N‐glycosylation in Archaea—New roles for an ancient posttranslational modification

Abstract

Genome analysis points to N‐glycosylation as being an almost universal posttranslational modification in Archaea. Although such predictions have been confirmed in only a limited number of species, such studies are making it increasingly clear that the N‐linked glycans which decorate archaeal glycoproteins present diversity in terms of both glycan composition and architecture far beyond what is seen in the other two domains of life. In addition to continuing to decipher pathways of N‐glycosylation, recent efforts have revealed how Archaea exploit this variability in novel roles. As well as encouraging glycoprotein synthesis, folding and assembly into properly functioning higher ordered complexes, N‐glycosylation also provides Archaea with a strategy to cope with changing environments. Archaea can, moreover, exploit the apparent species‐specific nature of N‐glycosylation for selectivity in mating, and hence, to maintain species boundaries, and in other events where cell‐selective interactions are required. At the same time, addressing components of N‐glycosylation pathways across archaeal phylogeny offers support for the concept of an archaeal origin for eukaryotes. In this MicroReview, these and other recent discoveries related to N‐glycosylation in Archaea are considered.

Novel Proteome and N-Glycoproteome of the Thermophilic Fungus Chaetomium thermophilum in Response to High Temperature

“…Glycosylation, the attachment of glycans to proteins, is a posttranslational modification to produce significant structural changes to proteins ( Ge et al, 2018 ). Protein glycosylation is common in all kinds of life (bacteria, archaea, and eukaryotes), demonstrating multiple cell functions, such as protein folding, signal transduction, stability, targeting, cell–cell interactions, and host immune response ( Mitra et al, 2006 ; Vigerust and Shepherd, 2007 ; Calo et al, 2010 ; Nothaft and Szymanski, 2010 ; Eichler, 2020 ). Glycosylation is considered the most complicated posttranslational modification due to the multiple enzymatic steps ( Eichler, 2020 ).…”

“…Protein glycosylation is common in all kinds of life (bacteria, archaea, and eukaryotes), demonstrating multiple cell functions, such as protein folding, signal transduction, stability, targeting, cell–cell interactions, and host immune response ( Mitra et al, 2006 ; Vigerust and Shepherd, 2007 ; Calo et al, 2010 ; Nothaft and Szymanski, 2010 ; Eichler, 2020 ). Glycosylation is considered the most complicated posttranslational modification due to the multiple enzymatic steps ( Eichler, 2020 ). Glycans are encoded in a complex dynamic network containing hundreds of genes, which form the enzymes for glycan synthesis.…”

“…Molecular events, such as transferring sugars from one substrate to another, linking monosaccharides, and trimming sugars from glycan structures, are involved in glycosylation. Glycosylation is non-templated, and cells employ a host of enzymes to add or remove sugars from one molecule to another to generate glycoproteins in a given cell ( Eichler, 2020 ). Importantly, glycosylation enhances the proteome’s diversity, as almost any aspect of glycosylation is modifiable, such as glycosidic linkage and glycan composition, structure, and length ( Zacchi and Schulz, 2016 ).…”

Structural basis for the strict exclusion of proline from the N-glycosylation sequon

“…N-Glycosylation is essential in Eukarya and the modern phyla of Archaea 7 . In contrast, in the ancient archaeal phylum Euryarchaeota, the N-glycosylation is dispensable for growth in laboratory conditions but presumably requisite for survival in harsh environments 8 . N-Glycosylation also occurs in the eubacterial genera Campylobacter 3 and Helicobacter 9 , in which the N-glycosylation is non-essential for growth but important for virulence by promoting the adhesion of these human enteropathogenic bacteria to host cells 10 .…”

“…Most eukaryotes use a well-conserved canonical 14-residue oligosaccharide structure, Glc3Man9GlcNAc2, and lower eukaryotes use a shorter version of the 14-residue structure, lacking the terminal glucose and/or mannose residues 29 . In contrast, Archaea and Eubacteria use completely different sets of oligosaccharide structures from species to species, with respect to the number, composition, and branching pattern of the monosaccharides 8 . Considering the substantial divergence of the oligosaccharide donor structures, comparisons between distantly related OST enzymes can capture the essence of substrate recognition and enzyme catalysis.…”