Identification of Novel Glycans in the Mucus Layer of Shark and Skate Skin

Abstract

The mucus layer covering the skin of fish has several roles, including protection against pathogens and mechanical damage. While the mucus layers of various bony fish species have been investigated, the composition and glycan profiles of shark skin mucus remain relatively unexplored. In this pilot study, we aimed to explore the structure and composition of shark skin mucus through histological analysis and glycan profiling. Histological examination of skin samples from Atlantic spiny dogfish (Squalus acanthias) sharks and chain catsharks (Scyliorhinus retifer) revealed distinct mucin-producing cells and a mucus layer, indicating the presence of a functional mucus layer similar to bony fish mucus albeit thinner. Glycan profiling using liquid chromatography–electrospray ionization tandem mass spectrometry unveiled a diverse repertoire of mostly O-glycans in the mucus of the two sharks as well as little skate (Leucoraja erinacea). Elasmobranch glycans differ significantly from bony fish, especially in being more sulfated, and some bear resemblance to human glycans, such as gastric mucin O-glycans and H blood group-type glycans. This study contributes to the concept of shark skin having unique properties and provides a foundation for further research into the functional roles and potential biomedical implications of shark skin mucus glycans.

Mass Spectrometry Analysis of Shark Skin Proteins

“…These proteins could, in principle, be from either cellular sloughing, a central process in skin physiology, or actively secreted to the mucus. The fact that more proteins were identified in spiny dogfish than catsharks is consistent with a previous study of ours in which less glycans were found in chain catshark skin and may be attributed to the tissue absorption sampling method, which was developed for teleost fish, or represent true biological differences such as a thinner mucus protein layer in chain catsharks [26]. Due to the importance of the mucus as a defense barrier, we focused our attention on the proteins that may have immune system roles.…”

“…We found mucin-5B and 5B-like (catshark, dogfish, respectively), mucin-2-like (dogfish), as well as von Willebrand factor domain (vWFD)-containing protein (dogfish, catshark), which all are large, secreted gel-forming mucins harboring a cysteine-rich domain that strengthens the mucus barrier [60]; however, the vWFD can also be found in other, non-glycosylated, proteins. Thus, despite the sharks not appearing "slimy" as bony fish, they are indeed covered by mucins albeit with a thinner layer [26]. A study from 2013 on gilthead sea bream (Sparus aurata) skin showed that mucin-2 and mucin-2-like are expressed at relatively low levels and that probiotics [61] and bacterial infection [62] increased mucin-5B expression.…”

“…Fucosylation is a glycan sugar protein modification essential to biological processes such as host-microbiota communication, viral infection or immunity [70]. We have previously shown that fucosylated glycans are common on spiny dogfish, chain catshark, and little skate skin mucus proteins [26]. Moreover, other proteins that are commonly posttranslationally modified by glycosylation including antithrombin, fibrinogen beta chain, transferrin and serotransferrin, hemoglobin subunit alpha, syndecan binding protein, and cystatin kininogen-type domain-containing protein were also identified in this study.…”