Glycomics, Glycoproteomics, and Glycogenomics: An Inter-Taxa Evolutionary Perspective

Abstract

Glycosylation is a highly diverse set of co- and posttranslational modifications of proteins. For mammalian glycoproteins, glycosylation is often site-, tissue-, and species-specific and diversified by microheterogeneity. Multitudinous biochemical, cellular, physiological, and organismic effects of their glycans have been revealed, either intrinsic to the carrier proteins or mediated by endogenous reader proteins with carbohydrate recognition domains. Furthermore, glycans frequently form the first line of access by or defense from foreign invaders, and new roles for nucleocytoplasmic glycosylation are blossoming. We now know enough to conclude that the same general principles apply in invertebrate animals and unicellular eukaryotes-different branches of which spawned the plants or fungi and animals. The two major driving forces for exploring the glycomes of invertebrates and protists are (i) to understand the biochemical basis of glycan-driven biology in these organisms, especially of pathogens, and (ii) to uncover the evolutionary relationships between glycans, their biosynthetic enzyme genes, and biological functions for new glycobiological insights. With an emphasis on emerging areas of protist glycobiology, here we offer an overview of glycan diversity and evolution, to promote future access to this treasure trove of glycobiological processes.

Keywords: Evolution; glycome; glycosyltransferase; invertebrate; protist.

Graphical abstract

Fig. 1

Evolutionary map of eukaryotic glycans based on the core sugar–amino acid linkage type. Glycan protein linkages, based on direct evidence or inferred from glycogenomics (see text), are layered on a cladogram from a current model for the phylogeny of eukaryotes (3), which emphasizes the protist subkingdoms and their proposed relation to the last eukaryotic common ancestor (LECA). Major groups where glycomic or bioinformatics information is available are named, with species names in italics. Human or plant pathogens are in red. Linkages found in any one species qualifies for assignment in the group. The dashed line represents likely lateral gene transfer. Poorly studied protists for which there is a lack of experimental data are not shown. Organisms that branched from the lineage that gave rise to the higher plants are referred to as Group 1, whereas those that gave rise to animals are classified as Group 2. Linkages are inferred to occur in the LECA if they are found in both groups of protists, but the absence of a linkage might be a result of incomplete information. The origin of linkages inferred to originate after the LECA is shown at the relevant branch point. Notes adjacent to linkages indicate names by which they are commonly referred. GPI anchors, a specialized glycolipid linked to protein C termini typically via a phosphoethanolamine linker to a nonreducing terminal mannose, was likely present in the LECA (not shown). SNFG symbols for sugars are summarized at the bottom. See text for explanations.

Fig. 2

Peripheral linkages described in protist, fungal and invertebrate glycans. Examples of peripheral saccharides and their nonsaccharide modifications of protist, fungal, and invertebrate glycans are summarized, together with organisms where found and relevant references (9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25). A, N-glycans. B, O-glycans. See Figure 1 for the symbol key and the text for explanations. Empty symbols indicate undetermined sugar isomer. N indicates linkage to Asn and R/R′/R′′ the remainder of a glycan structure.