Double-edged sword of FeS oxidation in estuarine and coastal sediments: accelerating elemental cycling yet enhancing antibiotic resistance enrichment.

Abstract

Biogeochemical cycles exert significant influences on the fate and behavior of antibiotics in estuarine and coastal environments; however, ferrous sulfide (FeS)-mediated enrichment and dissemination of antibiotic resistance genes (ARGs) remain poorly understood. Here, we conducted microcosm experiments and field investigations to examine the relationships of FeS amendment, microbial communities, functional potentials in relation to elemental cycling, and ARG abundance. The positive effects of FeS on ARG abundance were aerobic dependent, which were accompanied by a significant enrichment of Proteobacteria, as the crucial hosts of ARGs. Proteobacteria were associated with systematic metabolic pathways for carbon fixation (Calvin-Benson-Bassham [CBB] cycle), N₂ fixation, and FeS oxidation. In addition, field samples from China estuarine and coastal wetlands further showed that CBB cycle, N₂ fixation, and sulfur oxidation pathways were significantly correlated with the relative abundance of ARGs. These findings collectively indicate that FeS oxidation facilitates enrichment and dissemination of ARGs through selective enrichment of Proteobacteria and consequent enhancement of metabolic synergies between sulfur, iron, carbon, and nitrogen cycles. However, FeS-mediated oxidation may also degrade microbial DNA and suppress ARG proliferation, indicating that the net outcome of ARG enrichment depends on oxygen conditions and microbial community filtering. The cascade processes of environmental regulation-community restructuring-metabolic synergy are of great significance to enhance ARG enrichment and dissemination. Therefore, redox fluctuations can enhance elemental cycling and further promote significant enrichment and dissemination of ARGs. These findings highlight the importance of redox dynamics in ARG monitoring and risk assessment in estuarine and coastal wetlands.IMPORTANCEEstuarine and coastal wetlands are important ecosystems for antibiotic resistance gene (ARG) enrichments. This study investigated FeS oxidation-mediated biogeochemical cycling and ARG dissemination. FeS oxidation increased enrichment and dissemination of the ARGs in estuarine and coastal sediments. The FeS oxidation reshaped microbial community structure and selectively enriched the critical Proteobacteria, which played the crucial hosts of the ARGs. The enrichment and dissemination of ARGs in the presence of FeS oxidation were due mainly to the enhanced metabolic coupling of sulfur oxidation, nitrogen fixation, and carbon fixation. CBB cycle, N₂ fixation, and sulfur oxidation pathways were also significantly correlated with ARG abundance along the latitudinal gradient. Therefore, enhanced elemental metabolic pathways under FeS oxidation exacerbated enrichment and dissemination of ARGs, highlighting the coupling mechanisms of biogeochemical cycle and ARGs in estuarine and coastal wetlands.