Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal Areas

Abstract

Environmental contamination by heavy metals (HMs) poses several indirect risks to human health, including the co-spreading of genetic traits conferring resistance to both HMs and antibiotics among micro-organisms. Microbial antibiotic resistance (AR) acquisition is enhanced at sites anthropogenically polluted by HMs, as well as in remote systems naturally enriched in HMs, such as hydrothermal vents in the deep sea. However, to date, the possible role of hydrothermal vents at shallower water depths as hot spots of microbial AR gain and spreading has not been tested, despite the higher potential risks associated with the closer vicinity of such ecosystems to coasts and human activities. In this work, we collected waters and sediments at the Panarea shallow-water hydrothermal vents, testing the presence of culturable marine bacteria and their sensitivity to antibiotics and HMs. All of the bacterial isolates showed resistance to at least one antibiotic and one HM and, most notably, 80% of them displayed multi-AR on average to 12 (min 8, max 15) different antibiotics, as well as multi-HM tolerance. We show that our isolates displayed high similarity (≥99%) to common marine bacteria, affiliating with Actinobacteria, Gammaproteobacteria, Alphaproteobacteria and Firmicutes, and all displayed wide growth ranges for temperature and salinity during in vitro physiological tests. Notably, the analysis of the genomes available in public databases for their closest relatives highlighted the lack of genes for AR, posing new questions on the origin of multi-AR acquisition in this peculiar HM-rich environment. Overall, our results point out that shallow-water hydrothermal vents may contribute to enhance AR acquisition and spreading among common marine bacteria in coastal areas, highlighting this as a focus for future research.