Geogenic high arsenic elevates the groundwater antibiotic resistomes: A blind spot of resistance in Anthropocene

Abstract

Metals/metalloids, being ubiquitous in the environment, can function as a co-selective pressure on antibiotic resistance genes (ARGs) threatening human health. However, the effect of geogenic arsenic (As) on groundwater antibiotic resistomes and their health risks remain largely unknown. Here, we systematically analyzed bacterial communities, pathogenic bacteria, antibiotic resistomes, and in-situ multidrug-resistant isolates with the assessment of the health risk of ARGs and the pathogenicity of their hosts in high As groundwater from the Hetao basin, Northwestern China. We found that long-term geogenic As exposure shifted the assembly of resistomes and resulted in a high abundance and diversity of ARGs in groundwater. Significantly positive associations among As, As cycling genes, ARGs, and mobile genetic elements (MGEs) revealed by network and pathway analyses, together with genetic evidence of As-tolerant multidrug-resistant isolates by whole genomic sequencing, robustly indicate the geogenic As-induced co-selection for antibiotic resistance in groundwater. Variance partitioning analysis further confirmed the determinative role of geogenic As in groundwater resistomes, with As species and As cycling genes as the core abiotic and biotic drivers, respectively. More seriously, geogenic As accelerated the prevalence of high-risk ARGs and multidrug-resistant bacteria. Our findings highlight the significance of geogenic As-induced co-selection for antibiotic resistance in groundwater and the hidden role of geogenic metals/metalloids in increasing antibiotic resistance. This study provides a basis for groundwater management of both high As and ARGs for human health.