Global analysis of the metaplasmidome: ecological drivers and spread of antibiotic resistance genes across ecosystems

Plasmids act as vehicles for the rapid spread of antibiotic resistance genes (ARGs). However, few studies of the resistome at the community level distinguish between ARGs carried by mobile genetic elements and those carried by chromosomes, and these studies have been limited to a few ecosystems. This is the first study to focus on ARGs carried by the metaplasmidome on a global scale. This study shows that only a small fraction of the plasmids reconstructed from 27 ecosystems representing 9 biomes are catalogued in public databases. The abundance of ARGs harboured by the metaplasmidome was significantly explained by bacterial richness. Few plasmids with or without ARGs were shared between ecosystems or biomes, suggesting that plasmid distribution on a global scale is mainly driven by ecology rather than geography. The network linking plasmids to their hosts shows that these mobile elements have thus been shared between bacteria across geographically distant environmental niches. However, certain plasmids carrying ARGs involved in human health were identified as being shared between multiple ecosystems and hosted by a wide variety of hosts. Some of these mobile elements, identified as keystone plasmids, were characterised by an enrichment in antibiotic resistance genes (ARGs) and CAS-CRISPR components which may explain their ecological success. The ARGs accounted for 9.2% of the recent horizontal transfers between bacteria and plasmids. By comprehensively analysing the plasmidome content of ecosystems, some key habitats have emerged as particularly important for monitoring the spread of ARGs in relation to human health. Of particular note is the potential for air to act as a vector for long-distance transport of ARGs and accessory genes across ecosystems and continents.