Abstract
The tandem gene clusters orfR-ombB-omaB-omcB and orfS-ombC-omaC-omcC of the metal-reducing bacterium Geobacter sulfurreducens PCA are responsible for trans-outer membrane electron transfer during extracellular reduction of Fe(III)-citrate and ferrihydrite [a poorly crystalline Fe(III) oxide]. Each gene cluster encodes a putative transcriptional factor (OrfR/OrfS), a porin-like outer-membrane protein (OmbB/OmbC), a periplasmic c-type cytochrome (c-Cyt, OmaB/OmaC) and an outer-membrane c-Cyt (OmcB/OmcC). The individual roles of OmbB, OmaB and OmcB in extracellular reduction of Fe(III), however, have remained either uninvestigated or controversial. Here, we showed that replacements of ombB, omaB, omcB, and ombB-omaB with an antibiotic gene in the presence of ombC-omaC-omcC had no impact on reduction of Fe(III)-citrate by G. sulfurreducens PCA. Disruption of ombB, omaB, omcB, and ombB-omaB in the absence of ombC-omaC-omcC, however, severely impaired the bacterial ability to reduce Fe(III)-citrate as well as ferrihydrite. These results unequivocally demonstrate an overlapping role of ombB-omaB-omcB and ombC-omaC-omcC in extracellular Fe(III) reduction by G. sulfurreducens PCA. Involvement of both ombB-omaB-omcB and ombC-omaC-omcC in extracellular Fe(III) reduction reflects the importance of these trans-outer membrane protein complexes in the physiology of this bacterium. Moreover, the kinetics of Fe(III)-citrate and ferrihydrite reduction by these mutants in the absence of ombC-omaC-omcC were nearly identical, which suggests that absence of any protein subunit eliminates function of OmaB/OmbB/OmcB protein complex. Finally, orfS was found to have a negative impact on the extracellular reduction of Fe(III)-citrate and ferrihydrite in G. sulfurreducens PCA probably by serving as a transcriptional repressor.
Highlights
Geobacter sp. play critical roles in global cycling of carbon, iron (Fe), manganese (Mn), and other elements
Geobacter sulfurreducens PCA employ the porin-cytochrome (Pcc) trans-outer membrane protein complexes for electron conductance across the outer membrane (Liu et al, 2014; Shi et al, 2014)
This model is similar to that proposed for MtrABC trans-outer membrane protein complex of the metal-reducing bacterium Shewanella oneidensis MR-1(Hartshorne et al, 2009; Richardson et al, 2012; White et al, 2013; Liu et al, 2014)
Summary
Geobacter sp. play critical roles in global cycling of carbon, iron (Fe), manganese (Mn), and other elements. Play critical roles in global cycling of carbon, iron (Fe), manganese (Mn), and other elements They can oxidize organic matter intracellularly and transfer the released electrons to the terminal electron acceptors, such as Fe(III) and Mn(IV) oxides that are external to the bacterial cells. It is proposed that OmbB or OmbC serves as a scaffold through which OmaB or OmaC and OmcB or OmcC are inserted to form a heme-based electron conduit of sufficient length to span the entire width of outer membrane This model is similar to that proposed for MtrABC trans-outer membrane protein complex of the metal-reducing bacterium Shewanella oneidensis MR-1(Hartshorne et al, 2009; Richardson et al, 2012; White et al, 2013; Liu et al, 2014). It should be pointed out that the Pcc proteins and Mtr proteins are phylogenetically unrelated and they appear to have evolved independently to the similar functions (Liu et al, 2014; Shi et al, 2014)
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