A Novel Shewanella Isolate Enhances Corrosion by Using Metallic Iron as the Electron Donor with Fumarate as the Electron Acceptor

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ABSTRACT

The involvement of Shewanella spp. in biocorrosion is often attributed to their Fe(III)-reducing properties, but they could also affect corrosion by using metallic iron as an electron donor. Previously, we isolated Shewanella strain 4t3-1-2LB from an acetogenic community enriched with Fe(0) as the sole electron donor. Here, we investigated its use of Fe(0) as an electron donor with fumarate as an electron acceptor and explored its corrosion-enhancing mechanism. Without Fe(0), strain 4t3-1-2LB fermented fumarate to succinate and CO ₂, as was shown by the reaction stoichiometry and pH. With Fe(0), strain 4t3-1-2LB completely reduced fumarate to succinate and increased the Fe(0) corrosion rate (7.0 ± 0.6)-fold in comparison to that of abiotic controls (based on the succinate-versus-abiotic hydrogen formation rate). Fumarate reduction by strain 4t3-1-2LB was, at least in part, supported by chemical hydrogen formation on Fe(0). Filter-sterilized spent medium increased the hydrogen generation rate only 1.5-fold, and thus extracellular hydrogenase enzymes appear to be insufficient to explain the enhanced corrosion rate. Electrochemical measurements suggested that strain 4t3-1-2LB did not excrete dissolved redox mediators. Exchanging the medium and scanning electron microscopy (SEM) imaging indicated that cells were attached to Fe(0). It is possible that strain 4t3-1-2LB used a direct mechanism to withdraw electrons from Fe(0) or favored chemical hydrogen formation on Fe(0) through maintaining low hydrogen concentrations. In coculture with an Acetobacterium strain, strain 4t3-1-2LB did not enhance acetogenesis from Fe(0). This work describes a strong corrosion enhancement by a Shewanella strain through its use of Fe(0) as an electron donor and provides insights into its corrosion-enhancing mechanism.

IMPORTANCE Shewanella spp. are frequently found on corroded metal structures. Their role in microbial influenced corrosion has been attributed mainly to their Fe(III)-reducing properties and, therefore, has been studied with the addition of an electron donor (lactate). Shewanella spp., however, can also use solid electron donors, such as cathodes and potentially Fe(0). In this work, we show that the electron acceptor fumarate supported the use of Fe(0) as the electron donor by Shewanella strain 4t3-1-2LB, which caused a (7.0 ± 0.6)-fold increase of the corrosion rate. The corrosion-enhancing mechanism likely involved cell surface-associated components in direct contact with the Fe(0) surface or maintenance of low hydrogen levels by attached cells, thereby favoring chemical hydrogen formation by Fe(0). This work sheds new light on the role of Shewanella spp. in biocorrosion, while the insights into the corrosion-enhancing mechanism contribute to the understanding of extracellular electron uptake processes.

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Iron corrosion by novel anaerobic microorganisms.

Friedrich Widdel, Jan Kuever, Achim Hassel … (2004)

Corrosion of iron presents a serious economic problem. Whereas aerobic corrosion is a chemical process, anaerobic corrosion is frequently linked to the activity of sulphate-reducing bacteria (SRB). SRB are supposed to act upon iron primarily by produced hydrogen sulphide as a corrosive agent and by consumption of 'cathodic hydrogen' formed on iron in contact with water. Among SRB, Desulfovibrio species--with their capacity to consume hydrogen effectively--are conventionally regarded as the main culprits of anaerobic corrosion; however, the underlying mechanisms are complex and insufficiently understood. Here we describe novel marine, corrosive types of SRB obtained via an isolation approach with metallic iron as the only electron donor. In particular, a Desulfobacterium-like isolate reduced sulphate with metallic iron much faster than conventional hydrogen-scavenging Desulfovibrio species, suggesting that the novel surface-attached cell type obtained electrons from metallic iron in a more direct manner than via free hydrogen. Similarly, a newly isolated Methanobacterium-like archaeon produced methane with iron faster than do known hydrogen-using methanogens, again suggesting a more direct access to electrons from iron than via hydrogen consumption.

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Corrosion of iron by sulfate-reducing bacteria: new views of an old problem.

Dennis Enning, Julia Garrelfs (2014)

About a century ago, researchers first recognized a connection between the activity of environmental microorganisms and cases of anaerobic iron corrosion. Since then, such microbially influenced corrosion (MIC) has gained prominence and its technical and economic implications are now widely recognized. Under anoxic conditions (e.g., in oil and gas pipelines), sulfate-reducing bacteria (SRB) are commonly considered the main culprits of MIC. This perception largely stems from three recurrent observations. First, anoxic sulfate-rich environments (e.g., anoxic seawater) are particularly corrosive. Second, SRB and their characteristic corrosion product iron sulfide are ubiquitously associated with anaerobic corrosion damage, and third, no other physiological group produces comparably severe corrosion damage in laboratory-grown pure cultures. However, there remain many open questions as to the underlying mechanisms and their relative contributions to corrosion. On the one hand, SRB damage iron constructions indirectly through a corrosive chemical agent, hydrogen sulfide, formed by the organisms as a dissimilatory product from sulfate reduction with organic compounds or hydrogen ("chemical microbially influenced corrosion"; CMIC). On the other hand, certain SRB can also attack iron via withdrawal of electrons ("electrical microbially influenced corrosion"; EMIC), viz., directly by metabolic coupling. Corrosion of iron by SRB is typically associated with the formation of iron sulfides (FeS) which, paradoxically, may reduce corrosion in some cases while they increase it in others. This brief review traces the historical twists in the perception of SRB-induced corrosion, considering the presently most plausible explanations as well as possible early misconceptions in the understanding of severe corrosion in anoxic, sulfate-rich environments.

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The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis.

Michael Baron, Dan Coursolle, Daniel Bond … (2009)

The Mtr respiratory pathway of Shewanella oneidensis strain MR-1 is required to effectively respire both soluble and insoluble forms of oxidized iron. Flavins (riboflavin and flavin mononucleotide) recently have been shown to be excreted by MR-1 and facilitate the reduction of insoluble substrates. Other Shewanella species tested accumulated flavins in supernatants to an extent similar to that of MR-1, suggesting that flavin secretion is a general trait of the species. External flavins have been proposed to act as both a soluble electron shuttle and a metal chelator; however, at biologically relevant concentrations, our results suggest that external flavins primarily act as electron shuttles for MR-1. Using deletion mutants lacking various Mtr-associated proteins, we demonstrate that the Mtr extracellular respiratory pathway is essential for the reduction of flavins and that decaheme cytochromes found on the outer surface of the cell (MtrC and OmcA) are required for the majority of this activity. Given the involvement of external flavins in the reduction of electrodes, we monitored current production by Mtr respiratory pathway mutants in three-electrode bioreactors under controlled flavin concentrations. While mutants lacking MtrC were able to reduce flavins at 50% of the rate of the wild type in cell suspension assays, these strains were unable to grow into productive electrode-reducing biofilms. The analysis of mutants lacking OmcA suggests a role for this protein in both electron transfer to electrodes and attachment to surfaces. The parallel phenotypes of Mtr mutants in flavin and electrode reduction blur the distinction between direct contact and the redox shuttling strategies of insoluble substrate reduction by MR-1.