Abstract
Frequent and persistent heavy metal pollution has profound effects on the composition and activity of microbial communities. Heavy metals select for metal resistance but can also co-select for resistance to antibiotics, which is a global health concern. We here document metal concentration, metal resistance and antibiotic resistance along a sediment archive from a pond in the North West of the United Kingdom covering over a century of anthropogenic pollution. We specifically focus on zinc, as it is a ubiquitous and toxic metal contaminant known to co-select for antibiotic resistance, to assess the impact of temporal variation in heavy metal pollution on microbial community diversity and to quantify the selection effects of differential heavy metal exposure on antibiotic resistance. Zinc concentration and bioavailability was found to vary over the core, likely reflecting increased industrialisation around the middle of the 20th century. Zinc concentration had a significant effect on bacterial community composition, as revealed by a positive correlation between the level of zinc tolerance in culturable bacteria and zinc concentration. The proportion of zinc resistant isolates was also positively correlated with resistance to three clinically relevant antibiotics (oxacillin, cefotaxime and trimethoprim). The abundance of the class 1 integron-integrase gene, intI1, marker for anthropogenic pollutants correlated with the prevalence of zinc- and cefotaxime resistance but not with oxacillin and trimethoprim resistance. Our microbial palaeontology approach reveals that metal-contaminated sediments from depths that pre-date the use of antibiotics were enriched in antibiotic resistant bacteria, demonstrating the pervasive effects of metal-antibiotic co-selection in the environment.
Highlights
The global emergence of antimicrobial resistance (AMR) is of acute concern: a 2014 review on tackling this crisis estimated the number of deaths that may occur globally due to AMR in the 35 years could be as high as 300 million individuals and that the economic damage could amount to 60–100 trillion US dollars (O'neill, 2014)
When a genetic change mediates resistance to both metals and antibiotics, or when metal resistance- and antibiotic resistance genes are genetically linked on mobile genetic elements (MGEs), metals can co-select for resistance to clinically relevant antibiotics (Baker-Austin et al, 2006; Peltier et al, 2010; Seiler and Berendonk, 2012)
A sediment core was extracted from Griffin Wood Pond (GWP), located in the highly industrialised urban landscape of Merseyside in the North West of England which has been a major site of chemical manufacturing for over a century
Summary
The global emergence of antimicrobial resistance (AMR) is of acute concern: a 2014 review on tackling this crisis estimated the number of deaths that may occur globally due to AMR in the 35 years could be as high as 300 million individuals and that the economic damage could amount to 60–100 trillion US dollars (O'neill, 2014). Pollution with heavy metals has the potential to result in the spread of AMR (Baker-Austin et al, 2006). Bacteria are generally highly sensitive to metal pollution but can evolve a variety of resistance mechanisms, mediated by chromosomal mutations or by the uptake of resistance genes on mobile genetic elements (MGEs) When a genetic change mediates resistance to both metals and antibiotics (cross-resistance), or when metal resistance- and antibiotic resistance genes are genetically linked on MGEs (co-resistance), metals can co-select for resistance to clinically relevant antibiotics (Baker-Austin et al, 2006; Peltier et al, 2010; Seiler and Berendonk, 2012)
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