Anaerobic oxidation of arsenite by autotrophic bacteria: The view from Mono Lake, California

Introduction

The phenomenon of arsenite [As(III)] oxidation by aerobic bacteria was first reported by Green (1918), and the many subsequent discoveries made in this realm, most occurring over the past three decades, are the primary focus of this book. In contrast, the fact that select anaerobes can also achieve this feat was an entirely serendipitous discovery. As often occurs in science, the intended path leading towards a stated goal can take an unexpected turn, ultimately leading to greater rewards than those originally anticipated. The intellectual freedom to meander such a path of curiosity-driven research is a great gift especially when one arrives at an unexpected revelation. It is perhaps the most rewarding aspect of a scientist's career. Such was the case when we first uncovered the phenomenon of anaerobic As(III) oxidation.

Our arsenic-related field work focused on Mono Lake, California because of its exceptionally high levels of dissolved inorganic arsenic (~200 μM), and the fact that we had previously isolated two novel species of arsenate [As(V)]-respiring bacteria, Bacillus arseniciselenatis and B. selenitireducens from its bottom sediments(Switzer Blum et al., 1998). Radiotracer investigations employing ⁷³As(V) measured high As(V) reductase activity in the anoxic water column of the lake, yielding an estimate that this electron sink could mineralize approximately 8-14% of annual phytoplankton productivity (Oremland et al., 2000), a value confirmed independently on the basis of mass balance considerations (Hollibaugh et al., 2005). In both studies both groups also used cultivation-based methods (Most-Probable-Numbers) to estimate the densities of As(V)-respiring bacteria in the anoxic water column, and arrived at similar low but detectable values (e.g. 10²-10³ ml^-1). The next goal was to determine what taxa of As(V)-respiring prokaryotes were involved in these water-column transformations, using culture-independent analyses (Denaturing Gradient Gel Electrophoresis) of As(V)-amended anoxic bottom water.

We had expected to find 16S rRNA gene amplicon sequences similar to those from the bacilli we isolated from the sediments, but instead found a few rather unremarkable amplicons in the Epsilon, Gamma and Delta proteobacteria; yet these incubations showed a complete reduction of the added As(V), caused by sulfide-linked oxidation by resident chemoautotrophs of the Delta-proteobacteria (Hoeft et al., 2004; Hollibaugh et al., 2006). This As(V) reductase activity was inhibited by nitrate, while addition of As(III) to nitrate-amended waters resulted in the formation of As(V). This observation led us to conclude that there was anaerobic biological oxidation of As(III) to As(V), linked to the provided nitrate ions (Hoeft et al., 2002).