Sunlight-triggered synergy of hematite and Shewanella oneidensis MR-1 in Cr(VI) removal

Abstract

Hematite is usually considered as a terminal electron acceptor for dissimilatory metal-reducing bacteria (DMRB), such as Shewanella oneidensis MR-1. However, hematite is also a semiconductor with visible light response. How the photocatalytic activity of hematite affects its electrical interplay with DMRB, as well as its role in relevant biogeochemical processes under sunlight, is still unclear. In this study, we investigated the effect of hematite on Cr(VI) removal by S. oneidensis MR-1 in the dark versus under stimulated sunlight using both batch experiments and photoelectrochemical analysis in a solar-assisted microbial photoelectrochemical system with a hematite photoanode covered by S. oneidensis MR-1. Under the dark conditions, hematite at low mineral-to-cell ratios can promote Cr(VI) removal through adsorbing both Cr(VI) and bacteria on/near hematite surface, which facilitates Cr(VI) bio-reduction and also alleviates self-poisoning processes of cells with time. However, as mineral-to-cell ratios reach a high level, hematite particles may cover cell surface and impact Cr(VI) bio-reduction, leading to the decreased Cr(VI) removal with increasing hematite particles. Under simulated sunlight, S. oneidensis MR-1 generates electrons from lactate metabolism and utilizes them to fill photoexcited holes in hematite, generating photoexcited electrons to reduce Cr(VI). Thus, in addition to directly enzymatic reduction of Cr(VI), the new light-triggered electron transfer pathway: lactate → S. oneidensis MR-1 → hematite → Cr(VI) further increases Cr(VI) removal and lactate metabolism. Also, the time-dependent cell survival is increased by the presence of hematite under the simulated sunlight, probably owing to the promoted Cr(VI) reduction and accumulation of Cr(III)-products on hematite surface. Moreover, organic hole scavenger, such as Ethylenediaminetetraacetic acid (EDTA), can further enhance Cr(VI) removal by hematite and S. oneidensis MR-1 under light irradiation. The photoelectrochemical results confirm that the light-triggered electron transfer pathway can be promptly and repeatedly produced upon illumination, and the rapid decrease of photocurrents after spiking Cr(VI) indicates Cr(VI) reduction by the photogenerated electrons from hematite. These findings suggest that semiconducting minerals, like hematite, can harvest solar energy to boost microbial metabolism and contaminant transformation by non-phototrophic, electroactive bacteria, which in turn increases bacterial tolerance toward toxic compounds in surrounding environments.