Can heavy metal pollution induce soil bacterial community resistance to antibiotics in boreal forests?
The emergence of microbial antibiotic resistance is a central threat to global health, food security, and development. It has been shown that heavy metal pollution can give rise to microbial resistance to antibiotics, but how wide-spread this phenomenon is remains an open question that urgently needs filling to enable appropriate environmental risk assessments. Here, we determined whether long-term differences in heavy metal pollution in boreal forests had affected soil microbial communities such that they had increased microbial resistance to antibiotics. First, we assessed variation in metal concentrations in samples collected across a distance trajectory from the pollution source, and also the microbial rates and levels of bacterial community resistance to the heavy metal Cu and the antibiotics tetracycline and vancomycin in those samples. Second, we tested if the exposure to Cu or tetracycline could increase bacterial community resistance to Cu and to antibiotics in soils with high versus low background levels of metal contamination. Metal pollution had affected microbial community structures and suppressed decomposer functioning. Importantly, bacterial community Cu resistance increased with higher metal concentrations, which coincided with an induced bacterial community resistance to tetracycline, but not to vancomycin. Laboratory experiments revealed that bacterial community Cu resistance could be further induced in both the low and high end of the pollution gradient, but also that these short-term inductions of community metal tolerance did not coincide with enhanced antibiotic resistance. This yielded a surprising negative correlation between long-term and short-term effects by metals on microbial metal and antibiotic resistances. One mechanism that could provide protection against both metal cations and tetracycline is the small multidrug resistance (SMR) family, which is an energy demanding physiological mechanism that may take time to confer protection. This may explain the different microbial responses to long-term gradients and metal addition experiments. Policy implications. We show that metal pollution in boreal forests will promote soil bacterial antibiotic resistance, revealing a so far unrecognized reservoir of microbial antibiotic resistance. We recommend that environmental risk assessments for any activity giving rise to increased soil metal concentrations need to also consider the induction of microbial antibiotic resistance.