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Nat Commun. 2019 Sep 2;10(1):3938. doi: 10.1038/s41467-019-11908-0.

The marginal cells of the Caenorhabditis elegans pharynx scavenge cholesterol and other hydrophobic small molecules.

Kamal M1,2, Moshiri H1,2, Magomedova L3, Han D2,4, Nguyen KCQ5, Yeo M1,2, Knox J1,2, Bagg R1,2, Won AM2,6,7,8, Szlapa K1,2, Yip CM2,6,7,8, Cummins CL3, Hall DH5, Roy PJ9,10,11.

Author information

1
Department of Molecular Genetics, University of Toronto, Toronto, ON, M5S 1A8, Canada.
2
The Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, ON, M5S 3E1, Canada.
3
Department of Pharmaceutical Sciences, Leslie Dan Faculty of Pharmacy, University of Toronto, 144 College Street, Toronto, ON, M5S 3M2, Canada.
4
Department of Pharmacology and Toxicology, University of Toronto, Toronto, ON, M5S 1A8, Canada.
5
Department of Neuroscience, Albert Einstein College of Medicine, New York, NY, 10461, USA.
6
Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, ON, M5S 3E1, Canada.
7
Department of Chemical Engineering and Applied Chemistry, University of Toronto, Toronto, ON, M5S 3E1, Canada.
8
Department of Biochemistry, University of Toronto, Toronto, ON, M5S 3E1, Canada.
9
Department of Molecular Genetics, University of Toronto, Toronto, ON, M5S 1A8, Canada. peter.roy@utoronto.ca.
10
The Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, ON, M5S 3E1, Canada. peter.roy@utoronto.ca.
11
Department of Pharmacology and Toxicology, University of Toronto, Toronto, ON, M5S 1A8, Canada. peter.roy@utoronto.ca.

Abstract

The nematode Caenorhabditis elegans is a bacterivore filter feeder. Through the contraction of the worm's pharynx, a bacterial suspension is sucked into the pharynx's lumen. Excess liquid is then shunted out of the buccal cavity through ancillary channels made by surrounding marginal cells. We find that many worm-bioactive small molecules (a.k.a. wactives) accumulate inside of the marginal cells as crystals or globular spheres. Through screens for mutants that resist the lethality associated with one crystallizing wactive we identify a presumptive sphingomyelin-synthesis pathway that is necessary for crystal and sphere accumulation. We find that expression of sphingomyelin synthase 5 (SMS-5) in the marginal cells is not only sufficient for wactive accumulation but is also important for absorbing exogenous cholesterol, without which C. elegans cannot develop. We conclude that sphingomyelin-rich marginal cells act as a sink to scavenge important nutrients from filtered liquid that might otherwise be shunted back into the environment.

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