Protein methylation coordinates epigenetic gene expression and drives cell development. For many human parasites, limited drug classes and resistance to frontline drugs mean new avenues for inhibiting parasite life-cycles are urgently required. Methyltransferase enzymes represent prime drug targets in Giardia— the most common human gastrointestinal parasite causing diarrheal disease in 200 million people worldwide. Giardia is a unique model for protein methylation; this deep-branching protist has a diverged lysine methylome (K-Me) and is the first eukaryote with no arginine methylome.
We acknowledge large-scale methyl-site identifications using LC-MS/MS are subject to high false discovery rates (FDR) in methylpeptide spectrum matches (methyl-PSMs)1. Ideally, ‘true’ methyl-sites are identified by orthogonal methyl-peptide identification through isotopic labelling of methylation sites via heavy-methyl SILAC. These are not feasible for non-model organisms and parasites which have limited in vitro cultures and/or undefined media. Therefore, we implemented new methyl-site confidence-filtering pipelines in Giardia. Filtering is implemented post-database searching with Maxquant2, complimented by avoiding methanol- and SDS-based sample preparation (which introduce methyl-artefacts1), and high-mass accuracy peptide fragmentation with higher-energy collisional dissociation (HCD). Filtering removes common sources of false positive methyl-PSMs, and retains sites with robust MS/MS evidence. We validated methyl-site filters with mouse controls, demonstrating filtering enriches known (‘true’) mouse methyl-sites.
These confidence filters identified over 200 K-Me sites in 160 proteins in Giardia. These Giardia K-Me proteins are mostly species- and lineage-specific with only 58/160 and 40/160 shared orthologs in H. sapiens and S. cerevisiae, respectively. Many K-Me proteins in Giardia specific gene-families were associated with cytoskeletal regulation. Significant enrichment for coiled-coil features demonstrated many K-Me sites specifically occurred within coiled-coil heptads in solvent-facing positions, with intriguing implication for regulation of this versatile protein folding motif.