What drives metal resistance genes in urban park soils? Park age matters across biomes

Although resistance genes are a global concern in ecosystems, the underlying factors responsible for their worldwide dissemination, especially in urban greenspaces, are poorly known. To investigate metal and metal resistance genes (MRGs) accumulation in urban parks, we used ICP-MS to analyze metal concentrations and GeoChip functional gene arrays to analyze MRGs abundances in vegetation types with labile and recalcitrant litter across urban parks and non-urban reference sites in three distinct climatic regions: Boreal (Finland), Temperate (Baltimore, USA), and Tropical (Singapore). Our results indicate that metal concentrations and MRGs abundances in park soils increase with park age across climatic zones, especially so for the dominant metals - Fe and Al - accounting for more than 90% of the total metal content, and others, e.g., Mn, Zn, and Pb. Correspondingly, Fe and Al resistance genes were the most abundant MRGs, representing 23% of all detected MRGs. Vegetation type affected metals and MRGs only in the boreal region, not in temperate or tropical regions, suggesting that vegetation context is not generalizable across climatic zones. Our analyses also indicate that the distribution of resistance genes is only weakly affected by soil properties, but largely associated with accumulation of metals from traffic and industrial sources. Our data further indicate that MRGs and antibiotic resistance genes (ARGs) are co-selected by metal accumulation. The pattern of MRG abundance between old and young parks is similar to that of ARGs, indicating a potential risk for human health in old urban parks. Our findings emphasize the importance of park age and the corresponding cumulative effects of anthropogenic activities as a driver of metal and MRG dynamics in urban soils globally.