Influence of epiphytic bacteria on arsenic metabolism in Hydrilla verticillata

Microbial assemblages such as biofilms around aquatic plants play a major role in arsenic (As) cycling, which has often been overlooked in previous studies. In this study, arsenite (As(III))-oxidizing, arsenate (As(V))-reducing and As(III)-methylating bacteria were found to coexist in the phyllosphere of Hydrilla verticillata, and their relative activities were shown to determine As speciation, accumulation and efflux. When exposed to As(III), As(III) oxidation was not observed in treatment H(III)-B, whereas treatment H(III)+B showed a significant As(III) oxidation ability, thereby indicating that epiphytic bacteria displayed a substantial As(III) oxidation ability. When exposed to As(V), the medium only contained 5.89% As(III) after 48 h of treatment H(V)-B, while an As(III) content of 86.72% was observed after treatment H(V)+B, thereby indicating that the elevated As(III) in the medium probably originated from As(V) reduction by epiphytic bacteria. Our data also indicated that oxidizing bacteria decreased the As accumulation (by approximately 64.44% compared with that of treatment H(III)-B) in plants, while reducing bacteria played a critical role in increasing As accumulation (by approximately 3.31-fold compared with that of treatment H(V)-B) in plants. Regardless of whether As(III) or As(V) was supplied, As(III) was dominant in the plant tissue (over 75%). Furthermore, the presence of epiphytic bacteria enhanced As efflux by approximately 9-fold. Metagenomic analysis revealed highly diverse As metabolism genes in epiphytic bacterial community, particularly those related to energetic metabolism (aioAB), and As resistance (arsABCR, acr3, arsM). Phylogenetic analysis of As metabolism genes revealed evidence of both vertical inheritance and horizontal gene transfer, which might have contributed to the evolution of the As metabolism genes. Taken together, our research suggested that the diversity of As metabolism genes in epiphytic bacterial community is associated with aquatic submerged macrophytes which may play an important role in As biogeochemistry in aquatic environments.