February 2014⎪Vol. 24⎪No. 2

J. Microbiol. Biotechnol. (2014), 24(2), 280–286http://dx.doi.org/10.4014/jmb.1310.10002 Research Article jmbEffects of Iron-Reducing Bacteria on Carbon Steel Corrosion Inducedby Thermophilic Sulfate-Reducing ConsortiaEduardo Valencia-Cantero1 and Juan José Peña-Cabriales2*

1Chemical and Biology Research Institute, Michoacan University of San Nicolas of Hidalgo (UMSNH), 58030 Michoacan, Mexico2Department of Biotechnology and Biochemistry, Center of Research and Advances Studies, 36500 Guanajuato, Mexico

Introduction

Microbe-influenced corrosion (MIC) is due to the presence

and activity of microorganisms, including bacteria and

fungi, and affects a wide range of industries, resulting in

severe economic losses [19]. Carbon steel, although susceptible

to corrosion, is frequently employed in industries and

infrastructure because of its strength, availability, relatively

low cost, and fire resistance [19]. Infrastructure affected by

MIC (e.g., buried pipelines) is often operated under anaerobic

or microaerobic conditions [20]. Most studies on anaerobic-

microaerobic MIC use sulfate-reducing bacteria (SRBs)

because they are sulfide producers and promoters of the

cathodic depolarization process in steel [14, 38]. According

to von Wolzogen and Van der Vlugt [36], under anaerobic

conditions, electrons from the metal surface (cathode)

reduce protons to form hydrogen, which forms a film that

prevents further proton reduction, thus producing electrostatic

isolation (passivation). Different bacteria that colonize the

metal surface can consume the hydrogen film, resulting in

Fe2+ release from the metal surface. Sulfide produced by

SRBs combines with Fe2+ to form ferrous sulfide and

generate an adhesive film. This mineral film acts as a cathode

for hydrogen evolution, thus increasing the corrosion rate

[16], but can also have a protective passivation effect

depending on the crystalline mineral composition [9, 11,

22]. The differences in SRB-related corrosive effects are also

caused, at least in part, by the SRB species themselves [26,

34], in addition to ambient factors.

Under microaerobic conditions, a protective mineral film

may be formed with ferric oxides. The dissolution of this

protective film by iron-reducing bacteria (IRBs) may result

in increased corrosion rates [10, 25]. SRBs and IRBs frequently

coexist in association with buried metallic structures [1,

20]. The corrosive effect of microbial cocultures (consortia)

composed of SRBs and IRBs is controversial [12]. It has

been suggested that ferrous ions derived from bacterial

ferric reduction may prevent formation of the protective

sulfide film [25], thus increasing corrosion rates, and that

bacterial consortia containing both bacterial types produce

higher corrosion rates than axenic cultures [33, 35];

however, other studies have shown that IRBs inhibit steel

Received: October 2, 2013

Revised: November 1, 2013

Accepted: November 5, 2013

First published online

November 13, 2013

*Corresponding author

Phone: +52-462-6239642;

Fax: +52-462-6239642;

E-mail: jpena@ira.cinvestav.mx

pISSN 1017-7825, eISSN 1738-8872

Copyright© 2014 by

The Korean Society for Microbiology

and Biotechnology

Four thermophilic bacterial species, including the iron-reducing bacterium Geobacillus sp. G2

and the sulfate-reducing bacterium Desulfotomaculum sp. SRB-M, were employed to integrate a

bacterial consortium. A second consortium was integrated with the same bacteria, except for

Geobacillus sp. G2. Carbon steel coupons were subjected to batch cultures of both consortia.

The corrosion induced by the complete consortium was 10 times higher than that induced by

the second consortium, and the ferrous ion concentration was consistently higher in iron-

reducing consortia. Scanning electronic microscopy analysis of the carbon steel surface

showed mineral films colonized by bacteria. The complete consortium caused profuse

fracturing of the mineral film, whereas the non-iron-reducing consortium did not generate

fractures. These data show that the iron-reducing activity of Geobacillus sp. G2 promotes

fracturing of mineral films, thereby increasing steel corrosion.

Keywords: Biocorrosion, thermophilic bacterial consortia, sulfate-reducing bacteria, iron-

reducing bacteria, protective mineral film

281 Valencia-Cantero and Peña-Cabriales

J. Microbiol. Biotechnol.

corrosion in a dual-species biofilm with SRBs [8, 21]. SRBs

and IRBs coexist in heterogeneous communities with

different bacterial populations that modify the metabolism

of the entire community [13, 39], thus likely modifying

their corrosive effect.

In natural environments, the reactions leading to steel

corrosion intensify with temperature [4], and high-temperature

environments are characterized by diverse bacterial communities

[32], many of which may have corrosive effects [2, 29]. In a

previous study with a microcosm approach [33], we

reconstructed different thermophilic bacterial consortia

and found that when IRBs and SRBs were cointegrated in a

consortium with Bacillus spp., they produced steel corrosion

rates 4.8 and 5.0 times higher than those of sterile controls.

Here, we provide evidence that, in bacterial consortia

containing IRBs-SRBs, IRBs produce high ferrous ion

concentrations that destabilize the mineral protective film

formed on the steel surface, thus increasing the corrosion

rate.

Materials and Methods

Bacteria Employed and Culture Conditions

We used the bacterial strains Bacillus sp. G2 (facultative anaerobic,

IRB) reclassified as Geobacillus sp. G2 by Nazina et al. [23], Bacillus

sp. G9a (facultative anaerobic, fermentative, slime forming), Bacillus

sp. G11 (strictly aerobic, growth-factor requiring), and Desulfotomaculum

sp. SRB-M (strictly anaerobic, hydrogen consuming, SRB) that

were isolated from two hot springs in central Mexico and

characterized as previously described [33]. The bacterial strains

were cultured in medium D2 (g/l): MgSO4·7H2O, 1.50; Fe(NH4)2(SO4)2,

0.10; glucose, 5.00; casein peptone, 5.00; meat extract, 3.00; yeast

extract, 0.20; pH 8; [3]; they were maintained by subculture in D2

agar plates (medium D2 plus agar, 20 g/l) at 55°C.

Analytical Techniques

The Fe2+ concentration in the cultures was determined by the

ferrozine assay [31]. The dissolved sulfide content was measured

in the culture media by the methylene blue method [6] with a

simple modification: to eliminate bacterial growth-related turbidity

interference, the samples were centrifuged and the supernatant

was assayed. The pH of the solution was measured using a

potentiometer. Oxygen in the culture medium was measured with

a dissolved oxygen meter.

Steel Corrosion by Bacterial Consortia

Carbon steel 1018 (AISI-SAE) coupons with an average area of

12.9 cm2 were used. The individual areas of the coupons were

estimated according to their density, weight, and geometry. Each

coupon was initially sterilized by immersion in 70% ethanol for

10 min; degreased in 100% ethanol for 15 min; and quickly dried

under ultraviolet light in a stream of warm, sterile air as a slight

modification of the method of Obuekwe et al. [24]; and then

placed in culture tubes (volume, 70 ml; 2.2 cm diameter × 20 cm

length) containing 35 ml of culture medium D2 and 35 ml of air.

At 55°C, the oxygen in the culture medium was of 28 µmol/l at

1 cm from the aerobic interface and 15 µmol/l at the bottom of the

tube (10 cm from the aerobic interface). The tubes were inoculated

with a sulfate- and iron-reducing consortium (SIRC) integrated by

overnight culture of 0.5 ml of Geobacillus sp. G2, Bacillus sp. G9a,

Bacillus sp. G11, and Desulfotomaculum sp. SRB-M, or they were

inoculated with a sulfate-reducing consortium (SRC) integrated

with the same bacteria except for the IRB Geobacillus sp. G2. In all

the experiments, non-inoculated tubes were included as sterile

controls. Tubes were incubated at 55°C for 3 or 25 days in a

microoxic environment. After incubation, the coupons were cleaned

using a slight modification of the method of Bryant et al. [5] in

which the coupons were sonicated in citric acid (5% (w/v)) for

5 min for remove the bio- and mineral film, and then rinsed in

distilled and deaerated water for 1 min. The coupons were flamed

and weighed. Corrosion was measured as weight loss divided by

the coupon area [33].

Scanning Electronic Microscopy

Carbon steel 1018 coupons with an average area of 2.4 cm2 were

degreased and experimentally oxidized in Petri dishes with distilled

water (depth, 2 mm), air drilled, ethanol-sterilized, and stored in

vacuum in hermetic vials. The other coupons were incubated

for 72 h in tubes with 35 ml of D2 medium inoculated with

Desulfotomaculum sp. SRB-M to produce a biogenic ferrous sulfide

film. Then, in an anaerobic chamber, the coupons were removed

from the tubes, submerged in 70% deaereated ethanol for 10 min,

drilled in absorbent paper under a N2 stream, and stored under

vacuum conditions. A third coupon group was not pretreated and

was only sterilized in 70% ethanol.

Coupons for the three treatments were incubated with cultures

of the SIRC or SRC, or in sterile D2 medium, for 3 or 25 days. After

the incubations, the coupons were removed and dehydrated in

increasing concentrations of 20%, 40%, 60%, 80%, and 100%

ethanol (in water (v/v)) for 5 min each. The coupons were stored

in vacuum for metalization with copper and were examined using

a scanning electronic microscope (JEOL JSM-6400) at 10 kV.

Results

Corrosion Experiments with Reconstructed Thermophilic

Bacterial Consortia

Carbon steel 1018 coupons were incubated in a sterile

medium, in SIRC cultures, or in SRC cultures. After 3 days

of incubation (short period), the steel coupons incubated in

sterile media showed corrosion of nearly 2.7 g/m2 (abiotic

corrosion), whereas the SIRC and SRC culture media showed

a slightly alkaline pH, with a ferrous ion concentration

Corrosive Effect of Iron-Reducing Bacteria 282

February 2014⎪Vol. 24⎪No. 2

(from steel dissolution) close to 1 mmol/l and a basal

sulfide concentration provided by the culture medium

(Table 1). Coupons incubated for 3 days in SRC cultures

did not show corrosion, as measured by weight loss, but

showed a slight increment in weight (0.05 g/m2), probably

because of mineral deposits on the metal surface. The

culture medium had a moderate acidic pH, the ferrous ion

levels were much lower (36 µmol/l) than those in the

abiotic controls, and the sulfide concentration was the

highest among all conditions in the entire experiment

(110 µmol/l). In contrast, coupons incubated in the SIRC

cultures showed the highest corrosion, almost two times

higher than that of the coupons incubated in sterile

medium. The culture medium of the SIRC had a pH nearly

identical to that of the SRC medium, but the ferrous ion

concentration was 10 times higher and the sulfide

concentration was 3.5 times lower (Table 1).

When the steel coupons were incubated for 25 days (long

period), similar results were obtained. Coupons incubated

in sterile media showed abiotic corrosion of 4.9 g/m2 with

a culture medium that had a slightly alkaline pH, but a

relatively low ferrous ion concentration (close to 1 mmol/l)

and a basal sulfide concentration. Coupons incubated with

the thermophilic consortia were also affected by the

presence or absence of the IRB Geobacillus sp. G2. The pH in

both consortia was close to neutral, but in the SRC culture

medium, the ferrous ion concentration was much lower

and the sulfide concentration was two times higher than

that in the SIRC medium. The formation of floccules of a

dark precipitate was very clearly seen at the bottom of the

culture tubes with SIRC. The difference in steel corrosion

was dramatic; the corrosion was 10-fold higher in coupons

incubated in SIRC relative to coupons incubated in SRC

(Table 1).

Examination of Carbon Steel Coupons by Scanning Electron

Microscopy

Carbon steel coupons were incubated for 3 or 25 days

under sterile conditions, in SIRC cultures, or in SRC cultures.

Some coupons were previously covered with an oxide or

biological sulfide film. After 3 days of incubation, steel

coupons incubated in sterile medium showed shallow pits

with limited extension and were essentially intact without

any mineral film (Fig. 1A). Coupons previously covered

with an oxide film and then incubated in sterile medium

showed an irregular dense mineral layer with numerous

edges (Fig. 1C) characteristic of iron oxides [24], whereas

coupons previously treated with biogenic sulfide and then

incubated in sterile medium showed a dense homogeneous

mineral layer with granular inclusions but without evident

cracks (Fig. 1F). A similar mineral layer was found in

coupons incubated with SIRC, regardless of whether they

were coated with a mineral layer (Fig. 1B) or had been

previously coated with an oxide (Fig. 1E) or sulfide layer

(Fig. 1H), although it is notable that cracks were apparent

with these three treatments. The mineral films were

colonized by bacteria. In contrast, coupons incubated in

SRC cultures showed dense mineral layers, without evident

cracks (Figs. 1D and 1G), and were colonized by fewer

bacteria than coupons exposed to SIRC.

When the steel coupons were incubated for 25 days, the

trend was the same as that at 3 days. However, all coupons

incubated in sterile media showed a similarly homogeneous

dense mineral film, regardless of whether they were pre-

Table 1. Comparison of parameters linked to corrosion of carbon steel incubated with SIRC or SRC.

After 3 days of incubationSteel corrosion

(g/m2)

Culture medium

pH Fe2+ concentration (µmol/l ) Sulfide concentration (µmol/l)

Sterile control 2.69 ± 0.24b 7.4 ± 0.0a 874 ± 99a 18 ± 8a

SRC -0.05 ± 0.11c 5.8 ± 0.1b 36 ± 14b 110 ± 61a

SIRC 4.80 ± 0.82a 5.7 ± 0.1b 654 ± 258b 31 ± 2a

After 25 days of incubation

Sterile control 4.92 ± 4.9b 7.4 ± 0.0a 1,207 ± 85b 7 ± 0b

SRC 1.24 ± 8.5c 6.3 ± 0.1b 66 ± 12b 72 ± 16b

SIRC 13.17 ± 10.5a 6.9 ± 0.3ab 4,028 ± 690a 30 ± 8a

Values shown represent the average of four replicates ± SE; letters are used to indicate that means on the same incubation day differ significantly by Duncan’s multiple

range test (p < 0.05).

283 Valencia-Cantero and Peña-Cabriales

J. Microbiol. Biotechnol.

coated with a mineral layer (Fig. 2A) or were pre-coated

with an oxide film (Fig. 2D) or a sulfide film (Fig. 2G).

Fig. 2G also shows the bacteria responsible for the

production of the biogenic sulfide film embedded in the

mineral layer; these bacteria were killed by flaming before

incubation in the sterile medium. The exposure of these

bacteria indicated weathering in the biogenic ferrous sulfide

film.

After 25 days of incubation with the thermophilic bacterial

consortia, a dense mineral film was found, and when the

coupons were incubated with SRC, the mineral film did not

show evident cracks (Figs. 2B and 2E), but when the coupons

were incubated with SIRC, the mineral film cracked

(Figs. 2C, 2F, and 2H). The width of the fractures increased

by 4-fold from 3 to 25 days, and the cracks were colonized

by bacteria (Figs. 2F and 2H).

Discussion

MIC of steel is a complex phenomenon that involves diverse

factors such as oxygen concentration (aerobic, microaerobic,

or anaerobic conditions), the environment (temperature,

pH, and nutrients), the groups of microorganisms (species,

physiological factors, and ecological factors) [26, 34], and

the particularities of steel itself. Because of this complexity,

generalizing the data available in the literature has been

difficult. Rodin et al. [28] previously showed that diverse

bacterial consortia that include SRBs have a corrosive or

protective effect on steel according to theculture conditions.

Various studies have shown that IRBs—in combination

with SRBs—have a protective effect on steel [8, 21], but

other studies have shown that IRBs enhance the corrosive

effect of SRBs [33, 35]. In the present study, we found that

addition of the IRB Geobacillus sp. G2 reversed the protective

effect of an SRC against steel corrosion.

Fig. 1. Overall appearance of the surface of carbon steel

coupons subjected to incubation at 55°C for 3 days and then

recovered.

Clean coupon incubated in (A) sterile culture medium or (B) SIRC

culture. Coupons covered with ferric oxide and incubated in (C)

sterile culture medium, (D) SRC culture, or (E) SIRC culture. Coupons

covered with biogenic ferrous sulfide and incubated in (F) sterile

culture medium, (G) SRC culture, or (H) SIRC culture. All

micrographs were obtained with a magnification of 5,000×.

Fig. 2. Overall appearance of the surface of carbon steel

coupons subjected to incubation at 55°C for 25 days and then

recovered.

Clean coupon incubated in (A) sterile culture medium, (B) SRC

culture, or (C) SIRC culture. Coupons covered with ferric oxide and

incubated in (D) sterile culture medium, (E) SRC culture, or (F) SIRC

culture. Coupons covered with biogenic ferrous sulfide and incubated

in (G) sterile culture medium or (H) SIRC culture. All micrographs

were obtained with a magnification of 5,000×.

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February 2014⎪Vol. 24⎪No. 2

The protective effect of the SRC was observed at both

short (3 days) and long (25 days) incubation times, but at

both time points, the pH was not the most important factor

whenever both consortia contained the fermenting bacterium

G9a, which produced the same pH in the respective media.

Fe2+ levels were much higher in SIRC cultures than in SRC

cultures. At the short incubation time, the sterile controls

had an Fe2+ concentration similar to that observed for SIRC,

but in our microaerobic system, it is expected that the Fe2+

can be re-oxidized; therefore, at the long incubation time,

the Fe2+ level in SIRC cultures was 3-fold higher than that

in sterile controls and 60-fold higher than that in SRC

cultures (Table 1), probably because of the iron-reducing

activity of Geobacillus sp. G2. Additionally, the higher Fe2+

concentration in SIRC cultures probably caused two other

observed effects: (i) lower sulfide concentration in SIRC

than in SRC cultures resulting from the formation of

ferrous sulfide floccules and (ii) increased steel corrosion

by SIRC compared with SRC (Fig. 3).

Sulfide is corrosive [18], but at low concentrations, it

reacts with the steel surface and produces a protective

film of ferrous sulfide crystallized as mackinawite [30]; in

our system, the maximum concentration of sulfide was

110 µmol/l, which was lower than the level in other systems

[18, 21] and may thus have caused the protective effect in

SRC [9, 33, 37]. King et al. [15, 17] previously showed that

in SRB cultures with a high ferrous concentration, the

breakdown of the mackinawite protective film by transformation

into other less-adhesive sulfide conferred less protection to

the underlying metal. It is therefore not surprising that

SIRC showed the highest steel corrosion in the present

study.

To evaluate the mineral film in different cultures, steel

coupons covered with an oxide film, a biogenic sulfide

film, or not covered were included in the two consortium

cultures (Figs. 1 and 2). Steel coupons in these cultures

presented a dense mineral film. Given that coupons pre-

covered with oxide appeared similar to coupons biogenically

covered with a sulfide film, it is possible that a secondary

mineral film of ferrous sulfide covered the surface. Steel

coupons incubated in SIRC cultures were extensively

fractured, regardless of whether the steel surfaces were

pre-coated, whereas SRC cultures did not show such

fractures. Over time, the fractures became wider and

reached a thickness of nearly 1 µm. Thus, the integrity and

fracture condition of the mineral film correlated with the

protective and corrosive effects of the SRC and SIRC,

respectively. This finding suggests that, in SIRC cultures,

the mineral film was transformed to a poorly adhesive

sulfide material with poor integrity and without protective

characteristics. A fractured mineral film permits diffusion

of ferrous ions from the corroded steel surface to the

Fig. 3. Schematic diagram of the proposed reaction mechanism

for acceleration of steel corrosion by IRBs in the presence of

SRBs.

The diagram shows a steel surface submerged in a medium in the

presence of SRBs (A) or in the presence of SRBs and IRBs (B), under

microaerobic conditions. Anaerobe facultative bacteria (not schematized)

that consume oxygen from an aerobic interface maintain microaerobic

conditions. Ferrous ions obtained from steel dissolution are oxidized

to ferric ions at the aerobic interface, which are precipitated or

produce ferric hydroxides on the metal surface. SRBs oxidize H2 from

the steel or from the glucose in the medium and reduce sulfate to

produce sulfide. At low ferrous ion concentrations (A), sulfide reacts

with the steel surface and produces a protective film of ferrous sulfide

crystallized as mackinawite. The protective sulfide film isolates the

steel surface from the protons present in the medium and limits

ferrous ion diffusion, thereby inhibiting steel corrosion. In the

presence of IRBs (B), ferric ions are reduced by IRBs, leading to the

accumulation of ferrous ions in the medium; sulfide reacts with these

ferrous ions from the medium to produces poorly adhesive ferrous

sulfide floccules. These floccules form a film that is easily fractured

and allows the interaction of protons from the medium with the steel

surface; new H2 evolution; and ferrous ion diffusion, all of which

enhance steel corrosion.

285 Valencia-Cantero and Peña-Cabriales

J. Microbiol. Biotechnol.

medium and facilitates the diffusion of aggressive species

such as sulfides to the steel surface for new corrosion

cycles. Dong et al. [7] proposed that transformed ferrous

sulfide minerals are conductive and undergo cathodic

depolarization; therefore, a porous layer of these minerals

also results in a large specific surface area composed of

porous films. A similar effect can be expected on fractured

sulfide film.

IRBs have been found to be protective against corrosion

when added to SRB-containing environments, probably by

depleting oxygen and biocompetitively excluding SRBs

[27]. The present study showed that (i) under microaerobic

conditions where ferrous ions can potentially accumulate,

with a low sulfide ion concentration, IRB addition to a

consortium of SRBs and fermentative bacteria increases

steel corrosion, possibly through destabilization of the

protective sulfide film, and (ii) that IRBs must be taken into

account in MIC diagnosis.

Acknowledgments

We thank the Coordinación de la Investigación Científica-

Universidad Michoacana de San Nicolás de Hidalgo (Grant

2.22) for financial support. The EVC PhD Scholarship

128343 was from Consejo Nacional de Ciencia y Tecnología,

México.

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