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.