A multi-omics study links human disturbance to antibiotic resistance gene changes in food-plant phyllosphere and wildlife gut microbiomes

Abstract

Human disturbance can alter antibiotic resistance gene (ARG) profiles in environmental and host-associated microbiomes, but the role of food-plant phyllosphere communities in linking these changes remains unclear. We integrated phyllosphere metagenomes from 18 food-plant samples with previously generated gut metagenomes and faecal metabolomes from 30 faecal samples collected from two wild Sichuan snub-nosed monkey (Rhinopithecus roxellana) populations inhabiting contrasting human-disturbance contexts. The human-disturbed phyllosphere contained more ARG-carrying contigs, including 24,582 habitat-specific contigs compared with 9,308 in the control habitat, and five Rank I ARG subtypes detected only in the disturbed habitat, whereas the abundance of shared Rank I ARGs did not differ significantly. An abundance-weighted genomic compatibility index integrating sequence homology and local collinearity was higher between phyllosphere ARG-associated regions and gut metagenome-assembled genomes in the human-disturbance group, particularly for Acidobacteria, Actinobacteria, and Firmicutes. Functional annotation of genomic regions flanking collinear ARGs showed differences in replication and repair, translation, signal transduction, membrane transport, and cofactor and vitamin metabolism. Faecal metabolomics showed lower 2-oxoglutarate, isocitrate, and D-sedoheptulose 7-phosphate and higher 6-phosphogluconic acid and NADH in the human-disturbance group, consistent with variation in the gut luminal carbon metabolic environment. These coordinated patterns may partly reflect disturbance-associated microbial community restructuring and species sorting. Collectively, our findings suggest that the food-plant phyllosphere may represent an ecological interface linking environmental ARG variation with wildlife gut microbiomes and provide a basis for ARG monitoring and microbial risk assessment under the One Health framework.