Bioelectrical corrosion of iron by lithotrophic sulfate-reducing bacteria

Abstract

Iron, a technological material of prime importance, deteriorates by interaction with its abiotic and biotic environment. While the corrosion of iron in oxic environments is, to our present knowledge, a largely chemical (abiotic) process, corrosion in anoxic environments is heavily affected by microbial activity. In technology, this is referred to as microbially influenced corrosion (MIC). Contrary to the more prominent rusting of iron with oxygen, MIC usually is a hidden process occurring in places such as closed cooling water systems or buried pipelines. The inferred economic costs are tremendous. Sulfate-reducing bacteria (SRB) are the suspected main culprits; MIC usually is most severe in sulfate-containing environments, and iron sulfides (FeS), the characteristic product of SRB-induced corrosion, are ubiquitously found at the affected sites. Metal destruction by SRB is conventionally attributed to three effects, (i) the chemical aggressiveness of their metabolic product sulfide, (ii) a facilitated cathodic reduction of protons to molecular hydrogen at deposited iron sulfides and (iii) the microbial consumption of cathodic hydrogen from the iron or iron sulfides. Recently, another mechanism, i.e. direct electron uptake from metallic iron, has been discovered in specialized lithotrophic SRB that were isolated from enrichment cultures with iron as the only source of electrons (Dinh et al., 2004). In the present study we investigated the suggested mechanisms of SRB-induced corrosion with particular emphasis on the latter, bioelectrical process. This was achieved by a combination of kinetic and electrochemical studies in axenic SRB microcosms, and the physicochemical analysis of the formed corrosion products. Little or no corrosion resulted from galvanically coupled iron sulfides and microbial consumption of hydrogen, respectively. However, the specialized lithotrophic SRB corroded metallic iron severely and formed large amounts of an electroconductive mineral crust. Their corrosiveness results from the formation of a galvanic element between the iron anode and the bacterial cathode. Electrons flow from the iron through the sulfidic crust to the crust-attached bacteria reducing sulfate. The biological cathodic reaction controls the rate and, with appropriately adjusted cultivation conditions, such bioelectrical corrosion progressed at technologically highly relevant rates in long-term incubations. The direct corrosion of iron through electron uptake is here referred to as electrical microbially influenced corrosion (EMIC). This mechanism is fundamentally different from the indirect corrosive effect of SRB owing to the excretion of the chemical hydrogen sulfide (chemical microbially influenced corrosion, CMIC). CMIC is also known to progress at high rates in laboratory cultures. Hence, we intended to unravel the relative contribution of EMIC and CMIC to total microbial corrosion in natural sulfate-rich environments. Careful chemical analysis of corrosion products combined with knowledge of the fundamental differences of the two corrosion mechanisms allowed such quantitative assessment. In a marine tidal mud flat, studied as an example of a sulfate-rich environment possibly favoring MIC, severe metal corrosion could indeed be observed and exclusively attributed to EMIC, i.e. bioelectrical corrosion by lithotrophic SRB. A better understanding of microbial corrosion mechanisms as well as their quantitative contribution to corrosion damage is expected to aid in the development of more effective MIC prevention and mitigation strategies. The striking physiological ability of the organisms to corrode iron by direct electron uptake apparently has polyphyletic origin; it was found in several phylogenetically unrelated bacterial isolates. However, the ecological role of such microorganisms in their natural (metal-free) habitat is currently unknown. Interestingly, we detected high numbers of directly corrosive SRB in marine anoxic sediment, despite obvious absence of man-made iron constructions. It is hypothesized that anaerobic biocorrosion is due to the promiscuous use of an ecophysiologically relevant catabolic trait for uptake of external electrons from natural abiotic and biotic sources.