Abstract
The mechanisms by which Geobacter sulfurreducens transfers electrons through relatively thick (>50 µm) biofilms to electrodes acting as a sole electron acceptor were investigated. Biofilms of Geobacter sulfurreducens were grown either in flow-through systems with graphite anodes as the electron acceptor or on the same graphite surface, but with fumarate as the sole electron acceptor. Fumarate-grown biofilms were not immediately capable of significant current production, suggesting substantial physiological differences from current-producing biofilms. Microarray analysis revealed 13 genes in current-harvesting biofilms that had significantly higher transcript levels. The greatest increases were for pilA, the gene immediately downstream of pilA, and the genes for two outer c-type membrane cytochromes, OmcB and OmcZ. Down-regulated genes included the genes for the outer-membrane c-type cytochromes, OmcS and OmcT. Results of quantitative RT-PCR of gene transcript levels during biofilm growth were consistent with microarray results. OmcZ and the outer-surface c-type cytochrome, OmcE, were more abundant and OmcS was less abundant in current-harvesting cells. Strains in which pilA, the gene immediately downstream from pilA, omcB, omcS, omcE, or omcZ was deleted demonstrated that only deletion of pilA or omcZ severely inhibited current production and biofilm formation in current-harvesting mode. In contrast, these gene deletions had no impact on biofilm formation on graphite surfaces when fumarate served as the electron acceptor. These results suggest that biofilms grown harvesting current are specifically poised for electron transfer to electrodes and that, in addition to pili, OmcZ is a key component in electron transfer through differentiated G. sulfurreducens biofilms to electrodes.
Highlights
Previous attempts to improve the power output of microbial fuel cells have primarily focused on overcoming electrochemical limitations, but a better understanding of how microorganisms transfer electrons to electrodes could lead to the design of microorganisms with improved electron-transfer capabilities [1,2,3,4].A wide diversity of microorganisms are capable of electron transfer to electrodes [5,6]
Previous studies demonstrated that G. sulfurreducens produced a biofilm on graphite surfaces that served as an electron acceptor in microbial fuel cells [20]
In order to determine if a biofilm would grow on the same graphite surface with an alternative electron acceptor, cells were grown in the presence of the same graphite surface, but electrically disconnected from the cathode, preventing electron transfer to the graphite
Summary
Previous attempts to improve the power output of microbial fuel cells have primarily focused on overcoming electrochemical limitations, but a better understanding of how microorganisms transfer electrons to electrodes could lead to the design of microorganisms with improved electron-transfer capabilities [1,2,3,4].A wide diversity of microorganisms are capable of electron transfer to electrodes [5,6]. Previous attempts to improve the power output of microbial fuel cells have primarily focused on overcoming electrochemical limitations, but a better understanding of how microorganisms transfer electrons to electrodes could lead to the design of microorganisms with improved electron-transfer capabilities [1,2,3,4]. We have focused our studies on Geobacter sulfurreducens because this species, or closely related organisms, are frequently the most abundant microorganisms colonizing anodes harvesting current from aquatic sediments [7,8,9] and in laboratory fuel cells designed for high current densities under highly anoxic conditions [10,11,12,13]. Experimental manipulation [14], electrochemical analysis [15,16] and modeling studies [17] have all suggested that G. sulfurreducens transfers electrons to anodes via bound mediator(s) rather than soluble electron shuttles. Conductive pili, commonly referred to as microbial nanowires [19], were not required for this low-density current production [18]
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