade Metazoa+Choanoflagellata.[4]
^abcdefgAdl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F, Cárdenas P, Čepička I, Chistyakova L, del Campo J, Dunthorn M, Edvardsen B, Eglit Y, Guillou L, Hampl V, Heiss AA, Hoppenrath M, James TY, Karnkowska A, Karpov S, Kim E, Kolisko M, Kudryavtsev A, Lahr DJG, Lara E, Le Gall L, Lynn DH, Mann DG, Massana R, Mitchell EAD, Morrow C, Park JS, Pawlowski JW, Powell MJ, Richter DJ, Rueckert S, Shadwick L, Shimano S, Spiegel FW, Torruella G, Youssef N, Zlatogursky V, Zhang Q (2019)."Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes".Journal of Eukaryotic Microbiology.66 (1):4–119.doi:10.1111/jeu.12691.PMC6492006.PMID30257078.
^Simpson AGB, Slamovits CH, Archibald JM (2017). "Chapter 1. Protist Diversity and Eukaryote Phylogeny". In Archibald JM, Simpson AGB, Slamovits CH (eds.).Handbook of the Protists. Vol. 1 (2 ed.). Springer International Publishing. pp. 1–22.ISBN978-3-319-28147-6.
^Brunet T, King N (2022). "The Single-Celled Ancestors of Animals: A History of Hypotheses". In Herron MD, Conlin PL, Ratcliff WC (eds.).The Evolution of Multicellularity. Evolutionary Cell Biology. CRC Press. pp. 251–278.doi:10.1201/9780429351907-17.ISBN9780429351907.
^Torruella G, de Mendoza A, Grau-Bové X, Donachie S, Pérez-Cordón G, Sitjà-Bobadilla A, Paley R, Manohar CS, Nichols K, Eme L, del Campo J (2014). "Phylotranscriptomics reveals ancient and convergent features inCorallochytrium andMinisteria (Holozoa, Opisthokonta)".Phylogeny and evolutionary perspective of Opisthokonta protists(PDF) (PhD thesis). Vol. 75. Universitat de Barcelona. pp. 1–9.
^Cavalier-Smith T (May 2013). "Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa".European Journal of Protistology.49 (2):115–178.doi:10.1016/j.ejop.2012.06.001.PMID23085100.
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