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: [email protected]
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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