Wikipedia

Holozoa

Holozoa(fromAncient Greekὅλος (holos)'whole' andζῷον (zoion)'animal') is acladeof organisms that includesanimalsand their closestsingle-celledrelatives, but excludesfungiand all other organisms. Together they amount to more than 1.5 million species of purelyheterotrophicorganisms, including around 300unicellularspecies. It consists of various subgroups, namelyMetazoa(or animals) and theprotistsChoanoflagellata,Filasterea,PluriformeaandIchthyosporea.Along with fungi and some other groups, Holozoa is part of theOpisthokonta,asupergroupofeukaryotes.Choanofilawas 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.

Holozoans
Temporal range:EarlyTonian-Present
FilastereaIchthyosporeaPluriformeaChoanoflagellataChoanoflagellataAnimal
Holozoan diversity. From top left corner:Capsaspora(Filasterea),Sphaeroforma(Ichthyosporea),Syssomonas(Pluriformea),Stephanoeca(Craspedida),Salpingoeca(Acanthoecida),Apis(Animalia)
Scientific classificationEdit this classification
Domain: Eukaryota
Clade: Amorphea
Clade: Obazoa
Clade: Opisthokonta
Clade: Holozoa
Lang et al., 2002[1]
Clades[4]

Incertae sedis

Synonyms
  • ChoanofilaCavalier-Smith, 2009[5](plus animals)

The holozoan protists play a crucial role in understanding the evolutionary steps leading to the emergence ofmulticellularanimals from single-celled ancestors. Recentgenomicstudies have shed light on the evolutionary relationships between the various holozoanlineages,revealing insights into the origins ofmulticellularity.Somefossilsof possible metazoans have been reinterpreted as holozoan protists.

Characteristics

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Composition

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Holozoa is acladethat includesanimalsand their closest relatives, as well as theircommon ancestor,but excludesfungi.It is defined on abranch-basedapproach as the clade encompassing all relatives ofHomo sapiens(an animal), but notNeurospora crassa(afungus).[4]Holozoa, besides animals, primarily comprises unicellularprotistlineages of variedmorphologiessuch aschoanoflagellates,filastereans,ichthyosporeans,and the distinct generaCorallochytrium,Syssomonas,andTunicaraptor.[6][2]

  • Choanoflagellata,with around 250 species,[7]are the closest living relatives of animals. They are free-livingunicellularorcolonialflagellatesthat feed onbacteriausing 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 mysteriousProterospongiais 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 unikontumis 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]

Genetics

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The firstsequencedunicellular holozoangenomewas that ofMonosiga brevicollis,achoanoflagellate.It measures around 41.6mega–base-pairs(Mbp) and contains around 9200 codinggenes,making it comparable in size to the genome of filamentousfungi.Animal genomes are usually larger (e.g.human genome,2900 Mbp;fruit fly,180 Mbp), with some exceptions.[15]

Evolution

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Phylogeny

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Holozoa, along with a clade that containsfungiand theirprotistrelatives (Holomycota), are part of the largersupergroupof eukaryotes known asOpisthokonta.Holozoadivergedfrom 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 onphylogeneticandphylogenomicanalyses, thecladogramof Holozoa is shown below:[17][18][6][2]

Opisthokonta
1250 Mya

Uncertainty remains around the relationship of the two mostbasalgroups,IchthyosporeaandPluriformea.[4]They may besisterto each other, forming the putative cladeTeretosporea.[19]Alternatively, Ichthyosporea may be the earliest-branching of the two, while Pluriformea is sister to theFilozoaclade comprising filastereans, choanoflagellates and animals. This second outcome is morestrongly supportedafter the discovery ofSyssomonas.[2][6]

The position ofTunicaraptor,the newest holozoan member, is still unresolved. Three different phylogenetic positions ofTunicaraptorhave been obtained from analyses: as the sister group toFilasterea,as sister toFilozoa,or as the most basal group of all Holozoa.[2][20]

Environmental DNAsurveys of oceans have revealed new diverse lineages of Holozoa. Most of them nest within known groups, mainlyIchthyosporeaandChoanoflagellata.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]

Unicellular ancestry of animals

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Unicellular holozoans do not go throughanimal embryonic development,but they display developmental processes using similar molecules. Anactomyosinnetwork controls the cellularization of both anichthyosporeancoenocyte(A) and afruit flyblastoderm(B). Similarly, actomyosin contraction allows both the shaping ofchoanoflagellatecolonies(C) and thegastrulationof animalembryos.

The quest to elucidate theevolutionary origins of animalsfrom a unicellular ancestor requires an examination of the transition tomulticellularity.In the absence of afossil recorddocumenting this evolution, insights into the unicellular ancestor of animals are obtained from theanalysisof sharedgenesandgenetic pathwaysbetween 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:

Additionally, many biological processes seen in animals are already present in their unicellular relatives, such assexual reproductionandgametogenesisin thechoanoflagellateSalpingoeca rosettaand several types of multicellular differentiation.[7]

Fossil record

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A fossilized sample ofBicellum brasieri,a billion-year-old potential holozoan.

Abillion-year-oldfreshwatermicroscopicfossilnamedBicellum brasieriis possibly the earliest known holozoan. It shows two differentiatedcell typesorlife 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 migrationto 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]

ProposedEdiacaranfossil "embryos"of earlymetazoans,discovered in theDoushantuo Formation,have been reinterpreted as non-animalprotistswithin Holozoa. According to some authors, although they present possibleembryonic cleavage,they lack metazoansynapomorphiessuch as tissue differentiation and nearby juveniles or adults. Instead, its development is comparable to thegerminationstage of non-animal holozoans. They possibly represent anevolutionary gradein which palintomic cleavage (i.e. rapidcell divisionswithoutcytoplasmicgrowth in between, a characteristic of animalembryonic cleavage)[23]was the method ofdispersalandpropagation.[24]

Taxonomy

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History

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Prior to 2002, a relationship betweenChoanoflagellata,Ichthyosporeaand theanimal-fungidivergence was considered on the basis ofmorphologyandultrastructure.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 astrichomycetefungi.[1]

Holozoa was first recognized as a clade in 2002 through aphylogenomicanalysis by Franz Bernd Lang, Charles J. O'Kelly and other collaborators, as part of apaperpublished in the journalCurrent Biology.The study used completemitochondrial genomesof 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 (fromAncient Greekὅλος (holos)'whole' andζῷον (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 (namelyFilastereasince 2008,[13]and thepluriformeanspeciesCorallochytriumandSyssomonassince 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]

Classification

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Further information:Taxonomy of Protista

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 kingdomMetazoaor Animalia.[26]This classification excludes animals, even though they descend from the same common ancestor as choanofilan protists, making it aparaphyleticgroup rather than a true clade. Moderncladisticapproaches toeukaryoticclassification prioritisemonophyleticgroupings 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]

Notes

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  1. ^abThe term "Choanozoa"has been used since 1991 byCavalier-Smithas 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 renamedChoanozoato fit the clade Metazoa+Choanoflagellata.[4]

References

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  2. ^abcdefgTikhonenkov DV, Mikhailov KV, Hehenberger E, Mylnikov AP, Aleoshin VV, Keeling PJ, et al. (2020)."New Lineage of Microbial Predators Adds Complexity to Reconstructing the Evolutionary Origin of Animals".Current Biology.30(22):4500–4509.doi:10.1016/j.cub.2020.08.061.PMID32976804.
  3. ^abcStrother, Paul K.; Brasier, Martin D.; Wacey, David; Timpe, Leslie; Saunders, Martin; Wellman, Charles H. (April 2021)."A possible billion-year-old holozoan with differentiated multicellularity".Current Biology.31(12): 2658–2665.e2.doi:10.1016/j.cub.2021.03.051.PMID33852871.
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