The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens

Abstract

<i>Geobacter sulfurreducens</i> mediates extracellular electron transfer (EET) reactions with different substrates, such as solid-phase Fe(III)-containing minerals, anodes and the cells of <i>Geobacter metallireducens</i>. To compare their roles in EET, the <i>pilA-N, omcE</i>, <i>omcS</i>, <i>omcT</i> and <i>omcZ</i> genes of <i>G. sulfurreducens</i> were systematically deleted. All mutants showed impaired and varied ability to form biofilms on nonconductive surface. Deletion of <i>omcE</i> also impaired bacterial ability to reduce ferrihydrite, but its impacts on the ability for anode reduction and the co-culture of <i>G. metallireducens</i>-<i>G. sulfurreducens</i> were minimal. The mutant without <i>omcS</i> showed diminished ability to reduce ferrihydrite and to form the co-culture, but was able to regain its ability to reduce anodes. Deletion of <i>omcT</i>, <i>omcZ</i> or <i>pilA-N</i> alone impaired bacterial ability to reduce ferrihydrite and anodes and to form the co-culture. Deletion of all tested genes abolished bacterial ability to reduce ferrihydrite and anodes. Triple-deletion of all <i>omcS, omcT</i> and <i>omcZ</i> abolished the ability of <i>G. sulfurreducens</i> to co-culture with <i>G. metallireducens</i>. However, deletion of only <i>omcZ</i> or <i>pilA-N</i> or both <i>omcS</i> and <i>omcT</i> abolished the ability of <i>G. sulfurreducens</i> without hydrogenase gene <i>hybL</i> to co-culture with <i>G. metallireducens</i>, which show their indispensable roles in direct electron transfer from <i>G. metallireducens</i> to <i>G. sulfurreducens</i>. Thus, the roles of <i>pilA-N, omcE</i>, <i>omcS</i>, <i>omcT</i> and <i>omcZ</i> for <i>G. sulfurreducens</i> in EET vary substantially, which also suggest that possession of PilA-N and multiple cytochromes of different structures enables <i>G. sulfurreducens</i> to mediate EET reactions efficiently with substrates of different properties.