Holozoa

{{good article}} {{Short description|Clade containing animals and some protists}} {{Automatic taxobox | name = Holozoans | display_parents = 5 | taxon = Holozoa | authority = Lang et al., 2002<ref name="Lang et al. 2002"/> | fossil_range = {{long fossil range|1100|0|Early Tonian - Present}} | image = <imagemap> File:Holozoan_diversity_v2.png|300px rect 1 1 400 300 Filasterea rect 400 1 800 300 Ichthyosporea

rect 1 300 400 600 Pluriformea rect 400 300 800 600 Choanoflagellata

rect 1 600 400 900 Choanoflagellata rect 400 600 800 900 Animalia </imagemap> | image_caption = Holozoan diversity. From top left corner: ''Capsaspora'' (Filasterea), ''Sphaeroforma'' (Ichthyosporea), ''Syssomonas'' (Pluriformea), ''Stephanoeca'' (Craspedida), ''Salpingoeca'' (Acanthoecida), ''Apis'' (Animalia) | subdivision_ranks = Clades<ref name="Adl 2019"/> | subdivision = * Ichthyosporea (=Mesomycetozoea) * ''Tunicaraptor''<ref name="ChoanoEvo"/> * Pluriformea ** ''Corallochytrium'' ** ''Syssomonas'' * Filozoa ** Filasterea ** Choanozoa *** Choanoflagellata *** Animalia ---- {{small|'''''Incertae sedis'''''}} *{{extinct}}''Bicellum brasieri''<ref name="Strother 2021"/> | synonyms = *Choanofila {{au|Cavalier-Smith, 2009}}<ref name="CavSmith09">{{cite journal|first1=Thomas|last1=Cavalier-Smith|date=2009|title=Megaphylogeny, Cell Body Plans, Adaptive Zones: Causes and Timing of Eukaryote Basal Radiations|journal=Journal of Eukaryotic Microbiology|volume=56|issue=1 |pages=26–33|doi=10.1111/j.1550-7408.2008.00373.x|pmid=19340985 |doi-access=free}}</ref> (plus animals) }} '''Holozoa''' ({{etymology|grc|ὅλος (holos)|whole||ζῷον (zoion)|animal}}) is a clade of organisms that includes animals and their closest single-celled relatives, but excludes fungi and all other organisms. Together they amount to more than 1.5 million species of purely heterotrophic organisms, including around 300 unicellular species. It consists of various subgroups, namely Metazoa (or animals) and the protists Choanoflagellata, Filasterea, Pluriformea and Ichthyosporea. Along with fungi and some other groups, Holozoa is part of the Opisthokonta, a supergroup of eukaryotes. '''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 therefore paraphyletic.

The holozoan protists play a crucial role in understanding the evolutionary steps leading to the emergence of multicellular animals from single-celled ancestors. Recent genomic studies have shed light on the evolutionary relationships between the various holozoan lineages, revealing insights into the origins of multicellularity. Some fossils of possible metazoans have been reinterpreted as holozoan protists.

== Characteristics == === Composition === Holozoa is a clade that includes animals and their closest relatives, as well as their common ancestor, but excludes fungi. It is defined on a branch-based approach as the clade encompassing all relatives of ''Homo sapiens'' (an animal), but not ''Neurospora crassa'' (a fungus).<ref name="Adl 2019"/> Holozoa, besides animals, primarily comprises unicellular protist lineages of varied morphologies such as choanoflagellates, filastereans, ichthyosporeans, and the distinct genera ''Corallochytrium'', ''Syssomonas'', and ''Tunicaraptor''.<ref name="Hehenberger-2017"/><ref name="ChoanoEvo"/>

* Choanoflagellata, with around 250 species,<ref name="Sebé-Pedrós et al. 2017"/> are the closest living relatives of animals. They are free-living unicellular or colonial flagellates that feed on bacteria using a characteristic "collar" of microvilli. The collar of choanoflagellates closely resembles sponge collar cells,<ref name="Steenkamp"/> leading to theories since the 19th century about their relatedness to sponges.<ref name="Handbook of the Protists 1"/> The mysterious ''Proterospongia'' is an example of a colonial choanoflagellate that was thought to be related to the origin of sponges.<ref name="Brunet & King 2022"/> The affinities of the other single-celled holozoans only began to be recognized in the 1990s.<ref>{{cite journal| doi=10.1073/pnas.93.21.11907| last1=Ragan | first1=Mark A.| last2=Goggin | first2=C. Louise| last3=Cawthorn | first3=Richard J.| last4=Cerenius | first4=Lage| last5=Jamieson | first5=Angela V.C.| last6=Plourde | first6=Susan M.| last7=Rand | first7=Thomas G.| last8=Söoderhäll | first8=Kenneth| last9=Gutell | first9=Robin R.| date=15 October 1996| title=A novel clade of protistan parasites near the animal-fungal divergence| journal=PNAS| volume=93 | pages=11907–11912| pmid=8876236| issue=21| pmc=38157 | bibcode=1996PNAS...9311907R | doi-access=free }}</ref>

* Ichthyosporea, also known as Mesomycetozoea and comprising around 40 species, largely consist of parasites or commensals. They interact with a diverse range of animals, from humans and fish to marine invertebrates. Most reproduce through multinucleated colonies and disperse as flagellates or amoebae.<ref name="Sebé-Pedrós et al. 2017"/>

* Filasterea is a group of 6 amoeboid species belonging to the genera ''Ministeria'', ''Pigoraptor'',<ref name="Hehenberger-2017"/> ''Capsaspora'', and ''Txikispora'',<ref name="Txikispora"/> united by the structure of their thread-like pseudopods.<ref name="pmid18461162"/>

* Pluriformea is a provisional name for the clade composed by the two species ''Corallochytrium limacisporium'' and ''Syssomonas multiformis''. These organisms have varied shapes, including cellular aggregations, amoebae, flagellates, and amoeboflagellates.<ref name="Hehenberger-2017"/>

* ''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.<ref name="ChoanoEvo"/>

* Metazoa, known as animals, are multicellular organisms that sum more than 1.5 million living species.<ref>{{cite journal|doi=10.11646/zootaxa.3703.1.3|first1=Zhi-Qiang|last1=Zhang|date=2013|journal=Zootaxa|title=Animal biodiversity: an update of classification and diversity in 2013+|volume=3703|issue=1|pages=5–11|doi-access=free}}</ref> They are characterized by a blastula phase during their embryonic development and, except for the amorphous sponges, the formation of germ layers and differentiated tissues.<ref name="Adl 2019"/>

===Genetics=== The first sequenced unicellular holozoan genome was that of ''Monosiga brevicollis'', a choanoflagellate. It measures around 41.6 mega–base-pairs (Mbp) and contains around 9200 coding genes, making it comparable in size to the genome of filamentous fungi. Animal genomes are usually larger (e.g. human genome, 2900 Mbp; fruit fly, 180 Mbp), with some exceptions.<ref name="King et al 2008">{{cite journal|vauthors=King N, Westbrook M, Young S, etal.|title=The genome of the choanoflagellate ''Monosiga brevicollis'' and the origin of metazoans|journal=Nature|volume=451|pages=783–788|date=2008|issue=7180 |doi=10.1038/nature06617|pmid=18273011 |bibcode=2008Natur.451..783K |doi-access=free|hdl=2027.42/62649|hdl-access=free|pmc=2562698}}</ref>

== Evolution == === Phylogeny === Holozoa, along with a clade that contains fungi and their protist relatives (Holomycota), are part of the larger supergroup of eukaryotes known as Opisthokonta. Holozoa diverged from their opisthokont ancestor around 1070 million years ago (Mya).<ref name="Lawal 2020">{{cite journal|vauthors=Lawal HM, Schilde C, Kin K, etal.|title=Cold climate adaptation is a plausible cause for evolution of multicellular sporulation in ''Dictyostelia''|journal=Scientific Reports|volume=10|article-number=8797|date=2020|issue=1 |doi=10.1038/s41598-020-65709-3|doi-access=free|pmid=32472019 |pmc=7260361 |bibcode=2020NatSR..10.8797L }}</ref> The choanoflagellates, animals and filastereans group together as the clade Filozoa. Within Filozoa, the choanoflagellates and animals group together as the clade Choanozoa.<ref name="pmid18461162"/> Based on phylogenetic and phylogenomic analyses, the cladogram of Holozoa is shown below:<ref name="Parfrey-2011"/><ref name="Torruella-2015"/><ref name="Hehenberger-2017"/><ref name="ChoanoEvo"/>

{{Clade|style=font-size:90%;|label1=Opisthokonta|sublabel1=1250 Mya|1={{clade |label1=Holomycota|sublabel1=1110 Mya|1={{clade |1=Cristidiscoidea 50px |2=Fungi 60px }} |label2='''Holozoa'''|sublabel2=1070 Mya|2={{clade |label1=Ichthyosporea|bar1=blue|1={{clade |1=Dermocystida 50px |2=Ichthyophonida 50 px }} |label2=Pluriformea|bar2=blue|state2=dashed|2={{clade |2=''Syssomonas'' 60px |1=''Corallochytrium'' 50px }} |3=''Tunicaraptor''|state3=dashed |label4=Filozoa|4={{clade |1=Filasterea 60 px |label2=Choanozoa |sublabel2=960 Mya |2={{clade |1=Choanoflagellata 50px |2={{clade|sublabel1=''multicellularity''|1=Metazoa 50px}} }} }} }} }} |grouplabel1={{clade labels|label1=Teretosporea|top1=40%}} }}

Uncertainty remains around the relationship of the two most basal groups, Ichthyosporea and Pluriformea.<ref name="Adl 2019"/> They may be sister to each other, forming the putative clade Teretosporea.<ref name="Grau-Bové 2017">{{cite journal|first1=Xavier|last1=Grau-Bové|first2=Guifré|last2=Torruella|first3=Stuart|last3=Donachie|first4=Hiroshi|last4=Suga|first5=Guy |last5=Leonard|first6=Thomas A|last6=Richards|first7=Iñaki|last7=Ruiz-Trillo|date=2017|title=Dynamics of genomic innovation in the unicellular ancestry of animals|journal=eLife|volume=6|article-number=e26036|doi=10.7554/eLife.26036|doi-access=free|pmid=28726632 |pmc=5560861}}</ref> Alternatively, Ichthyosporea may be the earliest-branching of the two, while Pluriformea is sister to the Filozoa clade comprising filastereans, choanoflagellates and animals. This second outcome is more strongly supported after the discovery of ''Syssomonas''.<ref name="ChoanoEvo"/><ref name="Hehenberger-2017"/>

The position of ''Tunicaraptor'', the newest holozoan member, is still unresolved. Three different phylogenetic positions of ''Tunicaraptor'' have been obtained from analyses: as the sister group to Filasterea, as sister to Filozoa, or as the most basal group of all Holozoa.<ref name="ChoanoEvo"/><ref name="Ros-Rocher 2021"/>

Environmental DNA surveys of oceans have revealed new diverse lineages of Holozoa. Most of them nest within known groups, mainly Ichthyosporea and Choanoflagellata. 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').<ref>{{cite journal|first1=Alicia S|last1=Arroyo|first2=Romain|last2=Lannes|first3=Eric|last3=Bapteste|first4=Iñaki |last4=Ruiz-Trillo|title=Gene Similarity Networks Unveil a Potential Novel Unicellular Group Closely Related to Animals from the ''Tara'' Oceans Expedition|journal=Genome Biology and Evolution|volume=12|issue=9|date=September 2020|pages=1664–1678|doi=10.1093/gbe/evaa117|doi-access=free|pmid=32533833 |pmc=7533066}}</ref>

=== Unicellular ancestry of animals === [[File:RG347357480 Fig1.png|thumb|upright=2|Unicellular holozoans do not go through animal embryonic development, but they display developmental processes using similar molecules. An actomyosin network controls the cellularization of both an ichthyosporean coenocyte (A) and a fruit fly blastoderm (B). Similarly, actomyosin contraction allows both the shaping of choanoflagellate colonies (C) and the gastrulation of animal embryos.]] The quest to elucidate the evolutionary origins of animals from a unicellular ancestor requires an examination of the transition to multicellularity. In the absence of a fossil record documenting this evolution, insights into the unicellular ancestor of animals are obtained from the analysis of shared genes and genetic 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).<ref name="Sebé-Pedrós et al. 2017"/><ref name="Hehenberger-2017"/> For example:

* Adhesion proteins are necessary in allowing cells to stick to each other and to the extracellular matrix, forming layers and tissues in animals. Some unicellular holozoans, like choanoflagellates and filastereans, possess genes that encode proteins involved in cell-cell adhesion and cell-matrix adhesion (e.g. cadherin and integrin, respectively). Other genes, however, seem to be exclusively found in animals (e.g. β-catenin).<ref name="Sebé-Pedrós et al. 2017"/>

* ECM-related proteins, involved in the formation of the extracellular matrix, are present in other holozoans (e.g. laminins, collagens and fibronectins).<ref name="Suga et al. 2013"/>

*Signal transduction proteins are another requirement for metazoan multicellularity. Some animal cytoplasmic tyrosine kinases (such as focal adhesion kinase) and the Hippo signaling pathway are present in unicellular holozoans. Other signaling pathways highly conserved in animals (e.g. Hedgehog, WNT, TGFβ, JAK-STAT and Notch) are absent in other holozoans, but similar signaling receptors evolved independently in choanoflagellates, filastereans and ichthyosporeans (e.g. receptor tyrosine kinases).<ref name="Sebé-Pedrós et al. 2017"/> *A considerable portion of animal transcription factors (TF) is already present in unicellular holozoans, including some TF classes previously thought to be animal-specific (e.g. p53 and T-box).<ref name="Sebé-Pedrós et al. 2017"/>

Additionally, many biological processes seen in animals are already present in their unicellular relatives, such as sexual reproduction and gametogenesis in the choanoflagellate ''Salpingoeca rosetta'' and several types of multicellular differentiation.<ref name="Sebé-Pedrós et al. 2017"/>

=== Fossil record === [[File:Naked stereoblasts of billion-years-old Bicellum Brasieri.jpg|thumb|A fossilized sample of ''Bicellum brasieri'', a billion-year-old potential holozoan.]] A billion-year-old freshwater microscopic fossil named ''Bicellum brasieri'' is possibly the earliest known holozoan. It shows two differentiated cell types or life cycle stages. It consists of a spherical ball of tightly packed cells (stereoblasts) enclosed in a single layer of elongated cells. There are also two populations of stereoblasts with mixed shapes, which have been interpreted as cellular migration to the periphery, a movement that could be explained by differential cell-cell adhesion. These occurrences are consistent with extant unicellular holozoans, which are known to form multicellular stages in complex life cycles.<ref name="Strother 2021"/>

Proposed Ediacaran fossil "embryos" of early metazoans, discovered in the Doushantuo Formation, have been reinterpreted as non-animal protists within Holozoa. According to some authors, although they present possible embryonic cleavage, they lack metazoan synapomorphies such as tissue differentiation and nearby juveniles or adults. Instead, its development is comparable to the germination stage of non-animal holozoans. They possibly represent an evolutionary grade in which palintomic cleavage (i.e. rapid cell divisions without cytoplasmic growth in between, a characteristic of animal embryonic cleavage)<ref>{{cite journal|title=Cell differentiation and germ–soma separation in Ediacaran animal embryo-like fossils|vauthors=Chen L, Xiao S, Pang K, Zhou C, Yuan X|pages=238–241|date=September 2014|journal=Nature|volume=516|issue=7530 |doi=10.1038/nature13766|pmid=25252979 |bibcode=2014Natur.516..238C |s2cid=4448316 }}</ref> was the method of dispersal and propagation.<ref name="Huldtgren et al. 2011"/>

== Taxonomy == ===History=== Prior to 2002, a relationship between Choanoflagellata, Ichthyosporea and the animal-fungi divergence was considered on the basis of morphology and ultrastructure. 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 as trichomycete fungi.<ref name="Lang et al. 2002"/>

Holozoa was first recognized as a clade in 2002 through a phylogenomic analysis by Franz Bernd Lang, Charles J. O'Kelly and other collaborators, as part of a paper published in the journal ''Current Biology''. The study used complete mitochondrial 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 ({{etymology|grc|ὅλος (holos)|whole||ζῷον (zoion)|animal}}), meaning 'whole animal', referencing the wider animal ancestry that it contains.<ref name="Lang et al. 2002"/>

Holozoa has since been supported as a robust clade by every posterior analysis,<ref name="Ros-Rocher 2021"/> even after the discovery of more taxa nested within it (namely Filasterea since 2008,<ref name="pmid18461162"/> and the pluriformean species ''Corallochytrium'' and ''Syssomonas'' since 2014<ref>{{cite thesis|vauthors=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|chapter=Phylotranscriptomics reveals ancient and convergent features in ''Corallochytrium'' and ''Ministeria'' (Holozoa, Opisthokonta)|title=Phylogeny and evolutionary perspective of Opisthokonta protists|date=2014|volume=75|pages=1–9|publisher=Universitat de Barcelona|url=https://www.tdx.cat/bitstream/handle/10803/286509/GTiC_PhD_THESIS.pdf?sequence=2.txt#page=80|degree=PhD}}</ref> and 2017<ref name="Hehenberger-2017"/> respectively). As of 2019, the clade is accepted by the International Society of Protistologists, which revises the classification of eukaryotes.<ref name="Adl 2019" />

===Classification=== {{further|Taxonomy of Protista}} In classifications that use traditional taxonomic ranks (e.g. kingdom, phylum, class), all holozoan protists are classified as subphylum '''Choanofila''' (phylum Choanozoa,{{efn|name=Choanozoa}} kingdom Protozoa) while the animals are classified as a separate kingdom Metazoa or Animalia.<ref name="CavSmith 2021">{{cite journal|vauthors=Cavalier-Smith T|title=Ciliary transition zone evolution and the root of the eukaryote tree: implications for opisthokont origin and classification of kingdoms Protozoa, Plantae, and Fungi|journal=Protoplasma|date=May 2022|volume=259|issue=3|pages=487–593|doi=10.1007/s00709-021-01665-7|pmid=34940909|pmc=9010356 |bibcode=2022Prpls.259..487C }}</ref> This classification excludes animals, even though they descend from the same common ancestor as choanofilan protists, making it a paraphyletic group rather than a true clade. Modern cladistic approaches to eukaryotic classification prioritise monophyletic 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.<ref name="Adl 2019" />

*'''Holozoa''' {{au|Lang et al. 2002}} **Incertae sedis: {{extinct}}''Bicellum brasieri'' {{au|Strother & Wellman 2021}}<ref name="Strother 2021"/> **''Tunicaraptor'' {{au|Tikhonenkov, Mikhailov, Hehenberger, Karpov, Prokina, Esaulov, Belyakova, Mazei, Mylnikov, Aleoshin & Keeling 2020}}<ref name="ChoanoEvo"/> **Ichthyosporea {{au|Cavalier-Smith 1998}} [Mesomycetozoea {{au|Mendoza et al. 2002}}] ***Dermocystida {{au|Cavalier-Smith 1998}} ***Ichthyophonida {{au|Cavalier-Smith 1998}} **Pluriformea {{au|Hehenberger et al. 2017}} ***''Corallochytrium'' {{au|Raghu-Kumar 1987}} ***''Syssomonas'' {{au|Tikhonenkov, Hehenberger, Mylnikov & Keeling 2017}} **Filozoa {{au|Shalchian-Tabrizi et al. 2008}} ***Filasterea {{au|Shalchian-Tabrizi et al. 2008}} ****''Capsaspora'' {{au|Hertel, Bayne & Loker, 2002}} ****''Ministeria'' {{au|Patterson et al. 1993}} ****''Pigoraptor'' {{au|Tikhonenkov et al. 2017}} ****''Txikispora'' {{au|Urrutia, Feist & Bass 2022}}<ref name="Txikispora"/> ***Choanozoa {{au|Brunet & King 2017}} [Choanozoa {{au|Cavalier-Smith et al. 1991}} (P)]{{efn|name=Choanozoa|The term "Choanozoa" has been used since 1991 by Cavalier-Smith as a paraphyletic phylum of opisthokont protists,<ref name="Early Evo Euk"/> and the terms "Apoikozoa" and "choanimal" were proposed as names for the clade Metazoa+Choanoflagellata. However, these terms have not been formally described or adopted, and were rejected in favor of a renamed Choanozoa to fit the clade Metazoa+Choanoflagellata.<ref name="Adl 2019"/>}} ****Choanoflagellata {{au|Kent 1880–1882}} [Choanoflagellatea {{au|Cavalier-Smith 1997 emend. Cavalier-Smith 1998}}] *****Craspedida {{au|Cavalier-Smith 1997, emend. Nitsche et al. 2011}} *****Acanthoecida {{au|Cavalier-Smith 1997, emend. Nitsche et al. 2011}} ****Metazoa {{au|Haeckel 1874, emend. Adl et al. 2005}} [Animalia {{au|Linnaeus 1758}}] *****Porifera {{au|Grant 1836}} *****Placozoa {{au|Grell 1971}} *****Ctenophora {{au|Eschscholtz 1829}} *****Cnidaria {{au|Hatschek 1888}} *****Bilateria {{au|Hatschek 1888}}

==Notes== {{notelist}}

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}}

{{Eukaryota}} {{Opisthokont protists}} {{Taxonbar|from=Q1205110}}

Category:Holozoa Category:Opisthokont taxa Category:Neoproterozoic first appearances Category:Taxa described in 2002