Arsenic Accumulation in Microbial Biomass and the Interpretation of Signals of Early Arsenic‐Based Metabolisms

Abstract

Carbonaceous particles that concentrate arsenic in microbialites as old as ~3.5 Ga are similar to As-rich organic globules in mod-ern microbialites. The former particles have been interpreted as tracers of As cycling by early microbial metabolisms. However,it is unclear if arsenic accumulation is a consequence of biological activity or passive postmortem binding of arsenic by organicmatter during diagenesis in volcanically influenced, As-rich environments. Here, we address this uncertainty by evaluating theconcentrations, speciation, and detectability of As in active or heat-killed biofilms formed by cyanobacteria or anoxygenic pho-tosynthetic microbes exposed to environmentally relevant concentrations of As(III) or As(V) (50 μM to 3 mM). The genomes ormetagenomes of these biofilms contain genes involved in detoxifying or energy-yielding As metabolisms. Biomass accumulatesAs from the solution in a concentration-dependent manner and with a preference for oxidized As(V) over As(III). Autoclaved bio-mass accumulates As even more strongly than active biomass, likely because living biofilms actively detoxify As. Active biofilmsoxidize and reduce As and accumulate both As(III) and As(V), whereas a small fraction of As(V) can be reduced in inactive bio-films that bind As during diagenesis. Arsenic enrichments in the biomass are detectable by X-ray based spectroscopy techniques(XRF, EPMA-WDS) that are commonly used to analyze geological materials. These findings enable the reconstruction of pastactive and passive interactions of microbial biomass with arsenic in fossilized microbial biofilms and microbialites from the earlyEarth.