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Philos Trans R Soc Lond B Biol Sci. 2020 Feb 17;375(1792):20190167. doi: 10.1098/rstb.2019.0167. Epub 2019 Dec 30.

Reorganization of complex ciliary flows around regenerating Stentor coeruleus.

Author information

1
Living Systems Institute, University of Exeter, Stocker Road, Exeter EX4 4QD, UK.
2
Marine Biological Laboratory, Physiology Course, Woods Hole, MA 02543, USA.
3
Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.
4
Department of Pathology, University of Washington, WA 98109, USA.
5
Center for Cardiovascular Biology, University of Washington, WA 98109, USA.
6
Department of Biochemistry and Biophysics, UCSF, San Francisco, CA 94143, USA.
7
Department of Biology, Vassar College, NY 12604, USA.
8
Marine Biological Laboratory, Whitman Center, Woods Hole, MA 02543, USA.
9
Department of Physics and Astronomy, Vassar College, NY 12604, USA.

Abstract

The phenomenon of ciliary coordination has garnered increasing attention in recent decades and multiple theories have been proposed to explain its occurrence in different biological systems. While hydrodynamic interactions are thought to dictate the large-scale coordinated activity of epithelial cilia for fluid transport, it is rather basal coupling that accounts for synchronous swimming gaits in model microeukaryotes such as Chlamydomonas. Unicellular ciliates present a fascinating yet understudied context in which coordination is found to persist in ciliary arrays positioned across millimetre scales on the same cell. Here, we focus on the ciliate Stentor coeruleus, chosen for its large size, complex ciliary organization, and capacity for cellular regeneration. These large protists exhibit ciliary differentiation between cortical rows of short body cilia used for swimming, and an anterior ring of longer, fused cilia called the membranellar band (MB). The oral cilia in the MB beat metachronously to produce strong feeding currents. Remarkably, upon injury, the MB can be shed and regenerated de novo. Here, we follow and track this developmental sequence in its entirety to elucidate the emergence of coordinated ciliary beating: from band formation, elongation, curling and final migration towards the cell anterior. We reveal a complex interplay between hydrodynamics and ciliary restructuring in Stentor, and highlight for the first time the importance of a ring-like topology for achieving long-range metachronism in ciliated structures. This article is part of the Theo Murphy meeting issue 'Unity and diversity of cilia in locomotion and transport'.

KEYWORDS:

Stentor; cilia coordination; ciliary flows; metachronal waves; morphogenesis; regeneration

PMID:
31884915
DOI:
10.1098/rstb.2019.0167

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