Acidic Glycosaminoglycans in Marine Teleost Larvae: Evidence for a Relationship Between Composition and Negative Charge Density in Elopomorph Leptocephali

Abstract

Glycosaminoglycan (GAG) composition was determined in larvae of 10 species of true eels (subdivision Elopomorpha; order Anguilliformes; families Chlopsidae, Congridae, Moringuidae, Muraenidae and Ophichthidae), two species from the subdivision Clupeomorpha (order Clupeiformes; families Engraulidae and Clupeidae) and one species from the subdivision Euteleostei (order Aulopiformes; family Synodontidae). Using a combination of specific GAG-degrading enzymes, cellulose acetate electrophoresis with known GAG standards and relative degree of staining with Alcian Blue, the predominant GAG in anguilliform leptocephali was identified as undersulfated chondroitin sulfate (uCS); the only exception was Bathycongrus macrurus (Congridae), where heparan sulfate was tentatively identified together with uCS. In representatives of the Clupeomorpha and Euteleostei, however, the predominant GAG was chondroitin sulfate; uCS was not detected. These results, combined with those from previous studies, provide data on GAG composition in 21 species from three of the four currently recognized elopomorph orders (Albuliformes, Elopiformes and Anguilliformes). The combined data suggest that although several different body matrix GAGs have evolved in different groups of leptocephali, selection has favored GAGs (mainly uCS and keratan sulfate) with relatively low average negative charge densities (average of about one negative charge per disaccharide repeat of the acidic GAG chain). The presence of normally sulfated CS (average per disaccharide negative charge density of 2) as the major GAG in the three species of non-elopomorph larvae further suggests that some aspect of the unique developmental pattern in elopomorph leptocephali may place constraints on the maximum negative charge density permitted in the body matrix GAGs. The presence of GAGs with low negative charge density is interpreted as an additional elopomorph synapomorphy, offering further support for the view that the Elopomorpha represents a monophyletic group of fishes. Possible scenarios for the evolution of GAGs in leptocephali are presented.