Abstract
BACKGROUND: Chryseobacterium spp. are environmentally widespread bacteria increasingly recognized as opportunistic pathogens in human and veterinary medicine, yet genome-scale determinants that may support persistence in host-associated microenvironments remain poorly defined. Isolates from anatomically specialized sites such as the ocular surface are underrepresented in comparative genomic datasets. METHODS: We performed integrated phenotypic and genome-resolved characterization of Chryseobacterium sp. NG-CE01, isolated from a bovine corneal infection. A high-quality hybrid assembly was analyzed using phylogenomics, curated comparative gene-content profiling across a 14-genome Chryseobacterium panel, CAZyme annotation, synteny-guided locus interrogation, mobilome profiling, and systematic screening of antimicrobial resistance, virulence, and genome-defense determinants, supported by functional curation of isolate-specific genes. RESULTS: Genome-based taxonomy placed NG-CE01 as a genomically distinct lineage most closely related to Chryseobacterium cheonjiense, falling below established species delineation thresholds and thus consistent with a putative novel genomospecies within the genus. Comparative gene-content profiling across the multi-species panel yielded an open interspecies repertoire (Heaps’ law α = 0.6897), with NG-CE01 contributing a focused isolate-specific set enriched in defense- and recombination-associated functions. Across analyses, the dominant axis of differentiation was synteny-guided, locus-scale remodeling of discrete carbohydrate-foraging modules (CBM48–GH13, CBM6–GH5, and a GH43-rich super-block), supported by conserved neighborhood architecture, Jaccard similarity gradients, and locus-centric enrichment patterns. Three genomic islands were identified; GI_3 represented the principal reservoir of isolate-specific functional novelty, enriched in envelope biogenesis and regulatory functions and consistent with a restrained mobilome. Comprehensive screening detected no acquired antimicrobial-resistance or virulence genes; instead, NG-CE01 encoded chromosomal intrinsic resistance and fitness-associated loci, while disk-diffusion results are reported as zone diameters given limited validated breakpoints for Chryseobacterium. Collectively, these results support a hypothesis that ocular-associated persistence may be shaped primarily by genome architecture and synteny-defined locus innovation rather than CAZyme burden or virulence acquisition. CONCLUSION: NG-CE01 exhibits pronounced synteny-defined remodeling of carbohydrate-foraging and intrinsic resistance loci, providing a genome-informed, hypothesis-generating framework for how Chryseobacterium may persist in specialized host environments and illustrating the value of synteny-aware comparative genomics for resolving functional remodeling beyond gene abundance alone. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-026-04950-8.