Biochar facilitates ferrihydrite reduction by Shewanella oneidensis MR-1 through stimulating the secretion of extracellular polymeric substances

Abstract

Biochar can mediate extracellular electron transfer (EET) of Shewanella oneidensis MR-1 and subsequently facilitate dissimilatory reduction of iron(III) minerals. Previous studies mainly focused on the interaction of biochar and membrane cytochrome complexes to reveal the mediating mechanisms between biochar and S. oneidensis MR-1. However, the influence of biochar on the production and activity of extracellular polymeric substances (EPS) has long been neglected, despite the fact that EPS are commonly exudated by S. oneidensis MR-1 and can participate in a variety of electron transfer processes due to their redox activity. Here, we performed a series of microbial ferrihydrite reduction experiments in combination with electrochemical voltametric and impedance analyses to investigate the role of biochar in the formation and transformation of cell EPS during EET. Results showed that the added biochar not only functioned as an electron shuttle facilitating electron transfer, but also induced the secretion of five times more EPS by S. oneidensis MR-1, leading to a 1.4-fold faster ferrihydrite reduction in comparison with biochar-free setups. We further extracted the secreted EPS and found that the proportion of redox-active exoproteins was significantly (p < 0.05) increased in the EPS and resulted in a higher electron exchange capacity in secreted EPS. Such increased exoprotein content also induced a higher ratio of exoprotein to exopolysaccharide, which largely dropped diffusion and electron transfer impedance of EPS to 1.1 and 18 Ω, respectively, and accelerated the EET and thus the ferrihydrite reduction. Overall, our findings revealed the interactions between biochar and EPS matrices, which could potentially play a critical role in EET processes in both environmental or biotechnological systems.