Bacteriophages from Arsenic-Resistant Bacteria Transduced Resistance Genes, which Changed Arsenic Speciation and Increased Soil Toxicity

Lysogenic phages are known to serve as transfer vectors for bacterial genes involved in biotransformation of various environmental pollutants. However, their role in arsenic-contaminated environments is largely undocumented. Here, lysogenic phages were chemically induced (with mitomycin C) in soil samples from two contaminated sites, and arsenic resistance genes arsC (coding for As(V) reduction to excretable (via efflux pumps) but more toxic As(III)) and arsM (coding for As(III) methylation) were detected in these phage genomes. The relative abundance of these genes (per phage particle) was positively correlated with that in the corresponding indigenous soil bacterial communities (resistance gene per 16S rRNA), with R2 = 0.974 for arsC and 0.761 for arsM. Microcosm studies with 100 mg/kg of arsenic soil showed that phages (amended at 5.0 × 107 phages per gram soil) enhanced the propagation of arsC by 122-fold and arsM by 575-fold, relative to unamended soil. This increased the As(III) concentration by 4.3 mg/kg (214%) after 15 days but also enabled arsenic methylation (to 0.8 mg/kg). Earthworm avoidance tests corroborated the increase in soil arsenic ecotoxicity after phage addition. Overall, this study demonstrates that arsenic resistance genes transduction by lysogenic phages can result in an overlooked but important phenomenon: a change in arsenic speciation and a significant increase in soil ecotoxicity.