Abstract
Microbial metabolism plays a key role in controlling the fate of toxic groundwater contaminants, such as arsenic. Dissimilatory metal reduction catalyzed by subsurface bacteria can facilitate the mobilization of arsenic via the reductive dissolution of As(V)-bearing Fe(III) mineral assemblages. The mobility of liberated As(V) can then be amplified via reduction to the more soluble As(III) by As(V)-respiring bacteria. This investigation focused on the reductive dissolution of As(V) sorbed onto Fe(III)-(oxyhydr)oxide by model Fe(III)- and As(V)-reducing bacteria, to elucidate the mechanisms underpinning these processes at the single-cell scale. Axenic cultures of Shewanella sp. ANA-3 wild-type (WT) cells [able to respire both Fe(III) and As(V)] were grown using 13C-labeled lactate on an arsenical Fe(III)-(oxyhydr)oxide thin film, and after colonization, the distribution of Fe and As in the solid phase was assessed using nanoscale secondary ion mass spectrometry (NanoSIMS), complemented with aqueous geochemistry analyses. Parallel experiments were conducted using an arrA mutant, able to respire Fe(III) but not As(V). NanoSIMS imaging showed that most metabolically active cells were not in direct contact with the Fe(III) mineral. Flavins were released by both strains, suggesting that these cell-secreted electron shuttles mediated extracellular Fe(III)-(oxyhydr)oxide reduction, but did not facilitate extracellular As(V) reduction, demonstrated by the presence of flavins yet lack of As(III) in the supernatants of the arrA deletion mutant strain. 3D reconstructions of NanoSIMS depth-profiled single cells revealed that As and Fe were associated with the cell surface in the WT cells, whereas for the arrA mutant, only Fe was associated with the biomass. These data were consistent with Shewanella sp. ANA-3 respiring As(V) in a multistep process; first, the reductive dissolution of the Fe(III) mineral released As(V), and once in solution, As(V) was respired by the cells to As(III). As well as highlighting Fe(III) reduction as the primary release mechanism for arsenic, our data also identified unexpected cellular As(III) retention mechanisms that require further investigation.
Highlights
In environments where oxygen is absent or depleted, bacteria and archaea are able to use a wide range of alternative terminal electron acceptors to conserve energy (Weber et al, 2006)
The Fetotal solubilized at day 11 (29 μM by the WT and 22 μM by the ARRA3) was measured by ICP-AES (Figure 1A), and the values were comparable to the total Fe(II) levels measured by ferrozine
In earlier exploratory work (Supplementary Figure 2B), Fetotal was only mobilized in incubations with cells and electron donor, and its concentration increased with incubation time
Summary
In environments where oxygen is absent or depleted, bacteria and archaea are able to use a wide range of alternative terminal electron acceptors to conserve energy (Weber et al, 2006). Ferrous iron [Fe(II)] predominates, whereas in oxygen-rich environments, ferric iron [Fe(III)] is the predominant species and forms Fe(III) minerals at circumneutral pH As these Fe(III) minerals are usually poorly soluble, this poses the challenge of transferring electrons to the cell surface via an extracellular electron transport system when respiring Fe(III) (Nevin and Lovley, 2002; Lovley et al, 2004; Reguera et al, 2005; Weber et al, 2006). As(III) is regarded as the more soluble and mobile of these oxyanions and is considered to be more toxic than As(V) (Cullen and Reimer, 1989; Shen et al, 2013) Anions, such as phosphate, promote As(V) desorption by competing for sorption sites in the subsurface, for instance, on Fe(III)-(oxyhydr)oxide minerals (Biswas et al, 2014). The occurrence of As(V) in the solid phase usually correlates with the presence of amorphous Fe(III)
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