Skip to content

Research at St Andrews

Pluripotency and the origin of animal multicellularity

Research output: Contribution to journalArticle

Open Access Status

  • Embargoed (until 12/12/19)

Author(s)

Shunsuke Sogabe, William L. Hatleberg, Kevin M. Kocot, Tahsha E. Say, Daniel Stoupin, Kathrein Roper, Selene L. Fernandez-Valverde, Sandie M. Degnan, Bernard M. Degnan

School/Research organisations

Abstract

A widely held—but rarely tested—hypothesis for the origin of animals is that they evolved from a unicellular ancestor, with an apical cilium surrounded by a microvillar collar, that structurally resembled modern sponge choanocytes and choanoflagellates1,2,3,4. Here we test this view of animal origins by comparing the transcriptomes, fates and behaviours of the three primary sponge cell types—choanocytes, pluripotent mesenchymal archaeocytes and epithelial pinacocytes—with choanoflagellates and other unicellular holozoans. Unexpectedly, we find that the transcriptome of sponge choanocytes is the least similar to the transcriptomes of choanoflagellates and is significantly enriched in genes unique to either animals or sponges alone. By contrast, pluripotent archaeocytes upregulate genes that control cell proliferation and gene expression, as in other metazoan stem cells and in the proliferating stages of two unicellular holozoans, including a colonial choanoflagellate. Choanocytes in the sponge Amphimedon queenslandica exist in a transient metastable state and readily transdifferentiate into archaeocytes, which can differentiate into a range of other cell types. These sponge cell-type conversions are similar to the temporal cell-state changes that occur in unicellular holozoans5. Together, these analyses argue against homology of sponge choanocytes and choanoflagellates, and the view that the first multicellular animals were simple balls of cells with limited capacity to differentiate. Instead, our results are consistent with the first animal cell being able to transition between multiple states in a manner similar to modern transdifferentiating and stem cells.
Close

Details

Original languageEnglish
Number of pages20
JournalNature
DOIs
Publication statusPublished - 12 Jun 2019

Discover related content
Find related publications, people, projects and more using interactive charts.

View graph of relations

Related by author

  1. Genome biology: unconventional DNA repair in an extreme genome

    Ferrier, D. E. K. & Sogabe, S., 22 Oct 2018, In : Current Biology. 28, 20, p. R1208-R1210

    Research output: Contribution to journalReview article

  2. The ontogeny of choanocyte chambers during metamorphosis in the demosponge Amphimedon queenslandica

    Sogabe, S., Nakanishi, N. & Degnan, B., 8 Mar 2016, In : EvoDevo. 7, 13 p., 6.

    Research output: Contribution to journalArticle

  3. Evolutionary origin of gastrulation: insights from sponge development

    Sogabe, S., Nakanishi, N. & Degnan, B., 28 Mar 2014, In : BMC Biology.

    Research output: Contribution to journalArticle

Related by journal

  1. Nature (Journal)

    Will Cresswell (Reviewer)
    21 Dec 2017

    Activity: Publication peer-review and editorial work typesPeer review of manuscripts

  2. Nature (Journal)

    Will Cresswell (Reviewer)
    11 Nov 2017

    Activity: Publication peer-review and editorial work typesPeer review of manuscripts

  3. Nature (Journal)

    David Gerard Dritschel (Editor)
    2005 → …

    Activity: Publication peer-review and editorial work typesEditor of research journal

  4. Nature (Journal)

    Ifor David William Samuel (Editor)
    2005 → …

    Activity: Publication peer-review and editorial work typesEditor of research journal

Related by journal

  1. Amphioxus functional genomics and the origins of vertebrate gene regulation

    Marletaz, F., Firbas, P., Maeso, I., Tena, J., Bogdanovic, O., Perry, M., Wyatt, C., de la Calle-Mustienes, E., Bertrand, S., Burguera, D., Acemel, R., van Heeringen, S., Naranjo, S., Herrera-Ubeda, C., Skvortsova, K., Jimenez-Gancedo, S., Aldea, D., Marquez, Y., Buono, L., Kozmikova, I. & 41 othersPermanyer, J., Louis, A., Albuixech-Crespo, B., Le Petillon, Y., Leon Florian, A., Subirana, L., Balwierz, P. J., Duckett, P., Farahani, E., Aury, J. M., Mangenot, S., Wincker, P., Albalat, R., Benito-Gutierrez, E., Canestro, C., Castro, F., D'Aniello, S., Ferrier, D. E. K., Huang, S., Laudet, V., Marais, G., Pontarotti, P., Schubert, M., Seitz, H., Somorjai, I. M. L., Takahashi, T., Mirabeau, O., Xu, A., Yu, J-K., Carninci, P., Martinez-Morales, J., Crollius, H., Kozmik, Z., Weirauch, M., Garcia-Fernandez, J., Lister, R., Lenhard, B., Holland, P., Escriva, H., Gomez-Skarmeta, J. L. & Irimia, M., 21 Nov 2018, In : Nature. 564, 7734, p. 64-70 29 p.

    Research output: Contribution to journalArticle

  2. An absolute sodium abundance for a cloud-free 'hot Saturn' exoplanet

    Nikolov, N., Sing, D. K., Fortney, J. J., Goyal, J. M., Drummond, B., Evans, T. M., Gibson, N. P., De Mooj, E. J. W., Rustamkulov, Z., Wakeford, H. R., Smalley, B., Burgasser, A. J., Hellier, C., Helling, C., Mayne, N. J., Madhusudhan, N., Kataria, T., Baines, J., Carter, A. L., Ballester, G. E. & 3 othersBarstow, J. K., McCleery, J. & Spake, J. J., 7 May 2018, In : Nature. 557, p. 526-529

    Research output: Contribution to journalArticle

  3. CO2 storage and release in the deep Southern Ocean on millennial to centennial timescales

    Rae, J. W. B., Burke, A., Robinson, L. F., Adkins, J. F., Chen, T., Cole, C., Greenop, R., Li, T., Littley, E., Nita, D. C., Stewart, J. A. & Taylor, B., 24 Oct 2018, In : Nature. 562, p. 569-573 16 p.

    Research output: Contribution to journalLetter

  4. Does the galaxy NGC1052-DF2 falsify Milgromian dynamics?

    Kroupa, P., Haghi, H., Javanmardi, B., Zonoozi, A. H., Mueller, O., Banik, I., Wu, X., Zhao, H. & Dabringhausen, J., 13 Sep 2018, In : Nature. 561, 7722, p. E4-E5 2 p.

    Research output: Contribution to journalComment/debate

ID: 259340991