Arsenic mobilization by Bathyarchaeia in subsurface sediments at the Jianghan Plain, China

As one of the most abundant microorganisms on Earth, Bathyarchaeia with diverse abilities to degrade complex organic carbon play a vital role in the global carbon cycle. However, the role of Bathyarchaeia in arsenic (As) metabolism and their contribution to As mobilization in aquifers remain unclear. In this study, we recovered 15 Bathyarchaeota metagenome-assembled genomes (MAGs) from metagenomes of borehole sediments in the Jianghan Plain (JHP), China. Together with 374 representative Bathyarchaeia MAGs from public databases, six As metabolism genes i.e. arrA, arsR, arsA, arsB, arsC (Trx) and arsM were identified, accounting for 4.4, 47.6, 20.3, 38.3, 37.5 and 49.4 % of total Bathyarchaeia MAGs, respectively. Heterologous expression of multiple arsC and arsM genes of Bathyarchaeia MAGs obtained from JHP sediments validated their abilities for As(V) reduction and As(III) methylation at environmentally relevant As concentration. These results indicate that in addition to providing bioavailable carbon sources for other microbial functional populations, Bathyarchaeia directly participate in As mobilization in the JHP aquifer via As(V) reduction and As(III) methylation. The diversified distribution of arsC and arsM in the class Bathyarchaeia suggests that Bathyarchaeia may contribute to As cycling in other As-rich environments, such as hot spring, saline lakes, marine hydrothermal sediments and soils.