Iron (Fe)- and manganese (Mn)-oxidizing bacteria are often cited individually and collectively as putative microorganisms for microbiologically influenced corrosion (MIC). The two groups of microorganisms have in common the ability to attach to surfaces and produce macroscopic accumulations (deposits) of metal oxides/hydroxides/oxyhydroxides that can influence corrosion of some metals and alloys in some environments. In all cases, once initiated, the corrosion is independent of the activities of the colonizing species. Despite the phylogenetic diversity of Fe-oxidizing bacteria (FeOB), the following sections will deal with corrosion mechanisms attributed to neutrophilic, lithotrophic, microaerophilic FeOB. The mineralogy of biologically oxidized Fe is consistent over a wide range of environments. All FeOB produce dense deposits that can cause corrosion of low alloy stainless steels (SS) directly, i.e., under-deposit corrosion. Association of Mn-oxidizing bacteria (MnOB) and other microorganisms may stabilize the under-deposit corrosion on low alloy SS. The influence of FeOB on the corrosion of carbon steel may be related to deposition of metal ions, causing galvanic corrosion or association with other corrosion-causing microorganisms. All MnOB produce Mn oxides that are strong oxidizing agents that can cause ennoblement of low alloy SS and increase corrosion currents on carbon steel in fresh water. Corrosion associated with Mn deposits depends on the relationship between the mineral deposit and the substratum.

THE MICROORGANISMS

Iron-Oxidizing Bacteria

Under a range of environmental conditions microorganisms from both Archaea and Bacteria domains can use the redox potential between ferric iron (Fe3+) and ferrous iron (Fe2+) to produce energy.1  Abiotic oxidation of Fe2+ in fully oxygenated water is rapid (i.e., half-life <1 min). Significant microbial iron (Fe) oxidation is limited to microaerobic conditions (e.g., 50 μM dissolved oxygen [DO]) where the half-life of Fe2+ can be up to 300 times longer.2  In neutral environments, solubleFe2+ is typically located at redox boundaries between oxic and anoxic regions and at corroding Fe substrata. In these environments neutrophilic, lithotrophic, microaerophilic Fe-oxidizing bacteria (FeOB) can compete with the kinetics of abiotic oxidation, conserve energy from the process, and convert inorganic carbon (i.e., CO2) into biomass. FeOB could inhabit any environment where Fe2+and O2 coexist.3 

To date, all cultivated oxygen-dependent obligate lithotrophic FeOB growing at neutral pH are members of the Proteobacteria.1,4-5  Freshwater species belong to the betaproteobacteria class and marine species belong to the zetaproteobacteria class. Zetaproteobacteria have been isolated in marine benthic environments6  and redox stratified estuarine water columns.3  James, et al.,7  performed both interspecies and intersite comparisons to conclude that precipitation of Fe3+ minerals in response to metabolic and autocatalytic Fe2+ oxidation is a common trait associated with lithotrophic FeOB. Kato, et al.,8  used comparative genomic analyses to conclude that freshwater and marine lithotrophic FeOB share common electron transport mechanisms and biomineralization pathways.

Fe3+ minerals include sixteen oxides, hydroxides, and oxyhydroxides9  and will further be collectively referred to as Fe oxides,10  unless otherwise noted. When Fe2+ is oxidized to Fe3+ at neutral pH, the Fe3+ will hydrolyze water and precipitate Fe3+ oxide. Deposition of Fe oxides by FeOB can occur in association with polymers, especially negatively charged acidic polysaccharides, e.g., extracellular stalks and sheaths produced by some FeOB. Fe-encrusted, twisted, polymeric stalks provide a “robust biosignature” for lithotrophic Fe-oxidizing metabolism (Figure 1).11  Fe-encrusted stalks have been identified in tubercles on carbon steel and cast Fe in drinking water distribution systems12  and on carbon steels pilings in fresh13-14  and marine waters.15 

In natural and industrial waters FeOB produce bacteriogenic iron oxides (BIOS) made up of live cells, dead cells, and extracellular material. The minerals resulting from FeOB activity are high surface-area nanoparticles that can accumulate metal ions, in addition to Fe3+ and nutrients.17  Several morphologies of BIOS, including dreads (resembling dreadlocks) and granules (nanoBIOS), have been identified.8  In all cases, BIOS formation results in the localized accumulation of Fe oxides/oxyhydroxides. Once deposited, the Fe oxides are net negatively charged and attract more positively charged Fe hydroxide ions. Such a process can continue indefinitely without any biological activity.18 

The biogenic mineral associated with BIOS produced by FeOB is always poorly crystalline nanoparticulate forms of ferrihydrite [(Fe3+)2O3•0.5 H2O].2,19  Because of its strong adsorptive capacity and large surface area, ferrihydrite is a sink for trace metals, metalloids, silicates, and organic matter.20  Ferrihydrite is a metastable mineral and a precursor to more crystalline minerals like hematite (Fe2O3) and goethite (α-FeOOH).21  The transformation of ferrihydrite in natural systems can be blocked by adsorbed chemical impurities, e.g., silicates.22 

Manganese-Oxidizing Bacteria

Manganese-oxidizing bacteria (MnOB) oxidize soluble divalent Mn (Mn2+) to the insoluble manganic (Mn3+ and Mn4+) oxides. Some bacteria, e.g., Leptothrix spp., can oxidize both soluble Fe2+ and Mn2+. Many different organisms, including bacteria, fungi, algae, and some eukaryotes, can catalyze Mn oxidation. Tebo, et al.,23  concluded that there was no definitive proof of lithotrophic Mn oxidation, meaning that Mn2+ oxidation does not produce energy for the microorganism.

In contrast to Fe2+, Mn2+ does not undergo abiotic oxidation rapidly below pH 9, suggesting that biological oxidation dominates in the environment.23  Abiotic Mn2+ oxidation requires strong oxidizing biocides, e.g., chlorine, peroxide, and ozone.24  Because of the stability of Mn2+ to chemical reactions, biomineralization takes place in fully oxygenated waters. Biomineralization of Mn2+ results in a layered structure (phyllomanganate) composed predominantly of Mn4+ and is a mineral similar to birnessite, a manganese oxide containing calcium, potassium and sodium.23 

Mn4+ oxide(s) (MnO2)(s) produced by microorganisms are among the most abundant and highly reactive Mn oxide phases in the environment.23  MnO2(s) and the mixed valence Mn4+/Mn3+ (hydroxyl)oxides (MnOOH) are collectively referred to as manganates,25  and will be henceforth, unless otherwise noted. Manganates are negatively charged; consequently, hydrogen ions, alkalis, alkaline earth, and transition metal cations sorb to manganates.23  Once manganate has formed on a surface, additional Mn2+ and Fe2+ can be sorbed and chemically oxidized without additional microbial activity.26 

CORROSION IN FRESH WATER ENVIRONMENTS

Stainless Steel ≤20% Chromium

The vulnerability of stainless steel (SS) alloys ≤20% chromium (Cr) to microbiologically influenced corrosion (MIC) is widely acknowledged. In 1994, a review of the literature since 1978 reported over 30 publications documenting MIC of types 304 and 316 SS and their low-carbon counterparts. The vulnerability of these alloys is directly related to the propensity to develop under-deposit or crevice corrosion and the acidity that develops in the pits/crevices during hydrolysis reactions. Sedriks27  reviewed the effects of alloy composition on pitting potential (Epit). An alloy with ≤20% Cr and no molybdenum (Mo) (e.g., 304 SS) has an Epit close to the corrosion potential (Ecorr). Alloying Mo does increase Epit and resistance to pitting. However, the 2% Mo added to 316 SS does not provide protection from crevice corrosion or under-deposit corrosion. Kovach and Redmond28  cited the absence of reports of MIC in alloys with 6% Mo as evidence that those materials were a “practical engineering solution” to MIC.

Specific microorganisms and specific mechanisms were not mentioned in the Kovach and Kovach and Redmond reviews.28  Kobrin29  was among the first to report pitting corrosion of austenitic SS (UNS S30403 [304L](1) and UNS S31603 [316L]) tanks and piping due to “Mn and Fe concentrating microorganisms” after exposure to stagnant hydrotest water (≤200 ppm chloride [Cl]).The microorganisms were identified by an unspecified microbiological analysis in mound-like deposits containing Fe, Mn, and chlorine (Cl). The mounds were often localized at welds. The mounds have subsequently been termed tubercles and the deposits, BIOS. In addition to the mounds, Kobrin29  reported a reddish-brown sludge layer at the bottom of one 316L pitted tank. Following the publication of Kobrin’s case histories29  describing the role of FeOB and MnOB in the pitting corrosion of the 300 series SS alloys, there followed a number of papers documenting pitting corrosion of UNS S30400 (304), UNS S31600 (316) and their low-carbon alloys (UNS S30403 [304L] and UNS S31603 [316L], respectively) after exposure to low Cl, natural and processed waters containing FeOB and MnOB. The relationship between FeOB, tubercle formation and corrosion at welds in 300 series SS alloys is so well established that MIC of these alloys is often taken for granted if tubercles have formed along a weld.30  Several arguments have been made for the relationship of MIC and welds including the following: microstructure,31-32  bead shape,33  surface roughness,31  and essential element segregation during welding.31 

The following is a summary of current understanding of MIC by FeOB on 304/304L and 316/316L alloys. Corrosion occurs at ambient temperatures in waters with Cl concentrations considered acceptable for 300 series SS (i.e., 200 ppm for 304/304L and 1,000 ppm for 316/316L).34  Pitted surfaces are covered with slimy, reddish-brown deposits. Mounds, containing microorganisms, cover flask-shaped pits. Corrosion rates are aggressive, e.g., 1 mm per month.35-36  Stagnation provides quiescent conditions conducive to the formation of microaerobic conditions and Fe2+ oxidation by FeOB at the metal/water interface. The mechanism for MIC is reportedly under-deposit corrosion caused by dense deposits of BIOS that effectively exclude oxygen from the area under the deposit. In an oxygenated environment, the area deprived of oxygen is a relatively small anode compared to the large surrounding oxygenated cathode (Figure 2). Metal at the anode dissolves, forming metal cations that undergo hydrolysis and decrease pH. The extent of the pH decrease is determined by the alloy composition.27,37  Hydrolysis reactions for Cr suggest pH values <2.0.38  In addition, Cl from the electrolyte migrates to the anode to neutralize charge within the pit and forms metal Cl(s) that are extremely corrosive. Under these circumstances, pitting involves the conventional features of differential aeration leading to oxygen concentration cells, a large cathode: anode surface area, and the development of acidity and metallic Cl(s).39 

There have been several challenges to the above model for the mechanism of FeOB influenced corrosion of 300 series SS alloys. Suleiman, et al.,40  tested the hypothesis that Fe oxides deposited by typical FeOB (e.g., Gallionella) in potable (i.e., low Cl) waters could stabilize pitting in 304L. They electrodeposited Fe oxides on 304L and demonstrated that the oxides were anion-selective at near-neutral pH. They reported that the deposits acted as “super crevices” in low Cl containing waters (0.005 M NaCl), permitting transport of aggressive anions (e.g., Cl) to the SS surface, but preventing the transport of metal ions away from the surface. However, in laboratory experiments, the effect of the abiotic deposits was short-lived, dissolved by the acidic solution within propagating pits. Similarly, Mathiesen and Frantsen30  reported case studies of failures of SS alloys 304, 316, and 316 L in low Cl waters. They concluded that the failures, always associated with voluminous tubercles, could not be the result of oxygen concentration cells alone. They made reference to possible ennoblement due to concurrent Mn deposition and further suggested that bacteria associated with tubercles, other than FeOB, could produce aggressive sulfide or thiosulfate.

Development of oxygen concentration cells (under-deposit corrosion), similar to those described for FeOB, has been cited as the mechanism for pitting in SS alloys ≤20% Cr in the presence of MnOB in fresh river water41  with one notable difference. Microbial deposition of Mn causes a shift of Ecorr in the positive direction, a process called ennoblement (Figure 3).42  Ennoblement increases the likelihood that stable pitting will occur in association with surface deposits on vulnerable alloys. The result is that SS alloys ≤20% Cr (e.g., 316L, UNS S32100) experience ennobled Ecorr, with high susceptibility to localized corrosion in fresh water containing ppm quantities of Cl.43 

Linhardt44  described a pitting corrosion failure in a hydroelectric plant attributed specifically to MnOB. From 1994 to the present there have been numerous published case histories of corrosion in industries due to biomineralized manganate on 304, 316L, and martensitic alloy EN1.4313 (UNS S41500).43-52  Linhardt and Nichtawitz49  observed a relationship between duration of stagnation, extent of manganate formation, and the severity of corrosion attack.

Dickinson and Lewandowski41  were the first to demonstrate biomineralized Mn deposits altered the electrochemical behavior of SS. MnOB deposited MnO2 directly around the cells in fresh water biofilms at the metal/biofilm interface in waters containing as little as 6 ppb Mn.30  Dickinson and Lewandowski53  demonstrated a 6% surface coverage of manganate deposits increased Ecorr of 316L SS by 500 mV. In laboratory experiments with a fresh water MnOB (Leptothrix discophora), Ecorr increased from 100 mVSCE to 350 mV in less than 40 h.54  Shi, et al.,55  demonstrated that as ennoblement of 316L SS and UNS R56400 (Ti-6Al-4 V) in the presence of Leptothrix discophora progressed, the total amount of surface-related manganate increased. They further concluded that mineral deposits on partially ennobled samples were MnOOH and Mn2O, whereas the mineral on fully ennobled surfaces was Mn2O. Lewandowski, et al.,56  demonstrated that pits initiated at the sites of bacterial attachment.

Ghiorse and Hirsch18  examined metal oxide deposition in a medium with a Pedomicrobium-like budding bacteria and low concentrations of both Fe2+ and Mn2+. In all cases manganates and Fe oxides accumulated in “intimate association with extracellular polymers produced by the cells.” In a series of experiments the authors concluded that the manganate accumulation was controlled by a biological Mn-oxidizing factor and that Fe deposition was the result of passive, nonbiological processes. Furthermore, Mn was preferentially deposited in association with extracellular polymers before Fe.

It is well established that Mn deposition on passive alloys in fresh water can produce ennoblement and that ennoblement can stabilize pitting. However, the presence of manganates on a 300 series SS surface cannot be interpreted as an indication of ennoblement. Kielemoes, et al.,57  demonstrated accumulation of Fe and Mn in a biofilm on 316L fed with brackish surface water. No ennoblement was measured and no signs of corrosion were detected. A requirement for ennoblement and increased susceptibility to localized corrosion is direct contact of the manganate with the metal surface. Increased manganate deposition will support a greater number of pitting sites, increasing the probability that a metastable site will become fixed. The extent to which the elevated current density can be maintained is controlled by the electrical capacity of the mineral, reflecting both total accumulation and conductivity of the mineral. The biomineralization rate and the corrosion current control manganate accumulation. Mn cycling at the surface of a passive metal, either by microbial reduction of Mn2O or by electrochemical reactions, produces renewable cathodic reactants.

Researchers have evaluated the possibility that a combination of under-deposit corrosion and ennoblement could be used to explain the aggressive corrosion of SS alloys ≤20% Cr. Chamritski, et al.,58  reproduced the Suleiman, et al.,40  observation in the laboratory by depositing a layer of Fe oxides on 304. The open-circuit potential of samples covered with Fe oxides, typical of those deposited by FeOB, was approximately 200 mV lower than that of control samples. The results suggested that pitting in 304 in potable water was enabled by pit-stabilizing effects of Fe oxides. However, the authors reported that, despite the effects of the combination of FeOB and MnOB, their presence could not account for the aggressive corrosion in the low-Cl medium.

Both Chamritski, et al.,58  and Newman, et al.,59  suggested that pitting in 304L and 304 alloys, respectively, could be influenced by oxidation of sulfate/sulfide mixtures. Such a circumstance could be relevant in a situation where sulfate-reducing bacteria (SRB) reduced a sulfate to sulfide that was subsequently oxidized to thiosulfate. Deposits produced by FeOB have long been proposed as probable niches for SRB on 300 series SS. The problem with the potential sulfur-assisted pitting mechanism is the inability of investigators to demonstrate SRB or sulfur compounds in association with FeOB or MnOB.29,36,60  Pit solutions in 304 and 316 are highly acidic (pH <2)37  and may not be suitable environments for SRB.

Zhang, et al.,61  and Xu, et al.,62  conducted laboratory experiments with Fe-oxidizing and sulfate-reducing isolates exposing 316L to a nutrient-rich medium containing yeast extract (YE [1 g/L]). The microorganisms were isolated from a cooling water at an oil refinery and were not further identified. Individual isolates and a mixed culture produced μM-sized open-mouthed shallow pits. The authors concluded that the mixed culture produced the highest corrosion rate. Works by Zhang, et al.,61  and Xu, et al.,62  illustrate some synergy between the SRB and FeOB; however, the data do not relate to a natural oligotrophic environment in which occluded pits develop with aggressive pit solutions. YE contains riboflavin and other B vitamins that can act as redox mediators, sorb to surfaces, and chelate metal ions. The presence of YE in the electrolyte complicates the interpretation of the electrochemical data.63 

Carbon Steel

The influence of manganates on the corrosion behavior of active alloys (e.g., carbon steel) in fresh water environments differs from that described for passive (e.g., SS alloys) metals. For mild steels under anodic control, manganates can elevate corrosion current but cause little positive shift in Ecorr. The increase in corrosion current can be significant for a mild steel covered with large mineral surfaces. Olesen, et al.,64  evaluated the effect of biomineralized Mn on the corrosion behavior of UNS C1008 mild steel. They concluded that deposition of Mn cannot be expected to cause elevated corrosion in systems built solely of mild steel. They further theorized that corrosion products electrically isolated the biominerals from the underlying metal and inhibited the cathodic effect of the mineral. However, when manganates were deposited on a passive alloy in electrical contact with mild steel the corrosion rate of the mild steel increased significantly.

Ridgway and Olson65  used scanning electron microscopy to demonstrate helical stalks (typical of lithotrophic Fe metabolism) partially coated with insoluble Fe3+ deposits attached to Fe oxides on pipe surfaces in a drinking water distribution system. There was no suggestion that FeOB were responsible for corrosion.

Ray, et al.,66  demonstrated Fe-encrusted helical stalks on and in the core regions of tubercles from many fresh water sources. Ray, et al.,67  examined the cause of aggressive localized corrosion associated with tubercles on carbon steel pilings in Duluth-Superior Harbor, Minnesota and Wisconsin (DSH), a freshwater harbor (Cl ≃ 1.42 ppm). Pitting occurred under tubercles of porous layers with Cu localized at the base. Ray, et al.,67  used galvanically coupled carbon steel electrodes isolated from each other in individual aerobic and anaerobic cells connected to a potentiostat/zero resistance ammeter to demonstrate that the magnitude of the resulting galvanic current was related to the amount of copper deposited on the anaerobic surface, which was directly related to the concentration of dissolved Cu2+. From the same steel pilings in DHS, Hicks60  isolated an Fe-related bacterium with 96% genetic similarity to Sideroxydans lithotrophicus, a neutrophilic, autotrophic, microaerophilic FeOB found in Fe2+-containing groundwater in Michigan.68 

In both field69  and laboratory70  observations, researchers have demonstrated a synergy between FeOB and SRB on corroding carbon steel in fresh water, suggesting that FeOB may provide the conditions for colonization by other microorganisms, especially SRB.

Liu, et al.,70  conducted experiments with an unidentified aerobic FeOB and anaerobic SRB isolated from oilfield sludge. Corrosion experiments with individual and combined isolates were conducted in an artificial medium consistent with a produced oilfield water and maintained with 4.2 ppm DO. Weight loss, an indication of uniform corrosion, was evaluated after 21 d. The mixed culture produced greater weight loss than the FeOB alone. Interestingly, the FeOB inhibited the growth of planktonic SRB but promoted the growth of sessile SRB. The greatest loss was measured in exposures with the SRB inoculum.69 

CORROSION IN MARINE ENVIRONMENTS

Stainless Steel ≤20% Chromium

SS ≤20% Cr are not typically recommended for seawater service27  because of susceptibility to crevice corrosion. However, these alloys have been used to study ennoblement of Ecorr resulting from marine biofilms. Ennoblement of passive alloys in marine environments has been attributed to depolarization of the oxygen-reduction reaction due to organometallic catalysis, microbial enzymes, unidentified extracellular chemicals, acidification of the electrode surface, the combined effects of elevated hydrogen peroxide (H2O2) and decreased pH, and the production of passivating siderophores.71  Ennoblement in marine waters has never been attributed to MnOB or FeOB. Martin, et al.,72  compared ennoblement of several alloys, including 304 SS, at two coastal seawater locations: Key West, Florida (oligotrophic sea water) and Delaware Bay (coastal seawater). The two locations have different temperatures and different salinities. They demonstrated that extent of ennoblement was site-specific, varying 100 mVSCE between locations, with higher potentials at Delaware Bay. Localized corrosion was observed for 304 exposed in Key West, but not in Delaware Bay. In summary, Martin, et al.,72  demonstrated that extent of ennoblement varied between two locations and that the extent of ennoblement for a particular material could not be used to predict an increased likelihood of localized corrosion for a crevice corrosion-prone alloy, i.e., 304 SS.

Carbon Steel

Unprotected carbon steel is not typically used for marine applications. There are no reported instances of MIC attributed to FeOB or MnOB in marine environments. McBeth, et al.,73  demonstrated that zetaproteobacteria were among the first colonizers on corroding carbon steel in a coastal marine environment. In this case the FeOB did not cause the corrosion of the unprotected carbon steel but did take advantage of Fe2+ at the microaerobic corroding metal interface. McBeth, et al.,73  concluded that coastal sediments were rich in FeOB that quickly colonized surfaces where Fe2+ was available.

Fe-encrusted twisted stalks, indicative of lithotrophic Fe metabolism, have been identified on and in Fe-rich accumulations, “rusticles,” on low alloy steel components of marine shipwrecks.74  Meter-long rusticles on the RMS Titanic have received a great deal of attention and sensational headlines indicating that bacteria are eating the Titanic.75  Cullimore and Johnsen76  described the rusticles on the RMS Titanic as “a complex of microbial communities within a Fe-rich and calcium deficient porous-like home.” They proposed a corrosion mechanism whereby bacteria were extracting Fe from the steel of the ship. The conclusion that the accumulations were solely the result of corrosion led to calculations of hull weight loss based on an estimation of Fe in the accumulations. Cullimore and Johnsen76  estimated a daily loss of between 0.13 tons and 0.20 tons and an estimated lifetime of 280 y to 420 y for that wreck. One of the problems with the interpretation that the FeOB are causing the anodic dissolution of the hull is that no cathodic reaction has been identified. Furthermore, Salazar and Little77  reviewed environmental sources of dissolved and colloidal Fe at the Titanic wreck site. Because of the large depositional potential for dissolved and particulate Fe in the area of the Titanic and the propensity for Fe oxides to accumulate abiotically, they concluded that environmental Fe was a contributor to rusticle formation on the RMS Titanic.

SUMMARY

Any discussion of MIC mechanisms due to metal-depositing bacteria must include environmental considerations. Metal-depositing bacteria, both FeOB and MnOB, are ubiquitous. Once Fe oxides and manganates have formed on a surface, abiotic processes can contribute to further oxidation and accumulation. FeOB have been identified in all environments where Fe2+ is prevalent, including corroding Fe surfaces. The presence of Fe encrusted shapes consistent with FeOB in corrosion products cannot be interpreted as MIC. The source of the Fe associated with FeOB can be either Fe from a substratum or environmental Fe. Under-deposit corrosion of 300 SS in fresh water may be the result of a combination of microbiological contributors, e.g., ennoblement caused by MnOB deposition of manganates. Deposits produced by FeOB on carbon steel in fresh water may provide an environments for deposition of Cu or for growth of SRB. There are no credible reports of MIC of ferrous alloys due to FeOB or MnOB in the marine environment.

(1)

UNS numbers are listed in Metals and Alloys in the Unified Numbering System, published by the Society of Automotive Engineers (SAE International) and cosponsored by ASTM International.

ACKNOWLEDGMENTS

NRL publication JA/7330-18-3991.

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