One of the most deleterious impacts of microbes on modern economies is metal corrosion [1]. The innovation of stainless steel, an alloy of iron, chromium, nickel, and molybdenum, was a major advance in reducing the corrosive activity of abiotic corrosive agents (O₂, chloride), as well as most corrosive microbes and their metabolites (sulfide and organic acids). This corrosion resistance can be attributed to the formation of a passive film that physically blocks corrosive agents from accessing the underlying metallic iron (Fe⁰) and also provides an electronic barrier to electron transfer from Fe⁰ to electron acceptors outside the passive film [2]. However, recent studies have demonstrated that electroactive microbes aggressively corrode stainless steel [3–9]. It has been widely proposed that electroactive microbes corrode stainless steel by progressively removing the iron-oxide outer layer and ultimately breaching the chromium-oxide inner layer of the passive film [2] to directly contact the underlying Fe⁰ [3,5,6,8,9] (Fig. 1A). This model is consistent with the prevailing view that the redox-active outer-surface proteins of electroactive microbes must contact extracellular electron donors and acceptors for direct electron exchange [10].

To better understand how electroactive microbes interact with the stainless steel passive film, studies were conducted with 316L stainless steel (subsequently referred to simply as stainless steel), one of the most corrosion-resistant types of stainless steel. As previously reported [4], it did not evolve H₂ in anaerobic incubations (Fig. 1B), demonstrating that the passive film protected the underlying Fe⁰ from reacting with protons (Fig. 1B). This contrasts with other ferrous metal forms that lack a passive film in which Fe⁰ donates electrons to protons to generate H₂ [1]:

The passive film of the stainless steel in these incubations was readily apparent as a distinct surface layer 3.5 nm thick with high-resolution transmission electron microscopy (HR-TEM) (Fig. 1C to F).

The stainless steel was treated with the reductants dithionite and sulfide, as a simplified test to mimic the electron transfer expected from electroactive microbes. The thickness of the passive films was reduced, but a distinct, intact film remained (Fig. 1D to F). Time-of-flight secondary ion mass spectrometry (ToF-SIMS) demonstrated that the dithionite- and sulfide-induced thinning was associated with the selective removal of much of the surface iron oxide layer of the passive film, but the underlying chromium oxide-rich layer that is the key protective component of the passive film remained (Fig. 1G to I). There was also no H₂ evolution (Fig. 1B), demonstrating that protons failed to reach the underlying Fe⁰ over the whole of the stainless steel surface. Because abiotic proton reduction on exposed Fe⁰ is rapid, the absence of H₂ evolution provides a highly sensitive, surface-integrative assay for passive-film continuity, placing a more stringent upper bound on any loss of chromium oxide barrier integrity than would be possible with localized surface-analytical measurements alone.

To determine whether some property of electroactive microbes other than serving as a source of electrons might further damage passive films, studies were conducted with Geobacter sulfurreducens strain ACL_HF. G. sulfurreducens is the most aggressively corroding electroactive microbe known [4,7]. Strain ACL_HF cannot use H₂ or formate as an electron donor, but corrodes stainless steel as fast as the wild-type strain [4]. Studies were conducted in a defined medium with fumarate as the only potential electron acceptor and stainless steel as the only potential electron donor and energy source [4].

As previously reported [4], strain ACL_HF grew as biofilms on the stainless steel surface (Fig. S1) and reduced fumarate to succinate (Fig. 2A), which is associated with high rates of stainless corrosion [4]. HR-TEM and ToF-SIMS revealed that, like the treatments with dithionite and sulfide, strain ACL_HF removed a substantial quantity of the iron oxides, but the chromium oxide-rich layer remained (Fig. 2C to G). In contrast to the steady electron flux to strain ACL_HF, there was no H₂ production (Fig. 2B), demonstrating that the chromium oxide component of the passive film retained its integrity, preventing corrosive agents even as small as protons from reaching the underlying Fe⁰ and remaining sufficiently insulating to restrict electron transfer through the passive film to external protons for H₂ production. Although some electroactive microbes interact with extracellular acceptors/donors with soluble electron shuttles, this possibility for electron transfer can be ruled out because (a) G. sulfurreducens does not produce electron shuttles; (b) even pure Fe⁰ reacts sluggishly with electron shuttles; and (c) exclusion of protons would also exclude larger shuttle molecules [10,11]. Yet, strain ACL_HF was able to extract electrons from the Fe⁰ underlying the passive film to support fumarate reduction.

The outer-surface redox-active proteins of electroactive microbes lower the activation energy required for oxidation or reduction at electrode surfaces, enabling oxidation/reduction reactions at much lower overpotentials [10]. Deleting genes for multi-heme c-type cytochromes that serve as outer-surface electrical contacts inhibits G. sulfurreducens stainless steel corrosion [4]. Additions of nanocrystals of magnetite, which functions like cytochromes to enhance extracellular electron exchange, accelerate it [7]. Therefore, we propose that the redox-active proteins at the microbe–passive film interface lower the activation barrier for electron transfer to the microbe below that required for abiotic H₂ evolution. This concept is consistent with electrochemical impedance spectroscopy, which demonstrated that the charge transfer resistance between the stainless steel and G. sulfurreducens was ca. 9-fold lower than in the abiotic control (Figs. S2 and S3). Localized defects or thinning sufficient to permit direct microbial contact with Fe⁰ are unlikely, because such breaches would also allow proton access to the metal surface and lead to detectable H₂ evolution, which was not observed. Instead, the findings suggest that while the passive film remains sufficiently insulating to block abiotic proton reduction, the redox activity of G. sulfurreducens can pull electrons from the underlying Fe⁰ across the passive film to support anaerobic respiration. This is analogous, with the direction of electron flow reversed, to the well-documented electron transfer over micrometer to millimeter scales from Geobacter species to electron-accepting minerals or cells of other microbial species when they are both in contact with diverse (semi-)conductive materials [10]. Determining whether this biologically activated electron transfer occurs via quantum tunneling or redox-active defect sites within the chromium-oxide lattice will require future dedicated studies beyond the scope of this Rapid Report.

These results reveal that electroactive microbes can “short-circuit” the passive film that physically and electrically protects Fe⁰ from other corrosive chemicals and microbes (Fig. 2H). Preventing electrobiocorrosion will likely require alloy or coating designs that suppress biologically activated interfacial electron transfer, not merely abiotic corrosion pathways. The discovery that microbes can drive electron flux through a material once considered electrically insulating also greatly expands the range materials that may facilitate microbe–mineral or microbe–microbe electron exchange.