Unlike plants and invertebrates, vertebrates reportedly lack proteins displaying truncated N-linked glycosylation (paucimannosylation) with the monosaccharide composition mannose_1-3fucose_0-1N-acetylglucosamine₂. Enabled by technology advancements in system-wide glycopeptide characterization (glycoproteomics), we document as the first that protein paucimannosylation is a significant host-derived molecularsignature in neutrophil-rich sputum from pathogen-infected human lungs and is negligible in pathogen-free sputum. Six paucimannose N-glycans were carried by inflammation-associated proteins of human neutrophil origin including myeloperoxidase, azurocidin and neutrophil elastase that localized specifically to azurophilic granules. Paucimannose in vitro synthesis by human azurophil-specific β-hexosaminidase A, together with promyelocyte stage-specific expression of paucimannosylated proteins and their biosynthetic enzymes, indicated a novel spatio-temporal biosynthetic route in early neutrophil maturation. Exogeneous generation of paucimannose was excluded by absence of bacterial exoglycosidase activity or paucimannosidic glycans. P. aeruginosa induced virulence-dependent secretion of paucimannosidic proteins from isolated and sputum neutrophils. Interestingly, paucimannosidic proteins displayed virulence-specific bacteriostatic effects towards P. aeruginosa and showed affinities to mannan-binding lectin suggesting multiple immune-related functions of paucimannosylation in activated neutrophils.