Giant mimivirus R707 encodes a glycogenin paralogue polymerizing glucose through α- and β-glycosidic linkages

Abstract

Acanthamoeba polyphaga mimivirus is a giant virus encoding 1262 genes among which many were previously thought to be exclusive to cellular life. For example, mimivirus genes encode enzymes involved in the biosynthesis of nucleotide sugars and putative glycosyltransferases. We identified in mimivirus a glycogenin-1 homologous gene encoded by the open reading frame R707. The R707 protein was found to be active as a polymerizing glucosyltransferase enzyme. Like glycogenin-1, R707 activity was divalent-metal-ion-dependent and relied on an intact DXD motif. In contrast with glycogenin-1, R707 was, however, not self-glucosylating. Interestingly, the product of R707 catalysis featured α1-6, β1-6 and α1-4 glycosidic linkages. Mimivirus R707 is the first reported glycosyltransferase able to catalyse the formation of both α and β linkages. Mimivirus-encoded glycans play a role in the infection of host amoebae. Co-infection of Acanthamoeba with mimivirus and amylose and chitin hydrolysate reduced the number of infected amoebae, thus supporting the importance of polysaccharide chains in the uptake of mimivirus by amoebae. The identification of a glycosyltransferase capable of forming α and β linkages underlines the peculiarity of mimivirus and enforces the concept of a host-independent glycosylation machinery in mimivirus.

A Persistent Giant Algal Virus, with a Unique Morphology, Encodes an Unprecedented Number of Genes Involved in Energy Metabolism

“…Among these eight predicted ORFs, four contained an additional non-overlapping GT domain (two GT2s, one GT6, and one GT60). Functional analyses of GTs in mimiviruses (or in related Paramecium bursaria Chlorella viruses) have demonstrated that some of these enzymes are functional, being able to modify viral collagen-like proteins (74) and polymerize sugars (75). Conservation between PkV RF01 GTs and functionally characterized GTs in viruses and cells is absent or extremely low, which precludes any predictions as to the specific roles of these enzymes in the PkV RF01 life cycle.…”

A persistent giant algal virus, with a unique morphology, encodes an unprecedented number of genes involved in energy metabolism

“…Among these eight predicted ORFs, four contained an additional non-overlapping GT domain (two GT2s, one GT6, and one GT60). Functional analyses of GTs in mimiviruses (or in related Paramecium bursaria Chlorella viruses) have demonstrated that some of these enzymes are functional, being able to modify viral collagen-like proteins (Luther et al, 2011) and polymerize sugars (Rommel et al, 2016).…”

“…We found that PkV RF01 encodes key β-oxidation enzymes. sugars (75). Conservation between PkV RF01 GTs and functionally characterized GTs in viruses and cells is absent or extremely low, which precludes any predictions as to the specific roles of these enzymes in the PkV RF01 life cycle.…”

Chemistry and Enzymology of Disulfide Cross-Linking in Proteins

“…As an adaptation to their site of replication, the viruses encode their own versions of enzymes that are compartmentalized in cells. For example, mimivirus encodes a set of enzymes involved in glycan formation, − allowing for the biosynthesis of surface glycoproteins independently of the host secretory pathway. In addition, as noted above (section ), large dsDNA viruses encode sulfhydryl oxidases.…”