Reversible Epithelial Adhesion Closes the Mouth of Beroe, a Carnivorous Marine Jelly.

Abstract

We investigated how the ctenophore Beroe, a carnivore of the marine zooplankton, keeps its mouth shut to maintain a streamlined body shape during forward swimming in search of prey. In big-mouthed, thin-walled beroids we found that mouth closure requires neither muscular nor nervous activity. Instead, mouth adhesion is due to paired strips of adhesive epithelial cells on opposing stomodaeal walls. The two joined epithelial layers make numerous close appositions interrupted by vacuolar intercellular spaces. At regions of apposition, the plasma membranes are highly folded and interdigitated with each other, and are separated by a uniform distance of about 15 nm. A dense cytoplasmic coat underlies the membranes at such appositions. Synapses of neurites are found on the basal ends of the adhesive cells. We found two orthogonally different orientations of the stomodaeal adhesive strips in B. sp. vs. B. forskali, correlated with different distributions of feeding macrocilia inside the stomodaeum. Mouth opening in response to food requires muscular contractions of the lips. However, the stomodaeal adhesive strips are not pulled apart all at once, but are peeled apart starting from a site of vigorous muscular tension. The mouth re-seals after feeding, or after being experimentally pulled open, showing that tissue adhesion is functionally reversible. Epithelial adhesion in Beroe appears to be a useful method for closing the mouth and streamlining the body of a gelatinous predator that spends most of its time swimming mouth-forward in search of prey. Opening of the mouth appears to be an efficient process as well, because peeling apart of the adhesive strips requires a smaller applied force than does separating them all at once. Tissue adhesion in Beroe shares many structural and functional properties with transient adhesions formed between moving cells in embryos and in culture, and may be a useful experimental system for studying the mechanisms and regulation of dynamic cell adhesions. "Loose lips Sink ships." --U. S. Navy slogan, WW II.