Oil-contaminated sites act as high-risk pathogen reservoirs previously overlooked in coastal zones

Abstract

In addition to the organic pollutants and disturbance to the microbial, plant and animal systems, oil contamination can also enrich opportunistic pathogens. But little is known about whether and how the most common coastal oil-contaminated water bodies act as reservoirs for pathogens. Here, we delved into the characteristics of pathogenic bacteria in coastal zones by constructing seawater-based microcosms with diesel oil as a pollutant. 16S rRNA gene full-length sequencing and genomic exploration revealed that pathogenic bacteria with genes involved in alkane or aromatic degradation were significantly enriched under oil contamination, providing a genetic basis for them to thrive in oil-contaminated seawater. Moreover, high-throughput qPCR assays showed an increased abundance of the virulence gene and enrichment in antibiotics resistance genes (ARGs), especially those related to multidrug resistance efflux pumps, and their high relevance to Pseudomonas, enabling this genus to achieve high levels of pathogenicity and environmental adaptation. More importantly, infection experiments with a culturable P. aeruginosa strain isolated from an oil-contaminated microcosm provided clear evidence that the environmental strain was pathogenic to grass carp (Ctenopharyngodon idellus), and the highest lethality rate was found in the oil pollutant treatment, demonstrating the synergistic effect of toxic oil pollutants and pathogens on infected fish. A global genomic investigation then revealed that diverse environmental pathogenic bacteria with oil degradation potential are widely distributed in marine environments, especially in coastal zones, suggesting extensive pathogenic reservoir risks in oil-contaminated sites. Overall, the study uncovered a hidden microbial risk, showing that oil-contaminated seawater could be a high-risk pathogen reservoir, and provides new insights and potential targets for environmental risk assessment and control.