Kinetid structure of choanoflagellates and choanocytes of sponges does not support their close relationship

Pozdnyakov, Igor R.; Agniya, M Sokolova; Alexander, V Ereskovsky; Karpov, Sergey A.

doi:10.21685/1680-0826-2017-11-4-6

Cited by 21 publications

(36 citation statements)

References 37 publications

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“…In conclusion, our analysis of sponge and unicellular holozoan cell transcriptomes, development and behaviour provides no support for the long-standing and widely-held hypothesis that multicellular animals evolved from an ancestor that was an undifferentiated ball of cells resembling extant choanocytes and choanoflagellates 1–4 . This conclusion is corroborated by recent studies that question the homology of choanocytes and choanoflagellates based on cell structure 27,28 . As an alternative, we posit that the ancestral metazoan cell type, regardless of its external character, had the capacity to exist in, and transition between, multiple cell states in a manner similar to modern transdifferentiating and stem cells.…”

Section: Mainsupporting

confidence: 77%

Pluripotency and the origin of animal multicellularity

Sogabe¹,

Hatleberg²,

Kocot

et al. 2019

Preprint

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Main 46The last common ancestor of all living animals appears to have possessed epithelial and 47 mesenchymal cell types that could transdifferentiate over an ontogenetic life cycle 48 ( Fig.1a) 1,4 . This capacity to develop and differentiate required a regulatory capacity to 49 control spatial and temporal gene expression, and included a diversified set of signalling 50 pathways, transcription factors, enhancers, promoters and non-coding RNAs (Fig. 1a) [5][6][7][8][9] . 51Recent analyses of the genomes and life cycles of unicellular holozoan relatives of 52 animals have revealed that the regulatory repertoire present in multicellular animals 53 largely evolved first in a unicellular ancestor ( Fig. 1a) 2,5,6 . These insights contrast with a 54 widely-held view that all animals evolved from a stem organism that was a simple ball 55 of ciliated cells 1,3,4 . Implicit in this traditional perspective is that (i) regulatory systems 56 necessary for cell differentiation evolved after the divergence of metazoan and 57 choanoflagellates lineages, and (ii) morphological features shared between 58 choanoflagellate and choanocytes are homologous and were present in the original 59 animal cell. While the former is not supported by recent data -unicellular holozoans 60 can change cell states by environmentally-induced temporal shifts in gene expression 61 ( Fig. 1a) 5,6,10-12 -the latter is contingent upon the still controversial aspect of whether 62 extant choanocytes and choanoflagellates accurately reflect the ancestral animal cell 63 type. 64To test this, we first compared cell type-specific transcriptomes 13 from the sponge 65Amphimedon queenslandica with each other, and with transcriptomes expressed during 66 the life cycles of closely-related unicellular holozoans, the choanoflagellate Salpingoeca 67 rosetta, the filasterean Capsaspora owczarzaki and the ichthyosporean Creolimax 68 fragrantissima (Fig. 1a) 10-12 . We chose three sponge somatic cell types hypothesised to 69 be homologous to cells present in the last common ancestor of contemporary Extended Data Figure 2: Percentage of KEGG cellular processes and 663 environmental information processing (i.e. cell signalling) genes present in each 664 cell type, corresponding to the number of components making up each KEGG 665 category identified. 666 a, Cellular processes genes. b, Environmental information processing (i.e. cell 667 signalling) genes. 668 669 Extended Data Figure 3: Evolutionary age of genes expressed in Amphimedon 670 queenslandica choanocytes, archeocytes and pinacocytes using different 671 expression thresholds. 672 *

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Section: Mainsupporting

confidence: 77%

Pluripotency and the origin of animal multicellularity

Sogabe¹,

Hatleberg²,

Kocot

et al. 2019

Preprint

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“…There are, however, some basic differences between sponges and choanoflagellates in how their collar and flagella interact, suggesting that choanocyte/choanoflagellate similarity might be superficial and that specific homology cannot be automatically assumed (see [71] for details). Indeed, recent ultrastructural studies on sponge choanocytes and choanoflagellates show that they are fundamentally different in many respects (see [72][73][74] for details), some of which are among the very few ultrastructural systems in eukaryotic cells considered sufficiently conservative to indicate phylogenetic relationships [75][76][77]. For example, specific features of the flagellar apparatus of the sponge Ephydatia fluviatilis are more similar to zoospores of chytrids than to choanoflagellates [78].…”

Section: Origins Of Multicellularitymentioning

confidence: 99%

“…For example, specific features of the flagellar apparatus of the sponge Ephydatia fluviatilis are more similar to zoospores of chytrids than to choanoflagellates [78]. Overall, the conclusion that sponges (and by extension all Metazoa) descend directly from a single-celled organism similar to choanoflagellates is not unambiguously supported by ultrastructure, as sometimes assumed [73].…”

Section: Origins Of Multicellularitymentioning

confidence: 99%

Insights into the origin of metazoan multicellularity from predatory unicellular relatives of animals

et al. 2020

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Background: The origin of animals from their unicellular ancestor was one of the most important events in evolutionary history, but the nature and the order of events leading up to the emergence of multicellular animals are still highly uncertain. The diversity and biology of unicellular relatives of animals have strongly informed our understanding of the transition from single-celled organisms to the multicellular Metazoa. Here, we analyze the cellular structures and complex life cycles of the novel unicellular holozoans Pigoraptor and Syssomonas (Opisthokonta), and their implications for the origin of animals. Results: Syssomonas and Pigoraptor are characterized by complex life cycles with a variety of cell types including flagellates, amoeboflagellates, amoeboid non-flagellar cells, and spherical cysts. The life cycles also include the formation of multicellular aggregations and syncytium-like structures, and an unusual diet for single-celled opisthokonts (partial cell fusion and joint sucking of a large eukaryotic prey), all of which provide new insights into the origin of multicellularity in Metazoa. Several existing models explaining the origin of multicellular animals have been put forward, but these data are interestingly consistent with one, the "synzoospore hypothesis." Conclusions: The feeding modes of the ancestral metazoan may have been more complex than previously thought, including not only bacterial prey, but also larger eukaryotic cells and organic structures. The ability to feed on large eukaryotic prey could have been a powerful trigger in the formation and development of both aggregative (e.g., joint feeding, which also implies signaling) and clonal (e.g., hypertrophic growth followed by palintomy) multicellular stages that played important roles in the emergence of multicellular animals.

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“…Another important source of information for phylogenies is the organization of the kinetids (flagellar apparatus). It has been suggested that the ultrastructure of the kinetids is useful for the phylogeny of Porifera (Pozdnyakov & Karpov, ; Pozdnyakov, Sokolova, Ereskovsky, & Karpov, , ). Conversely, we now believe that the general organization and architecture of the aquiferous system observed in previous investigations and in this work (summarized in Table ) do not corroborate the idea that these characteristics are useful to understand/construct the phylogeny of Haplosclerida.…”

Section: Discussionmentioning

confidence: 99%

Anatomy and ultrastructure of the tropical sponge Cladocroce caelum (Haplosclerida, Demospongiae)

Hora

Cavalcanti

Lanna

2018

Journal of Morphology

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The main characteristic of sponges (Porifera) is the presence of the aquiferous system-a system formed by canals and choanocyte chambers, in which the sponges carry out most of their physiological functions. Despite of the importance for the biology of the group, the knowledge about this structure is still incipient, even when morphological investigations are taken in account.Here, we investigated the anatomy and ultrastructure of the tropical demosponge Cladocroce caelum (Haplosclerida, Demospongiae) using light and electron microscopy. In the studied region, specimens of this species were repent or repent-branched, possessing one to several oscula. A uniform and reduced atrium was found just below each osculum. There was a thin ectosome and the choanosome presented meager mesohyl, but a high number of choanocyte chambers. The choanocyte chambers were rounded, and, as in other haplosclerids, they are found separated from the mesohyl by endopinacocytes, "hanging" in the inhalant canals. Even though the utility of the general organization of the aquiferous system has been advocated as a possible tool to understand the phylogeny of the group, we found that these characters might not be as useful as expected. The size of the particles ingested by the sponge and the amount of bacteria to sustain their bodies are discussed. In addition, we found that the density of choanocyte chambers was reduced when the specimens were carrying out the spermatogenesis, indicating that the reproduction may impair the filtering activity of the sponge. Our findings consist in a first step to better comprehend the physiology, development, and adaptation to the environmental conditions where the species is found.

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Kinetid structure of choanoflagellates and choanocytes of sponges does not support their close relationship

Cited by 21 publications

References 37 publications

Pluripotency and the origin of animal multicellularity

Pluripotency and the origin of animal multicellularity

Insights into the origin of metazoan multicellularity from predatory unicellular relatives of animals

Anatomy and ultrastructure of the tropical sponge Cladocroce caelum (Haplosclerida, Demospongiae)

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