Sponges as models to study emergence of complex animals

Adamska, Maja

doi:10.1016/j.gde.2016.05.026

Cited by 30 publications

(22 citation statements)

References 93 publications

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“…Several studies on unicellular relatives of animals including choanoflagellates, filastereans, and ichthyosporeans have significantly contributed to understanding how unicellular organisms transform into multicellular structures such as colonial choanoflagellate [33][34][35]. This suggests similar transitions may have taken place in the animal ancestors, which eventually evolved into a stable and functional multicellular animal [36,37]. The current hypothesis on the origin of multicellular animals generally agrees that choanoflagellates share a common ancestor with animals ( Fig.9).…”

Section: Lessons To Learn On the Origin Of Multicellularity Over The mentioning

confidence: 74%

“…This idea is based on the molecular phylogeny and morphological similarity between choanoflagellates and sponge choanocytes ( Fig.9 A-C) [38]. Further, the choanoflagellate colonies partially resemble the choanocyte chambers of the sponge [37,39,40]. In addition to their unicellular sister lineages, we also need to investigate other close relatives of the first multicellular animals.…”

Section: Lessons To Learn On the Origin Of Multicellularity Over The mentioning

confidence: 99%

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Regeneration in spongeSycon ciliatummimics postlarval development

Soubigou

Ross

Touhami

et al. 2020

Preprint

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Somatic cells dissociated from an adult sponge can re-organize and develop into a functional juvenile. However, the extent to which regeneration recapitulates embryonic developmental signaling pathways has remained enigmatic for more than a century. To this end, we have standardized and established a sponge Sycon ciliatum regeneration protocol to achieve consistent regeneration in cell culture. From the morphological analysis, we demonstrated that dissociated sponge cells follow a series of morphological events resembling embryonic and postlarval development. Hence, we propose that sponge regeneration represents somatic development. To support our hypothesis, we performed high-throughput sequencing on regenerating samples and compared the data with regular embryonic and postlarval development of Sycon ciliatum. Our comparative transcriptomic analysis illuminates that sponge regeneration is equally as dynamic as embryogenesis. We find that sponge regeneration is orchestrated by complex regulatory mechanisms by recruiting signaling pathways like those utilized in embryonic development to organize into a functional juvenile. In the current study, we lay down the basic framework to study Sycon ciliatum regeneration. Since sponges are likely to be the first branch of extant multicellular animal and the sister lineage to nearly all animals, we suggest that this system can be explored to study the genetic features underlying the evolution of multicellularity and regeneration.

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Section: Lessons To Learn On the Origin Of Multicellularity Over The mentioning

confidence: 74%

Section: Lessons To Learn On the Origin Of Multicellularity Over The mentioning

confidence: 99%

Regeneration in spongeSycon ciliatummimics postlarval development

Soubigou

Ross

Touhami

et al. 2020

Preprint

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“…The findings suggest that, in addition to nutrient acquisition, choanocytes have immune functionality. This is particularly interesting considering that the structural similarities between choanocytes and choanoflagellates, the unicellular eukaryotes that are sister group to all animals, are often discussed as a sign of homology (Maldonado 2004;Funayama 2013;Adamska 2016). This raises the interesting possibility that the ancestral continuity between innate immune defence and digestion has been preserved in sponge choanocytes.…”

Section: What Can the Sponge Tell Us About The Origin Of Immunity Andmentioning

confidence: 99%

Deciphering the genomic toolkit underlying animal-bacteria interactions – insights through the demosponge Amphimedon queenslandica

Yuen¹

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All animals are inhabited by bacteria, and maintaining homeostasis in the multicellular environment of the host involves the complex balancing act of promoting the survival of symbionts while defending against intruders. Sponges (Porifera), in addition to housing diverse bacterial symbiont assemblages, also rely on bacteria filtered from the water column for nutrition. My research uses the genome-enabled demosponge, Amphimedon queenslandica, a member of one of the earliest-diverging animal phyletic lineages, as an experimental platform to investigate the genomic toolkit underpinning animal-bacteria interactions. Using comparative bioinformatics tools, I characterised a surprisingly large and complex repertoire of innate immune receptors from the NLR family of genes encoded in the A. queenslandica genome. I then used a high throughput RNAseq approach to profile the sponge's global transcriptomic response to foreign versus its own native bacteria. Conserved metazoan innate immune pathways were activated in response to both foreign and native bacteria. However, only the native bacteria elicited the expression of a more extensive suite of signalling pathways, involving TGF-β signalling and the transcription factors NF-κB and FoxO. Upregulation of the nutrient sensor AMPK in all treatments along with immune signalling genes, which all regulate FoxO activity, further suggests an interplay between metabolic homeostasis and immunity. Finally, I used microscopy to track the cellular-level processing of the different bacteria by the sponge. Consistent with the observed transcriptional response, the native bacteria were ingested by archaeocytes more rapidly than the foreign bacteria. The slower processing of foreign bacteria also correlated with the expression of numerous Nrf2-associated detoxification genes, indicative of cellular stress, only in response to foreign bacteria.iii Deciphering the genomic tool-kit underlying animal-bacteria interactions

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“…It is not clear how an expanded developmental genetic repertoire in the ancestors of modern sponges might have been expressed phenotypically [38], and we should not necessarily expect Cambrian sponges to look more 'animal-like' than modern representatives. Even so, chancelloriids have the potential to shed light on the disparity, development and tissue complexity of early sponges, and to test hypotheses from evolutionary developmental biology of body plan homologies among metazoans [39]. A sponge affinity for chancelloriids deserves renewed consideration.…”

Section: (A) Chancelloriids As Spongesmentioning

confidence: 99%

Naked chancelloriids from the lower Cambrian of China show evidence for sponge-type growth

et al. 2018

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Chancelloriids are an extinct group of spiny Cambrian animals of uncertain phylogenetic position. Despite their sponge-like body plan, their spines are unlike modern sponge spicules, but share several features with the sclerites of certain Cambrian bilaterians, notably halkieriids. However, a proposed homology of these 'coelosclerites' implies complex transitions in body plan evolution. A new species of chancelloriid, , from the lower Cambrian (Stage 3) Chengjiang Lagerstätte is distinguished by its large size and sparse spination, with modified apical sclerites surrounding an opening into the body cavity. The sclerite arrangement in and certain other chancelloriids indicates that growth involved sclerite addition in a subapical region, thus maintaining distinct zones of body sclerites and apical sclerites. This pattern is not seen in halkieriids, but occurs in some modern calcarean sponges. With scleritome assembly consistent with a sponge affinity, and in the absence of cnidarian- or bilaterian-grade features, it is possible to interpret chancelloriids as sponges with an unusually robust outer epithelium, strict developmental control of body axis formation, distinctive spicule-like structures and, by implication, minute ostia too small to be resolved in fossils. In this light, chancelloriids may contribute to the emerging picture of high disparity among early sponges.

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Sponges as models to study emergence of complex animals

Cited by 30 publications

References 93 publications

Regeneration in spongeSycon ciliatummimics postlarval development

Regeneration in spongeSycon ciliatummimics postlarval development

Deciphering the genomic toolkit underlying animal-bacteria interactions – insights through the demosponge Amphimedon queenslandica

Naked chancelloriids from the lower Cambrian of China show evidence for sponge-type growth

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