Insight into the Role of Iron(III)-Reducing Microflora in the Arsenic Biogeochemistry of Earthworm (Pheretima guillemi) Guts

The guts of soil animals are hotspots for arsenic biotransformers and iron(III) reducers. However, the roles of gut iron(III)-reducing bacteria (IRB) in arsenic transformation in soil animals remain unclear. This study enriched gut IRB from soil earthworms (Pheretima guillelmi) over three generations (189 days) with glucose and lactate as electron donors to investigate their impacts on arsenic reduction, methylation, and demethylation. Intestinal IRB was dominated by Clostridium (42%) and Bacillaceae spp. (25%) in glucose treatments and by Veillonellales-Selenomonadales spp. (34%) and Thermincola (19%) in lactate treatments. As(V) reduction and DMAs(V) demethylation mediated by IRB were detected during incubation, which was more efficient in glucose treatments than in lactate setups. However, no arsenic methylation was identified in all treatments. The dominant IRB in the earthworm gut, including Clostridium, Bacillus, and Paenibacillus, harbored genes involved in As(V) respiration (arrA), As(V) reduction (arsC, arsR, GstB, mgsR, and spxA), and arsenic efflux (ACR3, arsA, arsB, arsD, etc.). Besides, Methanobacterium, Methanomassiliicoccus, and Methanosarcina were potential DMAs(V)-demethylating taxa. Overall, arsenic-transforming microbes comprised up to 100% of gut iron(III)-reducing microbial communities during incubation. Therefore, this research deepens our insights into the role of gut microbiota in soil-dwelling animals in iron–arsenic biogeochemical cycles.