Cytochrome‐mediated direct electron uptake from metallic iron by Methanosarcina acetivorans

Abstract

Impact statement Methane‐producing microorganisms accelerate the corrosion of iron‐containing metals. Previous studies have inferred that some methanogens might directly accept electrons from Fe(0), but when this possibility was more intensively investigated, H2 was shown to be an intermediary electron carrier between Fe(0) and methanogens. Here, we report that Methanosarcina acetivorans catalyzes direct metal‐to‐microbe electron transfer to support methane production. Deletion of the gene for the multiheme, outer‐surface c‐type cytochrome MmcA eliminated methane production from Fe(0), consistent with the key role of MmcA in other forms of extracellular electron exchange. These findings, coupled with the previous demonstration that outer‐surface c‐type cytochromes are also electrical contacts for electron uptake from Fe(0) by Geobacter and Shewanella species, suggest that the presence of multiheme c‐type cytochromes on corrosion surfaces might be diagnostic for direct metal‐to‐microbe electron transfer and that interfering with cytochrome function might be a strategy to mitigate corrosion.

H2is a Major Intermediate inDesulfovibrio vulgarisCorrosion of Iron

“…Unlike pure Fe 0 , H 2 production from stainless steel is minimal (16). However, microbes capable of direct electron uptake from Fe 0 can extract electrons from stainless steel to support anaerobic respiration (16, 17, 19). D. vulgaris did not reduce sulfate with stainless steel as the electron donor (Figure 3C).…”

“…Furthermore, D. vulgaris lacks outer-surface cytochromes (20) and no other D. vulgaris outer surface electrical contacts are known. Unlike the microbes previously shown to directly accept electrons from Fe 0 (15–19), D. vulgaris does not directly reduce Fe(III) (21), a capability common to most electroactive microbes (22).…”

“…This distinction is important because pure Fe 0 abiotically generates H2 via reaction #1 (15,25), but stainless steel does not (16). In contrast to D. ferrophilus, stainless steel was an effective electron donor for Geobacter and Methanosarcina strains capable of direct electron uptake from Fe 0 (16,19,24). Notably, protease digestion of D. ferrophilus extracellular proteins did not affect sulfate reduction rates with Fe 0 as the electron donor (26), a result inconsistent with a microbe making direct electrical contact with Fe 0 .…”

“…Direct Fe 0 -to-microbe electron transfer for D. vulgaris has also been proposed (14). Studies with Geobacter (15, 16), Shewanella (17, 18), and Methanosarcina (19) species have provided evidence for direct electron uptake from Fe 0 by: 1) eliminating the possibility that H 2 was serving as an electron shuttle between Fe 0 and cells; and 2) demonstrating with gene deletions that outer-surface c -type cytochromes were required for electron uptake from Fe 0 . In contrast, no studies have previously reported on D. vulgaris corrosion with strains that were unable to use H 2 (7).…”

“…A rigorous strategy to evaluate the possibility of H 2 serving as an intermediary electron carrier is to determine whether strains unable to use H 2 can respire with Fe 0 as the sole electron donor (15, 16, 18, 19, 27). In instances in which the wild-type strain of interest can consume H 2 , this can be accomplished by deleting genes necessary for H 2 uptake (15, 18, 27).…”