Desulfovibrio vulgaris has been a primary pure culture sulfate reducer for developing microbial corrosion concepts. Multiple mechanisms for how it accepts electrons from Fe0 have been proposed. We investigated Fe0 oxidation with a mutant of D. vulgaris in which hydrogenase genes were deleted. The hydrogenase mutant grew as well as the parental strain with lactate as the electron donor, but unlike the parental strain, it was not able to grow on H2. The parental strain reduced sulfate with Fe0 as the sole electron donor, but the hydrogenase mutant did not. H2 accumulated over time in Fe0 cultures of the hydrogenase mutant and sterile controls but not in parental strain cultures. Sulfide stimulated H2 production in uninoculated controls apparently by both reacting with Fe0 to generate H2 and facilitating electron transfer from Fe0 to H+. Parental strain supernatants did not accelerate H2 production from Fe0, ruling out a role for extracellular hydrogenases. Previously proposed electron transfer between Fe0 and D. vulgaris via soluble electron shuttles was not evident. The hydrogenase mutant did not reduce sulfate in the presence of Fe0 and either riboflavin or anthraquinone-2,6-disulfonate, and these potential electron shuttles did not stimulate parental strain sulfate reduction with Fe0 as the electron donor. The results demonstrate that D. vulgaris primarily accepts electrons from Fe0 via H2 as an intermediary electron carrier. These findings clarify the interpretation of previous D. vulgaris corrosion studies and suggest that H2-mediated electron transfer is an important mechanism for iron corrosion under sulfate-reducing conditions.
IMPORTANCE Microbial corrosion of iron in the presence of sulfate-reducing microorganisms is economically significant. There is substantial debate over how microbes accelerate iron corrosion. Tools for genetic manipulation have only been developed for a few Fe(III)-reducing and methanogenic microorganisms known to corrode iron and in each case those microbes were found to accept electrons from Fe0 via direct electron transfer. However, iron corrosion is often most intense in the presence of sulfate-reducing microbes. The finding that Desulfovibrio vulgaris relies on H2 to shuttle electrons between Fe0 and cells revives the concept, developed in some of the earliest studies on microbial corrosion, that sulfate reducers consumption of H2 is a major microbial corrosion mechanism. The results further emphasize that direct Fe0-to-microbe electron transfer has yet to be rigorously demonstrated in sulfate-reducing microbes.
Microbial corrosion of iron-containing metals is a substantial economic problem, but the mechanisms are poorly understood (1–3). Fundamentally, iron corrosion is the oxidation of metallic iron to ferrous iron:
This reaction must be coupled with an electron accepting reaction to proceed. Thus, microorganisms can stimulate iron corrosion by either accelerating reaction 1 or by contributing to one or more reactions that consume the electrons from reaction 1.
Sulfate reducers are often implicated in iron corrosion (1, 4–6). Desulfovibrio spp. have been the most studied pure culture isolates for investigating iron corrosion under sulfate-reducing conditions, dating back to the some of the earliest studies on microbial corrosion (1, 3, 7). Three mechanisms for Desulfovibrio species to consume electrons derived from Fe0 oxidation have been proposed (Fig. 1A). The first mechanism proposed (8) was abiotic oxidation of Fe0 coupled to proton reduction to generate H2:
combined with consumption of the H2 via sulfate reduction:
Several mechanisms that might enhance H2 production have been proposed (Fig. 1B). Hydrogenases released from moribund cells may accelerate reaction 1 by catalyzing H2 production from Fe0 (9). H2S generated from sulfate reduction may promote H2 production from Fe0 in two ways. Sulfide can react with Fe0 to generate H2 (1):
and iron sulfide precipitates might facilitate electron transfer from the Fe0 to H+, accelerating reaction 2 (2, 10).
One of the most intriguing proposed mechanisms for Desulfovibrio species to participate in iron corrosion is direct microbial electron uptake from Fe0 (1, 11–14). D. ferrophilus (previously known as strain IS5) can grow with H2 as the sole electron donor, but it was inferred to directly consume electrons from Fe0 based on the observation that it reduced sulfate faster than several other H2-oxidizing sulfate reducers (11). However, this inference relies on the unsubstantiated assumption that direct electron transfer is faster than H2-mediated electron transfer from Fe0 to microbes. Furthermore, possible adaptions in D. ferrophilus for enhanced growth on H2 derived from Fe0—such as producing an extracellular hydrogenase to accelerate Fe0 oxidation, a higher affinity for H2, or possibly a better capacity for attachment to Fe0—were not considered (3).
In subsequent studies, D. ferrophilus grew with pure Fe0 as the electron donor, but not with stainless steel (15). This distinction is important because pure Fe0 abiotically generates H2 via reaction 1 (16, 17), but stainless steel does not (18). In contrast to D. ferrophilus, stainless steel is an effective electron donor for Geobacter and Methanosarcina strains capable of direct electron uptake from Fe0 (15, 18, 19). Notably, protease digestion of D. ferrophilus extracellular proteins did not affect sulfate reduction rates with Fe0 as the electron donor (20), a result inconsistent with a microbe making direct electrical contact with Fe0 because protease degrades outer-surface electrical contacts (21). Therefore, the evidence available to date suggests that D. ferrophilus most likely accepts electrons from Fe0 via an H2 intermediate (15).
D. vulgaris is the most intensively studied sulfate reducer for biochemical and physiological investigations, and has served as a model sulfate reducer for many corrosion studies (7). Direct Fe0-to-microbe electron transfer has also been proposed for D. vulgaris (13, 14, 22), but as with the D. ferrophilus studies, the possibility of H2-mediated metal-to-microbe electron transfer was not rigorously eliminated. Studies with Geobacter (17, 18), Shewanella (23, 24), and Methanosarcina (19) species have provided evidence for direct electron uptake from Fe0 by (i) eliminating the possibility that H2 was serving as an electron shuttle between Fe0 and cells and (ii) demonstrating with gene deletions that outer-surface c-type cytochromes were required for electron uptake from Fe0. In contrast, no studies have previously been reported on D. vulgaris corrosion with strains that were unable to use H2 (7). D. vulgaris lacks outer-surface cytochromes (25), and no other D. vulgaris outer surface electrical contacts are known. Unlike the microbes previously shown to directly accept electrons from Fe0 (17–19, 23, 24), D. vulgaris does not directly reduce Fe(III) (26), an ability common to most microbes that can directly exchange electrons with extracellular electron donors and acceptors (27).
Higher rates of corrosion following the addition of riboflavin (14, 28, 29) led to the suggestion that riboflavin can function as an electron shuttle that Fe0 reduces:
with D. vulgaris oxidizing the reduced riboflavin with the reduction of sulfate:
However, those studies did not determine whether Fe0 could donate electrons to riboflavin or whether reduced riboflavin can serve as an electron donor for sulfate reduction. The alternative possibility that riboflavin might stimulate other aspects of microbial metabolism was also not evaluated. Furthermore, electron transfer via H2 was still possible in those studies.
A rigorous strategy to evaluate the possibility of H2 serving as an intermediary electron carrier is to determine whether strains unable to use H2 as an electron donor can respire with Fe0 as the sole electron donor (17–19, 23, 30). In instances in which the wild-type strain of interest can consume H2, this can be accomplished by deleting genes necessary for H2 metabolism (17, 23, 30). A strain of D. vulgaris in which genes for all of the annotated hydrogenases on the genome were deleted is available as one of a large collection of mutant strains (31). We report here on studies on Fe0-dependent sulfate reduction conducted with this hydrogenase-deficient strain.
RESULTS AND DISCUSSION
Hydrogenase mutant unable to grow with H2 as electron donor.
The hydrogenase-deficient mutant grew as well as the parental strain in medium with lactate as the electron donor and sulfate as the electron acceptor (Fig. 2A), but unlike the parental strain, the hydrogenase mutant did not grow in medium with H2 as the sole electron donor (Fig. 2B). These results suggested that the hydrogenase mutant was a suitable strain to evaluate the role of H2 as an intermediary electron carrier during growth with Fe0 as the electron donor.
Hydrogenase mutant cannot reduce sulfate with Fe0 as electron donor.
The parental strain reduced sulfate with Fe0 as the sole electron donor, but the hydrogenase mutant did not (Fig. 3A). The slight decline in sulfate over time in cultures with the hydrogenase mutant could be attributed to carry over of lactate with the inoculum because the final sulfate levels for the hydrogenase mutant with Fe0 were the same as for the parental strain without Fe0 (Fig. 3A). As expected from previous studies under similar conditions (17), H2 accumulated in sterile controls (Fig. 3B), reflecting abiotic Fe0 oxidation coupled to H+ reduction. H2 also accumulated in cultures inoculated with the hydrogenase mutant, further demonstrating the inability of this strain to consume H2. H2 accumulated more in the hydrogenase mutant cultures than in the uninoculated control, probably due to the sulfide that was transferred along with the inoculum (see sulfide effect on H2 production below). In contrast, the parental strain maintained low H2 concentrations (Fig. 3B), as expected for a microbe that can consume H2 produced from Fe0 (17). These results indicated that H2 produced from Fe0 was an important electron donor for sulfate reduction by the parental strain.
However, the quantity of H2 that accumulated in abiotic Fe0-only controls or in the presence of Fe0 and the hydrogenase mutant was not sufficient to account for the amount of sulfate that the parental strain reduced with Fe0 as the electron donor. For example, on day 14 the parental strain had reduced 3.4 mM sulfate (50% of the time zero concentration of 6.8 mM), which would require 13.6 mM H2 (4:1 stoichiometry of H2 oxidized per sulfate reduced, reaction 2). Only about half that much H2 accumulated in the hydrogenase mutant cultures (Fig. 3B). One possibility for this disparity is that because rapid H2 uptake by the parental strain maintained low H2 concentrations (Fig. 3B), H2 production from Fe0 (reaction 1) was more thermodynamically favorable, possibly accelerating H2 generation over that in the hydrogenase mutant cultures in which H2 accumulated. We could not devise an experimental approach to abiotically mimic the expected rapid removal of H2 at the Fe0 surface. However, the alternative possibility that sulfide produced during the growth of the parental strain on Fe0 accelerated H2 production could be evaluated.
Sulfide stimulates H2 production from Fe0.
Sulfide that the parental strain generated from sulfate reduction with Fe0 as the electron donor is also likely to have promoted H2 production (Fig. 4). Parental strain sulfide production was evident from the intense black precipitates indicative of iron sulfides on the Fe0 (Fig. 4A). In contrast, there was only a small amount of iron sulfide on the Fe0 of the hydrogenase mutant cultures, which could be attributed to sulfide transferred along with the inoculum (Fig. 4A). Sulfide was added to sterile medium, generating black iron sulfide precipitates (Fig. 4B), to assess the possible sulfide impact on H2 production. Adding sulfide stimulated H2 generation (Fig. 4C). One potential source of more H2 was the reaction of sulfide with Fe0 (reaction 3) in which there is a 1:1 stoichiometry for sulfide reacted and H2 produced. However, within 300 h the addition of 1.25 mM sulfide produced 2.7 mmol/L H2 (Fig. 4C), more than twice that expected from reaction 3. This result suggested that, as previously proposed (2, 10), iron sulfide precipitates also facilitated electron transfer from Fe0 to H+ (reaction 1), leading to additional H2 formation. The addition of 10-fold more sulfide only increased H2 an additional ~2-fold (Fig. 4C), further demonstrating a lack of defined stoichiometry between sulfide additions and H2 formation.
Hydrogenases released from some microbes can accelerate H+ reduction with Fe0 (30, 32, 33), and hydrogenase activity has been detected in supernatants of moribund D. vulgaris cultures (9). However, supernatants from D. vulgaris cultures grown either with H2 or Fe0 did not stimulate H2 production from Fe0 over that in abiotic controls (see Fig. S1).
Stainless-steel studies confirm importance of H2 as intermediary electron carrier.
The inability of the hydrogenase mutant to reduce sulfate with Fe0 as the electron donor contrasts with electroactive microbes such as Geobacter sulfurreducens (17) or Shewanella oneidensis (23), which continue to utilize Fe0 as an electron donor even after gene deletions have eliminated the capability for H2 uptake. Both G. sulfurreducens and S. oneidensis are capable of direct electron uptake as evidenced from an inhibition of Fe0-based respiration when genes for key outer-surface c-type cytochromes are deleted (17, 23, 24). Thus, the lack of sulfate reduction by the D. vulgaris hydrogenase mutant when Fe0 was the electron donor suggests that it is incapable of direct electron uptake from Fe0.
This conclusion was further supported with the results of studies in which stainless steel was provided as the electron donor. Unlike pure Fe0, H2 production from stainless steel is minimal (18). However, microbes capable of direct electron uptake from Fe0 can extract electrons from stainless steel to support anaerobic respiration (18, 19, 24). D. vulgaris did not reduce sulfate with stainless steel as the electron donor (Fig. 3C).
Electron shuttles do not promote Fe0-dependent sulfate reduction.
An alternative proposed electron transfer mechanism in Fe0 corrosion is that flavins shuttle electrons between Fe0 and D. vulgaris (Fig. 1A). An observed increase in Fe0 corrosion when riboflavin is added to D. vulgaris cultures has been offered as evidence for flavin shuttling (14, 28, 29). However, the riboflavin amendments were to complex medium in which lactate was provided as an electron donor in addition to Fe0. It was not demonstrated that the riboflavin additions increased rates of Fe0-dependent sulfate reduction. In order to examine the possibility of electron shuttles facilitating electron transfer between Fe0 and D. vulgaris, studies were conducted under defined conditions with Fe0 as the sole electron donor for sulfate reduction and either riboflavin or the known electron shuttle anthraquinone-2,6-disulfonate (AQDS) (34, 35). Riboflavin or AQDS did not accelerate Fe0-dependent sulfate reduction in the parental strain and did not enable the hydrogenase mutant to reduce sulfate with Fe0 as the electron donor (Fig. 3D). The midpoint potentials of AQDS (−184 mV) and riboflavin (−208 mV) are probably too positive for the reduced form of these molecules to support the reduction of sulfate to sulfide (midpoint potential, −217 mV). Therefore, the enhanced D. vulgaris Fe0 corrosion with riboflavin amendments (14, 28, 29) is likely to represent an impact of riboflavin on some aspect of growth or metabolism other than enhancement of electron transfer from Fe0 via an electron shuttle.
D. vulgaris attaches to Fe0 electron donor.
The turbidity of D. vulgaris growing on Fe0 was very low compared to the turbidity in H2-grown cultures when a comparable amount of sulfate had been reduced (Fig. 5A). A portion of the cells in the D. vulgaris parental strain culture have a mutation that can, in the short-term (~100 h), delay attachment to glass surfaces (36), but confocal scanning laser microscopy revealed that cells colonized Fe0 (Fig. 5B and C). Individual cells were distributed across the Fe0 surface, without apparent cell stacking, in a manner similar to the surface growth of Geobacter (17), Shewanella (23), and Methanosarcina species (19) with Fe0 serving as the sole electron donor. The attachment of cells should be advantageous because it enables H2 uptake at the point of production where localized H2 concentrations are higher than in the bulk surrounding environment. Furthermore, localized conditions at the cell/Fe0 interface are likely to accelerate Fe0 oxidation (Fig. 5D). For example, attached D. vulgaris oxidizing H2 can make Fe0 oxidation more thermodynamically favorable, both by removing a product of the reaction (H2) and resupplying a reactant (H+) near the Fe0 surface. Sulfide produced at the Fe0 surface can further accelerate H2 production.
A common practice in Fe0 corrosion studies has been to infer that corrosion rates faster than that observed from abiotic H2 generation are indicative of corrosion mechanisms other than H2 serving as an intermediary electron carrier between Fe0 and cells (3). However, the possibilities for attached H2-consuming cells to accelerate H2 production from Fe0 illustrate the limitations to that reasoning.
Understanding how D. vulgaris promotes Fe0 oxidation is important because it is the microbe that has been used to develop much of the existing mechanistic framework to describe how sulfate reducers corrode Fe0 (7). The results demonstrate that the primary mechanism for D. vulgaris to reduce sulfate with Fe0 as an electron donor is with H2 serving as an electron shuttle between Fe0 and the cells. Sulfate was not reduced in the absence of genes required for H2 uptake, even when previously proposed organic electron shuttles were added. All the microbes that have been previously shown to be capable of direct electron uptake from Fe0 have outer-surface c-type cytochromes known to be involved in extracellular electron exchange with other donors/acceptors (17–19, 23, 24). D. vulgaris lacks outer-surface c-type cytochromes (25). Direct electron uptake from extracellular electron donors by routes other than cytochromes is possible (37). For example, several methanogen species that lack outer-surface c-type cytochromes appear to directly accept electrons from Geobacter metallireducens (38–41). However, the results presented here demonstrate that D. vulgaris does not function as an electrotroph with Fe0 as the electron donor. If D. vulgaris is representative of the sulfate reducers most responsible for the corrosion of ferrous metals, then potent hydrogenase inhibitors might provide a targeted approach to mitigate iron corrosion.
Microbes other than sulfate reducers also contribute to corrosion (3, 33, 42, 43). Elucidating the mechanisms by which a diversity of microbes accelerate corrosion is essential for understanding why corrosion takes place, predicting corrosion rates under various environmental conditions, and developing strategies for corrosion prevention. The studies reported here further demonstrate that construction of appropriate mutants is a powerful approach to distinguish between a complexity of potential corrosion mechanisms.
MATERIALS AND METHODS
Desulfovibrio vulgaris strains JW710 and JW5095, which were constructed in the laboratory of Judy Wall, University of Missouri (31, 44), were provided from a repository of D. vulgaris mutants by Valentine V. Trotter and Adam M. Deutschbauer of the Lawrence Berkeley Laboratory. Strain JW710 is a platform strain for a markerless genetic exchange system in D. vulgaris (44). The upp gene encoding uracil phosphoribosyltransferase has been deleted, to enable utilization of the upp gene as a counterselectable marker (44). Strain JW5095 was constructed by markerless deletion of all the hydrogenases that have been described in the D. vulgaris genome: DVU1921-22, DVU2525-26, DVU1917-18, DVU1769-70, DVU0429-34, DVU2286-93, and DVU1771 (31).
Cultures were routinely grown anaerobically at 37°C in 10 mL of medium in 28-mL anaerobic pressure tubes (Bellco, Inc.) under N2/CO2 (80:20) in a modification of the previously described NBAF medium (45), designated NB medium. NB medium contains (per L of deionized water): 0.42 g of KH2PO4, 0.22 g of K2HPO4, 0.2 g of NH4Cl, 0.38 g of KCl, 0.36 g of NaCl, 0.04 g of CaCl2 · 2H2O, 0.1 g of MgSO4 · 7H2O, 1.8 g of NaHCO3, 0.5 g of Na2CO3, 1.0 mL of 1 mM Na2SeO4, 15.0 mL of a vitamin solution (46), and 10.0 mL of NB trace mineral solution. The composition of the NB trace mineral solution per L of deionized water is 2.14 g of nitrilotriacetic acid, 0.1 g of MnCl2 · 4H2O, 0.3 g of FeSO4 · 7H2O, 0.17 g of CoCl2 · 6H2O, 0.2 g of ZnSO4 · 7H2O, 0.03 g of CuCl2 · 2H2O, 0.005 g of AlK(SO4)2 · 12H2O, 0.005 g of H3BO3, 0.09 g of Na2MoO4, 0.11 g of NiSO4 · 6H2O, and 0.02 g of Na2WO4 · 2H2O. The medium pH was 6.7. Cells were routinely grown with sodium l-lactate as the electron donor (20 mM) and sodium sulfate (20 mM) as the electron acceptor. Growth was monitored by inserting culture tubes directly into a spectrophotometer and determining the A600 value. Growth with H2 as the sole electron donor was evaluated with 5 mM sodium acetate as a carbon source and H2 (140 kPa) as the sole electron donor. Cultures were incubated horizontally with shaking at 25 rpm and were routinely repressurized with H2 to compensate for any H2 consumption.
To evaluate growth with Fe0 as the potential electron donor, cells were grown in NB medium with Fe0 granules (2 g; 1 to 2 mm in diameter; Thermo Scientific) as the sole electron donor, 5 mM sulfate as the electron acceptor, and 5 mM sodium acetate as a carbon source. A 10% inoculum of a mid-log-phase culture of lactate-grown cells served as the inoculum. When specified, 50 μM riboflavin or 50 μM AQDS was added from concentrated anaerobic stock solutions. For studies with 316L stainless steel as the potential electron donor for sulfate reduction, five stainless steel cubes (5 mm × 3 mm × 3 mm) replaced the pure Fe0. The stainless-steel cubes were polished with sand paper, and the pure Fe0 and stainless steel were presterilized with ethanol as previously described (15).
Impact of added sulfide or culture supernatant on H2 production.
A final concentration of either 1.25 or 12.5 mM sodium sulfide was added to sterile Fe0-containing medium to determine whether sulfide stimulated H2 production. Culture filtrates were prepared by filtering late-log-grown cultures (Fe0-grown or H2-grown) through a 0.2 μM PES filter in a Coy anaerobic glove bag (gas phase, 7:20:73 H2/CO2/N2) into pressure tubes with 2 g of Fe0. Tubes were resealed and flushed with N2/CO2 (80:20) for 5 min. Controls were sterile NB medium.
For sulfate determinations, culture aliquots (0.1 mL) were anaerobically withdrawn with a syringe and needle, filtered (0.22 μm; polyvinylidene difluoride), and analyzed with a Dionex ICS-1000 with an AS22 column and AG22 guard with an eluent of 4.1 mM sodium carbonate and 1 mM sodium bicarbonate at 1.2 mL/min. H2 concentrations in the headspace were monitored on an Agilent 6890 gas chromatograph fitted with a thermal conductivity detector. The column was a Supelco Carboxen 1010 plot capillary column (30 m × 0.53 mm) with N2 carrier gas and 0.5-mL injections. The oven temperature was 40°C, the inlet was splitless at 5.5 lb/in2 and 225°C, and the detector had a makeup flow of 7 mL/min and a temperature of 225°C.
For confocal microscopy, Fe0 was gently removed from the pressure tube, soaked in isotonic wash buffer for 10 min, drained, stained for 10 min (Live/Dead BacLight bacterial viability kit (Thermo Fisher); 1 mL staining with 3 μL of each stain per mL), and destained for 10 min in isotonic wash buffer. Fe0 pieces were then mounted on petri plates with an antifade/glycerol mixture. Cells were visualized with a 100× objective on a Nikon A1R-SIMe confocal microscope with NIS-Elements software.
This study was made possible by using the public available Desulfovibrio vulgaris strains JW710 and JW5095 made in the laboratory of Judy Wall, University of Missouri. Thomas R. Juba constructed strain JW5095. We thank Valentine Trotter and Adam Deutschbauer of the Berkeley National Laboratory for providing strains used in this study. Confocal microscopy was performed in the Light Microscopy Facility and Nikon Center of Excellence at the Institute for Applied Life Sciences, UMass Amherst. We thank the reviewers for helpful comments that improved the manuscript.
This article is a direct contribution from Derek R. Lovley, a Fellow of the American Academy of Microbiology, who arranged for and secured reviews by Kara Deleong, University of Okalhoma, and Scott Wade, Swinburne University of Technology.
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