Light-regulated collective contractility in a multicellular choanoflagellate

Brunet, Thibaut; Larson, Ben T.; Linden, Tess A.; Vermeij, Mark J. A.; McDonald, Kent L.; King, Nicole

doi:10.1126/science.aay2346

Cited by 133 publications

(186 citation statements)

References 96 publications

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“…This is not generally regarded as a key factor in the origin of multicellularity in ancestors of Metazoa, but we suggest this should be considered. It is an interesting parallel that morphological and developmental changes (e.g., colony formation) in choanoflagellates can be also triggered by prey, although bacterial [94][95][96]. The functional basis for these changes requires further study, as does the relationship between the life cycle, morphology, formation of multicellular structures, and impacts of environmental change.…”

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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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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“…Moreover, S. rosetta is just one tip on the 285 choanoflagellate branch. A recent survey of 21 choanoflagellate transcriptomes revealed that choanoflagellates are at least as genetically diverse as animals (Richter et al, 2018), with other species retaining genetic pathways or exhibiting behaviors that are not found in S. rosetta (e.g., Marron et al, 2013;Leadbeater, 2015;Brunet et al, 2019). Together with future findings from S. rosetta, we anticipate that the establishment of genome editing in other choanoflagellates will 290 provide an increasingly complete portrait of the last common ancestor of choanoflagellates and animals.…”

Section: Discussionmentioning

confidence: 77%

Genome editing enables reverse genetics of multicellular development in the choanoflagellateSalpingoeca rosetta

Booth

King

2020

Preprint

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In a previous study, we established a forward genetic screen to identify genes required for multicellular development in the choanoflagellate, Salpingoeca rosetta (Levin et al., 2014). Yet, the paucity of reverse genetic tools for choanoflagellates has hampered direct tests of gene 25 function and impeded the establishment of choanoflagellates as a model for reconstructing the origin of their closest living relatives, the animals. Here we establish CRISPR/Cas9-mediated genome editing in S. rosetta by engineering a selectable marker to enrich for edited cells. We then use genome editing to disrupt the coding sequence of a S. rosetta C-type lectin gene, rosetteless, and thereby demonstrate its necessity for multicellular rosette development. This 30 work advances S. rosetta as a model system in which to investigate how genes identified from genetic screens and genomic surveys function in choanoflagellates and evolved as critical regulators of animal biology.

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“…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%

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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Light-regulated collective contractility in a multicellular choanoflagellate

Cited by 133 publications

References 96 publications

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

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

Genome editing enables reverse genetics of multicellular development in the choanoflagellateSalpingoeca rosetta

Regeneration in spongeSycon ciliatummimics postlarval development

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