Macroscopic waves, biological clocks and morphogenesis driven by light in a giant unicellular green alga
Abstract
A hallmark of self-organisation in living systems is their capacity to stabilise their own dynamics, often appearing to anticipate and act upon potential outcomes. Caulerpa brachypus is a marine green alga consisting of differentiated organs resembling leaves, stems and roots. While an individual can exceed a metre in size, it is a single multinucleated giant cell. Thus Caulerpa presents the mystery of morphogenesis on macroscopic scales in the absence of cellularization. The experiments reported here reveal self-organised waves of greenness — chloroplasts — that propagate throughout the alga in anticipation of the day-night light cycle. Using dynamical systems analysis we show that these waves are coupled to a self-sustained oscillator, and demonstrate their entrainment to light. Under constant conditions light intensity affects the natural period and drives transition to temporal disorder. Moreover, we find distinct morphologies depending on light temporal patterns, suggesting waves of chlorophyll could link biological oscillators to metabolism and morphogenesis in this giant single-celled organism.
Copyright and License
© The Author(s) 2023. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Acknowledgement
The authors thank A. Kornfeld for the computer-aided design of the 3d-printed apparatus, as well as Caltech Library Techlab and staff for 3D Printers access, materials and support. We are grateful to L.J. Schulman, M. Mussel and T. Li for stimulating discussions through various stages of the research, as well as to L. Michaeli, A.I. Flamholz, G. Manella and S.A. Wilson for helpful discussions and critical comments on the manuscript. E.A. is thankful for fruitful discussions at the SRBR2022 and EBRS2022 meetings. Distributed image processing was conducted in the Resnick High Performance Computing Center, a facility supported by Resnick Sustainability Institute at the California Institute of Technology. The laboratory of E.M.M. is supported by the Howard Hughes Medical Institute. E.A. has been awarded the Zuckerman Israeli Postdoctoral Scholar, Zuckerman STEM Leadership Program, and the Biology and Biological Engineering Divisional Fellowship, Caltech. T.J.B.L. has been awarded the Summer Undergraduate Research Fellowship (SURF), Caltech. This article is subject to HHMI's Open Access to Publications policy. HHMI lab heads have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. Pursuant to those licenses, the author-accepted manuscript of this article can be made freely available under a CC BY 4.0 license immediately upon publication.
Contributions
Conceptualisation: E.M.M proposed studying morphogenesis in Caulerpa; E.A. designed the study; Methodology: E.A. designed the experimental system and analysis; Investigation: E.A. performed the measurements; E.A. and T.J.B.L. performed computational analysis; Visualisation: E.A. and T.J.B.L.; Funding acquisition: E.M.M.; Writing—original draft: E.A.; Writing—review & editing: E.A. and E.M.M.; All authors discussed and commented on the manuscript.
Data Availability
The datasets generated and analysed during the current study are available in the figshare repository, https://doi.org/10.6084/m9.figshare.23797020.
Code Availability
All programming and computer aided analysis has been done using open-source projects, primarily tools from the Scientific Python ecosystem28: SciPy29, pandas30, IPython and JupyterLab31; image processing has been distributed using dask and xarray; visualisation has been done using HoloViz and Matplotlib. Custom computer codes used to analyse the results reported in the manuscript are available in the figshare repository, 10.6084/m9.figshare.23797020, and from the corresponding authors on reasonable request.
Conflict of Interest
The authors declare no competing interests.
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Additional details
- PMCID
- PMC10550971
- DOI
- 10.1038/s41467-023-41813-6
- Howard Hughes Medical Institute
- California Institute of Technology
- Accepted
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2023-10-04published online
- Caltech groups
- Resnick Sustainability Institute, Division of Biology and Biological Engineering