Deciphering environmental resistome and mobilome risks on the stone monument: A reservoir of antimicrobial resistance genes

Antimicrobial resistance (AMR) in the environment has attracted increasing attention as an emerging global threat to public health. Stone is an essential ecosystem in nature and also an important material for human society, having architectural and aesthetic values. However, little is known about the AMR in stone ecosystems, particularly in the stone monument, where antimicrobials are often applied against biodeterioration. Here, we provide the first detailed metagenomic study of AMR genes across different types of biodeteriorated stone monuments, which revealed abundant and diverse AMR genes conferring resistance to drugs (antibiotics), biocides, and metals. Totally, 132 AMR subtypes belonging to 27 AMR types were detected including copper-, rifampin-, and aminocoumarins-resistance genes, of which diversity was mainly explained by the spatial turnover (replacement of genes between samples) rather than nestedness (loss of nested genes between samples). Source track analysis confirms that stone resistomes are likely driven by anthropogenic activities across stone heritage areas. We also detected various mobile genetic elements (namely mobilome, e.g., prophages, plasmids, and insertion sequences) that could accelerate replication and horizontal transfer of AMR genes. Host-tracking analysis further identified multiple biodeterioration-related bacterial genera such as Pseudonocardia , Sphingmonas , and Streptomyces as the major hosts of resistome. Taken together, these findings highlight that stone microbiota is one of the natural reservoirs of antimicrobial-resistant hazards, and the diverse resistome and mobilome carried by active biodeteriogens may improve their adaptation on stone and even deactivate the antimicrobials applied against biodeterioration. This enhanced knowledge may also provide novel and specific avenues for environmental management and stone heritage protection.

Automated summary

Stone microbiota is a natural reservoir of antimicrobial-resistant hazards, containing abundant and diverse resistance genes. The diversity of these genes is mainly driven by gene replacement between stone monuments, rather than gene loss. Antimicrobial resistance genes are likely spread by anthropogenic activities in stone heritage areas. Additionally, various mobile genetic elements that can accelerate the replication and horizontal transfer of resistance genes have been detected.