Abstract
Echinoderms are among the most primitive deuterostomes and have been used as model organisms to understand chordate biology because of their close evolutionary relationship to this phylogenetic group. However, there are almost no data available regarding the N-glycomic capacity of echinoderms, which are otherwise known to produce a diverse set of species-specific glycoconjugates, including ones heavily modified by fucose, sulfate, and sialic acid residues. To increase the knowledge of diversity of carbohydrate structures within this phylum, here we conducted an in-depth analysis of N-glycans from a brittle star (Ophiactis savignyi) as an example member of the class Ophiuroidea. To this end, we performed a multi-step N-glycan analysis by HPLC and various exoglyosidase and chemical treatments in combination with MALDI-TOF MS and MS/MS. Using this approach, we found a wealth of hybrid and complex oligosaccharide structures reminiscent of those in higher vertebrates as well as some classical invertebrate glycan structures. 70% of these N-glycans were anionic, carrying either sialic acid, sulfate, or phosphate residues. In terms of glycophylogeny, our data position the brittle star between invertebrates and vertebrates and confirm the high diversity of N-glycosylation in lower organisms.
Highlights
Echinoderms are among the most primitive deuterostomes and have been used as model organisms to understand chordate biology because of their close evolutionary relationship to this phylogenetic group
There are almost no data available regarding the N-glycomic capacity of echinoderms, which are otherwise known to produce a diverse set of species-specific glycoconjugates, including ones heavily modified by fucose, sulfate, and sialic acid residues
We hypothesized that echinoderm species would display a mixture of invertebrate and vertebrate structural features; we found many N-glycans with antennal sialic acid or sulfate and others displaying difucosylation of the core
Summary
Our initial hypothesis regarding echinoderm N-glycosylation was that there would be a substantial degree of modification of oligosaccharides with anionic moieties as in vertebrates but that there may be vestiges of invertebrate-type N-glycomic features, such as difucosylation of the asparagine-bound chitobiosyl core. Despite similar fragmentation patterns and only slightly different 2D-HPLC elution properties, the two isomers with sialylated galactose were shown to differ in terms of which antenna carried the sialic acid residue by performing 1,3-specific galactosidase treatment followed by incubation with the arm-specific insect FDL hexosaminidase [25] (Fig. 8, Q–Z). Some glycans were predicted to contain both sulfate and sialic acid; in the case of two isomeric structures (Hex HexNAc4Fuc1NeuGc1S1) with different 2D-HPLC elution properties, fragments at either m/z 282 or 387 were observed and correlated with loss of either 307 or 387 Da upon sialidase S treatment This suggested that the sulfate residues were either on an antennal GlcNAc or covalently bound to the terminal sialic acid residue (Fig. 7, H–M).
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