Biophysical principles of choanoflagellate self-organization

Larson, Ben T.; Ruiz-Herrero, Teresa; Lee, Stacey; Kumar, Sanjay; Mahadevan, L.; King, Nicole

doi:10.1073/pnas.1909447117

Title: Biophysical principles of choanoflagellate self-organization

Journal Article · 01 January 2020 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1909447117 · OSTI ID:1633256

Larson, Ben T. ^[1]; Ruiz-Herrero, Teresa ^[2]; Lee, Stacey ^[3];

^[3];

^[4];

^[1]

Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Institute
Harvard Univ., Cambridge, MA (United States). Paulson School of Engineering and Applied Sciences
Univ. of California, Berkeley, CA (United States); Univ. of California, San Francisco, CA (United States)
Harvard Univ., Cambridge, MA (United States). Paulson School of Engineering and Applied Sciences and Kavli Institute for NanoBio Science and Technology

Inspired by the patterns of multicellularity in choanoflagellates, the closest living relatives of animals, we quantify the biophysical processes underlying the morphogenesis of rosette colonies in the choanoflagellate Salpingoeca rosetta. We find that rosettes reproducibly transition from an early stage of 2-dimensional (2D) growth to a later stage of 3D growth, despite the underlying variability of the cell lineages. Our perturbative experiments demonstrate the fundamental importance of a basally secreted extracellular matrix (ECM) for rosette morphogenesis and show that the interaction of the ECM with cells in the colony physically constrains the packing of proliferating cells and, thus, controls colony shape. Simulations of a biophysically inspired model that accounts for the size and shape of the individual cells, the fraction of ECM, and its stiffness relative to that of the cells suffices to explain our observations and yields a morphospace consistent with observations across a range of multicellular choanoflagellate colonies. Overall, our biophysical perspective on rosette development complements previous genetic perspectives and, thus, helps illuminate the interplay between cell biology and physics in regulating morphogenesis.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1633256

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 3 Vol. 117; ISSN 1091-6490; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Blastocoel morphogenesis: a biophysics perspective Le-Verge-Serandour, Mathieu; Turlier, Hervé arXiv https://doi.org/10.48550/arxiv.2106.14509	preprint	January 2021
Genome editing enables reverse genetics of multicellular development in the choanoflagellate Salpingoeca rosetta Booth, David S.; King, Nicole eLife, Vol. 9 https://doi.org/10.7554/elife.56193	journal	June 2020

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