Holozoa (from
Ancient Greek ὅλος (holos) 'whole', and 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
protistsChoanoflagellata,
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.
Choanoflagellata, with around 250 species,[7] are the closest living relatives of animals. They are free-living
unicellular or
colonialflagellates that feed on
bacteria using a characteristic "collar" of
microvilli. The collar of choanoflagellates closely resembles sponge
collar cells,[8] leading to theories since the 19th century about their relatedness to
sponges.[9] The mysterious Proterospongia 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 a
blastula phase during their
embryonic development and, except for the amorphous
sponges, the formation of
germ layers and differentiated
tissues.[4]
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).[16] The choanoflagellates, animals and filastereans group together as the clade
Filozoa. Within Filozoa, the choanoflagellates and animals group together as the clade
Choanozoa.[13] Based on
phylogenetic and
phylogenomic analyses, the
cladogram of Holozoa is shown below:[17][18][6][2]
Uncertainty remains around the relationship of the two most
basal groups,
Ichthyosporea and
Pluriformea.[4] They may be
sister to each other, forming the putative clade
Teretosporea.[19] 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.[2][6]
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.[2][20]
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').[21]
Unicellular ancestry of animals
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).[7][6] For example:
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).[7]
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.[3]
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.[1]
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 (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 (namely
Filasterea since 2008,[13] and the
pluriformean species Corallochytrium and Syssomonas 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 traditional
taxonomic ranks (e.g. kingdom, phylum, class), all holozoan protists are classified as subphylum Choanofila (phylum
Choanozoa,[a] kingdom
Protozoa) while the animals are classified as a separate kingdom
Metazoa or Animalia.[26] 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.[4]
^
abThe term "
Choanozoa" has been used since 1991 by
Cavalier-Smith as a paraphyletic phylum of opisthokont protists,[27] 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.[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.
^Huldtgren T, Cunningham JA, Yin C, Stampanoni M, Marone F, Donoghue PCJ, Bengtson S (2011). "Fossilized Nuclei and Germination Structures Identify Ediacaran "Animal Embryos" as Encysting Protists". Science. 334 (6063): 1696–1699.
Bibcode:
2011Sci...334Q1696H.
doi:
10.1126/science.1209537.
PMID22194575.
S2CID39813961.
^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 in Corallochytrium and Ministeria (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.