Wildlife as sentinels for spread of antibiotic resistance in the environment

Most research on emerging antibiotic resistant (AR) bacteria has focused on clinical settings. However, antibiotics and resistance genes originated in environmental bacteria long before the antibiotic era. On the one hand, the... [ view full abstract ]

Most research on emerging antibiotic resistant (AR) bacteria has focused on clinical settings. However, antibiotics and resistance genes originated in environmental bacteria long before the antibiotic era. On the one hand, the enormous microbial diversity in the environment is a source of AR. On the other hand, human activities release AR bacteria and antibiotics into the environment. Mixing of these two resistance reservoirs can lead to the transfer and selection of AR among both environmental and human-associated bacteria. Wildlife may facilitate exchange of AR bacteria and genes between human-made and natural reservoirs. We hypothesized that gulls may play an important role in facilitating this exchange because they are frequently found near human-modified habitats. To explore this hypothesis, we assessed the prevalence of AR bacteria and the diversity of AR genes present in samples of gull feces collected from coastal Maine and New Hampshire, USA. We found widespread resistance to a variety of clinically-relevant antibiotics in Gram negative bacteria cultured from gull fecal samples. In gull colonies, transmission of AR bacteria was more likely in high density nesting areas compared to low density ones. Using functional metagenomics, we discovered that gulls carry an extensive diversity of resistance genes including genes in 9 different class A beta-lactamase categories and 32 unknown genes, which were associated with a wide variety of bacteria. Analysis of sequence diversity in the most common AR gene revealed 100% similarity to an AR gene found in a clinically-derived E. coli isolate. This study more than doubled the number of clinically relevant AR gene types known to be carried by gulls or by wildlife in general. Together with the propensity of gulls to visit human-dominated habitats, this high diversity of AR gene types suggests that gulls can facilitate the spread of AR.