Evidence for Long-Term Anthropogenic Pollution: The Hadal Trench as a Depository and Indicator for Dissemination of Antibiotic Resistance Genes

Knowledge of the distribution and dissemination of antibiotic resistance genes (ARGs) is essential for understanding anthropogenic impacts on natural ecosystems. The transportation of ARGs via aquatic environments is significant and has received great attention, but whether there has been anthropogenic ARG pollution to the hadal ocean ecosystem has not been well explored. For investigating ecological health concerns, we profiled the ARG occurrence in sediments of the Mariana Trench (MT) (10 890 m), the deepest region of the ocean. Metagenomic-based ARG profiles showed a sudden increase of abundance and diversity in the surface layer of MT sediments reaching 2.73 × 10^–2 copy/cell and 81 subtypes, and a high percentage of ∼63.6% anthropogenic pollution sources was predicted by the Bayesian-modeling classification method. These together suggested that ARG accumulation and anthropogenic impacts have already permeated into the bottom of the deepest corner on the earth. Moreover, six ARG-carrying draft genomes were retrieved using a metagenomic binning strategy, one of which assigned as Streptococcus was identified as a potential bacterial host to contribute to the ARG accumulation in MT, carrying ermF, tetM, tetQ, cfxA2, PBP-2X, and PBP-1A. We propose that the MT ecosystem needs further long-term monitoring for the assessment of human impacts, and our identified three biomarkers (cfxA2, ermF, and mefA) could be used for the rapid monitoring of anthropogenic pollution. Together our findings imply that anthropogenic pollution has penetrated into the deepest region of the ocean and urge for better pollution control to reduce the risk of ARG dissemination to prevent the consistent accumulation and potential threat to the natural environment.