Bioelectrochemistry 113 (2017) 1–8

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Bioelectrochemistry

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Short communication

Accelerated corrosion of 2205 duplex stainless steel caused by marine

aerobic Pseudomonas aeruginosa biofilm
Dake Xu a,b, Jin Xia c, Enze Zhou d, Dawei Zhang a,⁎, Huabing Li d, Chunguang Yang b,⁎, Qi Li c, Hai Lin a,
Xiaogang Li a, Ke Yang b
a
Corrosion and Protection Centre, University of Science and Technology Beijing, Beijing 100083, PR China
b
Institute of Metal Research, China Academy of Science, Shenyang, 110016, PR China
c
Department of Chemistry, Liaoning University, Shenyang, 110036, PR China
d
School of Metallurgy, Northeastern University, Shenyang, 110819, PR China

a r t i c l e i n f o a b s t r a c t

Article history: Microbiologically influenced corrosion (MIC) of 2205 duplex stainless steel (DSS) in the presence of Pseudomonas
Received 14 April 2016 aeruginosa was investigated through electrochemical and surface analyses. The electrochemical results showed
Received in revised form 2 August 2016 that P. aeruginosa significantly reduced the corrosion resistance of 2205 DSS. Confocal laser scanning microscopy
Accepted 15 August 2016
(CLSM) images showed that the depths of the largest pits on 2205 DSS with and without P. aeruginosa were 14.0
Available online 22 August 2016
and 4.9 μm, respectively, indicating that the pitting corrosion was accelerated by P. aeruginosa. X-ray photoelec-
Keywords:
tron spectroscopy (XPS) results revealed that CrO3 and CrN formed on the 2205 DSS surface in the presence of
2205 duplex stainless steel P. aeruginosa.
Microbiologically influenced corrosion © 2016 Elsevier B.V. All rights reserved.
Pitting
Biofilm
Pseudomonas aeruginosa

1. Introduction
Duplex stainless steels (DSSs) are widely applied in the petroleum
industry and maritime development, where austenitic stainless steel
cannot fully satisfy the environmental requirements [1,2]. DSS exhibits
a good combination of characteristics, including a favourable mechani-
cal strength from the ferrite (α) phase and a high corrosion resistance
from the austenite (γ) phase [3–5]. The high content of chromium, nick-
el and molybdenum in these alloys would easily lead to formation of a
dense passivation film that can inhibit the permeation of aggressive
ions such as chloride [6,7]. While DSS possesses a high pitting resistance
equivalent number (PREN) that always exceeds 35 [8], the pitting of DSS
due to microbiologically influenced corrosion (MIC) has been previous-
ly reported [6,9,10]. The amount of global corrosion cost is over 4 trillion
dollars, and MIC accounts for 20% or more [11,12].
Pseudomonas aeruginosa, a rod-shaped and Gram-negative bacteri-
um, is well known to metabolise alkenes in fuels for growth. This bacte-
rium possesses two alkane hydroxylases (alkB1 and alkB2), cytochrome
P450 and other essential electron transfer proteins that enable it to
metabolise medium and long normal alkanes [13]. Moritz et al. [14] re-
ported that P. aeruginosa was versatile and ubiquitous in drinking water
and oil systems. A number of studies have confirmed that Pseudomonas
species are involved in the corrosion process of mild steel, stainless steel
and aluminium in marine habitats [15,16]. It is generally acknowledged
that the aerobic P. aeruginosa is the pioneer coloniser in the process of
biofilm formation. They can produce oxygen-free areas for the survival
of sulphate-reducing bacteria (SRB), thereby creating oxygen concen-
tration cells [16,17]. Busalmen [18] and Coumet et al. [19] found that ca-
thodic oxygen reduction is also accelerated owing to the catalysis by
P. aeruginosa.
The present study seeks to gain a better understanding of the influ-
ence of marine P. aeruginosa bacterium on the corrosion behavior of
2205 DSS. In electrochemical studies, linear polarisation resistance
(LPR) measurement and electrochemical impedance spectroscopy
(EIS) were performed to evaluate the corrosion behaviors of 2205 DSS
immersed in media with and without P. aeruginosa inoculation. The sur-
face morphology was assessed by scanning electron microscopy (SEM),
and the pit depths were measured by confocal laser scanning microsco-
py (CLSM). The corrosion products were analysed by X-ray photoelec-
tron spectroscopy (XPS).
2. Materials and methods
2.1. Materials

⁎ Corresponding authors. 2205 DSS was purchased from Taiyuan Iron & Steel (Group) Co., Ltd.,
E-mail addresses: dzhang@ustb.edu.cn (D. Zhang), cgyang@imr.ac.cn (C. Yang). Taiyuan, Shanxi, China. Its chemical composition (wt%) was analysed,

http://dx.doi.org/10.1016/j.bioelechem.2016.08.001
1567-5394/© 2016 Elsevier B.V. All rights reserved.
2 D. Xu et al. / Bioelectrochemistry 113 (2017) 1–8

and is given in Table 1. All of the specimens were sequentially abraded 2.4. XPS analysis
with silicon carbide papers of 150, 240, 400, 600, 800 and 1000 grit,
rinsed with sterile distilled water, and then degreased with ethanol. For the XPS analysis, the specimens were quickly removed from the
Each specimen was sterilised in 75% ethanol solution for 2 h and was ex- vials and gently rinsed three times with deionised water. After blow-
posed to UV light for 30 min prior to uses. Specimens with dimensions drying with pure nitrogen, the specimens were stored in an air-tight
of 10 mm × 10 mm × 5 mm were used for electrochemical measure- vacuum desiccator prior to use.
ments and surface analysis. XPS measurements were performed via an ESCALAB250 spectrome-
In this study, P. aeruginosa MCCC 1A00099 was obtained from the ter (Thermo VG, Massachusetts, USA) with a monochromatic X-ray
Marine Culture Collection of China (MCCC), Xiamen, China. The 2216E source (an Al kα electrode at 15 kV and 150 W). The pass energy of
medium was used to simulate a nutritious seawater environment. The the spectra within the range of 0–1350 eV and high-resolution spectra
medium consisted of the following components: Na2SO4, 1.8 g/L CaCl2, were recorded using a passing energy of 50 eV and a step of 0.1 eV. To
0.55 g/L KCl, 0.16 g/L Na2CO3, 0.08 g/L KBr, 0.034 g/L SrCl2, 0.08 g/L compensate for the surface charging effect, all core-level spectra were
SrBr2, 0.022 g/L H3BO3, 0.004 g/L NaSiO3, 0.0024 g/L NaF, 0.0016 g/L referenced to the C 1 s hydrocarbon peak at 284.6 eV.
NH4NO3, 0.008 g/L NaH2PO4, 5.0 g/L peptone, 1.0 g/L yeast extract and
0.1 g/L ferric citrate. The pH of the medium was adjusted to 7.2 ± 0.2, 3. Results and discussion
and the medium was sterilised by autoclaving at 121 °C for 15 min.
The initial cell concentration was approximately 106 cells mL−1, as mea- 3.1. LPR results
sured by a haemocytometer under a light microscope.
LPR is considered to be a rapid and efficient method which reflects
the transient electrochemical process and can therefore be used to de-
2.2. Electrochemical measurements termine corrosion rates [28]. The variations in polarisation resistance
(Rp) of 2205 DSS in the presence of P. aeruginosa and in sterile medium
To prepare the working electrodes, the 2205 DSS specimens were are shown in Fig. 1(a). The Rp value of 2205 DSS in sterile medium in-
connected with copper wire and mounted in epoxy resin, leaving an ex- creased dramatically from ~ 200 to ~1000 kΩ cm2 after only 3 days of
posed area of 1 cm2. The specimen surfaces were abraded and sterilised exposure. The value then gradually decreased and reached
as described above. Subsequently, they were soaked in 2216E sterile ~ 800 kΩ cm2 after 14 days, confirming the excellent corrosion resis-
and P. aeruginosa inoculated medium at 37 °C for up to 14 days. Electro- tance of 2205 DSS in 2216E medium. However, in the presence of
chemical studies were conducted at 37 °C in 2216E medium using an P. aeruginosa, the Rp value was much smaller at 3 to 10 days compared
Autolab potentiostat-galvanostat (Reference 600, Gamry, Warminster,
PA, USA). A saturated calomel electrode (SCE) and a platinum plate
(10 mm × 10 mm × 1 mm) were used as the reference electrode and
the counter electrode, respectively. LPR measurements was conducted
at a scan rate of 0.125 mV s−1 over the range of − 5 to 5 mV versus
the EOCP, with a sampling period of 1 s. EIS was performed under EOCP
using a 5 mV amplitude sinusoidal signal over the frequency range of
0.01 to 10,000 Hz. The glass cell for electrochemical tests was sterilised
in the autoclave. The electrodes were sterilised by 75% alcohol, and then
exposed under UV for 45 min. The whole setup was finally sealed with
parafilm to prevent potential contamination. The successful disinfection
has avoided the appearance of the flocs in this study. To obtain precise
results and good repeatability, each experiment was conducted three
times with triplicate coupons. Spent medium or killed bacterial system
control was not used in this study because the outcome of similar re-
search has been well established as reported in the literature [20–25].

2.3. Surface morphology

To observe the P. aeruginosa biofilm on the 2205 DSS surface, the

specimens were fixed and dehydrated following procedures reported
in the literature [26]. The specimens were sputter-coated with gold
and were then observed by SEM (SU8010 model, Hitachi, Tokyo, Japan).
The biofilm was then removed according to the Chinese national
standard GB/T4334.4-2000 [27]. The largest pit depth was measured
using a Zeiss CLSM (LSM 710, Zeiss, Jena, Germany). In the CLSM mea-
surements, the entire sample surface was first scanned at a low resolu-
tion to confirm the location with the deepest pits, which were
subsequently examined at a higher resolution to produce a detailed
depth profile. The average pit depth was obtained by measurements
taken at 10 different locations for each specimen.

Table 1
Chemical composition of 2205 DSS (wt%).

Element Si Mn P S Ni Cr Mo N Fe
Fig. 1. Variation in Rp (a) and icorr (b) in sterile and P. aeruginosa inoculated medium
DSS (wt%) 0.51 1.14 0.03 b0.001 5.89 23.22 3.10 0.17 Balance
( sterile; innoculated).
 D. Xu et al. / Bioelectrochemistry 113 (2017) 1–8 3

Fig. 2. Nyquist and Bode plots obtained for 2205 DSS in sterile medium (a, a′) and P. aeruginosa inoculated medium (b, b′) (■ 1 day; 3 days; 7 days; 14 days).

Passive film
Cf
a Rs

Rf

b
Passive film Biofilm
Cb

RS
Cdl

Rb
Rct

Rs: resistance of solution; Cf: capacitance of passive film; Rf: resistance of passive film;
Cb: capacitance of biofilm; Rb: resistance of biofilm; Cdl: capacitance of EDL; Rs: resistance of EDL

Schematic 1. Physical models and equivalent electrical circuits simulating the EIS diagrams based on a (a) single- and (b) double-layer model with a biofilm.
4 D. Xu et al. / Bioelectrochemistry 113 (2017) 1–8

Table 2 by a single impedance loop that increased slightly in diameter with in-
Fitting parameters of the impedance spectra of 2205 DSS in sterile and P. aeruginosa inoc- oculation time. In Fig. 2(a′), the Bode plots exhibit only one time con-
ulated medium.
stant. The corresponding physical model and equivalent circuit are
Sample
Rs (Ω Cf (F Rf (Ω Cb (F Rb (Ω Cdl (F Rct (Ω shown in Schematic 1(a) [30]. Fig. 2(b) and (b′) shows the impedance
cm2) cm−2) cm2) cm−2) cm2) cm−2) cm2) spectra of the 2205 DSS in the P. aeruginosa inoculated medium. The di-
2205 DSS in the sterile medium ameters of the impedance loops in the Nyquist plots (Fig. 2(b)) de-
1 day 12.15 2.779E-5 1.109E5 – – – – creased within the first 3 days and then markedly increased. In the
3 day 23.85 1.864E-5 1.312E5 – – – –
phase plots (Fig. 2(b′)), two peaks emerged with time. The peak located
7 day 15.60 2.172E-5 3.447E5 – – – –
14 day 14.54 1.429E-5 2.868E5 – – – – at the higher frequency was most likely due to the biofilm, while the
peak at the lower frequency can be attributed to the electrical double
2205 DSS in the presence of P. aeruginosa
layer (EDL) [15]. The maximum phase angles in the lower frequency
1 day 7.59 – – 1.933E-5 523.2 2.983E-5 5.105E4
3 day 7.17 – – 1.725E-7 443.9 2.860E-5 4.392E4 range decreased from ~ 70° to ~30° after 3 days of exposure, followed
7 day 13.46 – – 7.179E-6 376.2 2.304E-5 2.027E5 by a gradual increase back to ~ 70° after 14 days. Schematic
14 day 9.42 – – 5.764E-6 340.7 2.501E-5 4.791E5 1(b) shows the corresponding physical model and equivalent circuit
[6,31].
The fitted parameters obtained from the EIS results are listed in
to that in the sterile medium, indicating a lower corrosion resistance. Table 2. The Chi-square (χ2) values were all b 10− 3, demonstrating
After 11 days, the Rp reached a constant value of ~900 kΩ cm2. The cor- the high quality of the fitting. In the presence of P. aeruginosa, the
rosion current density (icorr) was calculated from Rp based on the Stern- charge transfer resistance (Rct) decreased from 5.105 × 104 to
Geary equation, assuming B to be 26 mV−1. This simplification is appro- 4.392 × 104 Ω cm2 after 3 days; these values are approximately one
priate because icorr is relatively insensitive to the Tafel slope [28]. As order of magnitude lower than the Rf values observed in the sterile
shown in Fig. 1, the icorr value of 2205 DSS in the P. aeruginosa inoculated medium, further demonstrating that P. aeruginosa accelerated the cor-
medium was much higher than that in the sterile medium, also rosion. However, continued inoculation resulted in a gradual increase
confirming the accelerated corrosion of 2205 DSS in the presence of in Rct to 4.791 × 104 Ω cm2 after 14 days.
P. aeruginosa. However, after 10 days of exposure, the Rp and icorr
changed to values similar to those obtained in the sterile medium.
3.3. Surface topography
3.2. EIS results
Fig. 3 shows the SEM images of 2205 DSS after inoculation with
EIS is a non-destructive technique that has been frequently used to P. aeruginosa for 7 and 14 days. Evenly distributed sessile P. aeruginosa
study electrochemical reactions at metal/biofilm interfaces and the for- cells can be observed on the surface of 2205 DSS after 7 days of exposure
mation of corrosion products and biofilms in MIC [15,29]. Typical im- (Fig. 3(a, b)). By contrast, the P. aeruginosa biofilm became aggregated,
pedance spectra of 2205 DSS in sterile medium are shown in and the quantity of sessile cells was reduced after 14 days (Fig. 3(c,
Fig. 2(a) and (a′). The Nyquist plot shown in Fig. 2(a) is characterised d)). It is noteworthy that at this stage, most bacteria existed in the

Fig. 3. SEM images of 2205 DSS exposed to P. aeruginosa inoculated medium for (a, b) 7 days and (c, d) 14 days.
 D. Xu et al. / Bioelectrochemistry 113 (2017) 1–8 5

Fig. 4. CLSM 3-D images of 2205 DSS surfaces exposed to sterile (a) and P. aeruginosa inoculated media (b) for 14 days.

form of bacterial clusters, and only very few scattered sessile cells could
be found.
After the biofilm was removed, the pits on the 2205 DSS surfaces
that were exposed to sterile and P. aeruginosa inoculated medium for
14 days were examined by CLSM. CLSM 3-D images of their pitting cor-
rosion morphologies are presented in Fig. 4(a) and (b). The largest pit
depth on the 2205 DSS surface in the sterile medium was 4.9 μm, with
a surface diameter of 6.3 μm. The P. aeruginosa biofilm significantly ac-
celerated the pitting corrosion of the 2205 DSS surface. The largest pit
was 14.0 μm in depth, with a surface diameter of 18.7 μm. The average
Table 3
Pit depths of 2205 DSS after inoculation in sterile and P. aeruginosa inoculated medium for
14 days.
Condition Sterile
Largest pit depth (μm) 4.9
Average pit depth (μm) 3.9 ± 1.3
pit depths on the specimens exposed to sterile and P. aeruginosa inocu-
lated medium were 3.9 ± 1.3 and 11.6 ± 2.2 μm, respectively (Table 3).
3.4. Surface chemical analysis
Fig. 5(a) shows wide-scan XPS results for the 2205 DSS surfaces after
14 days of immersion in sterile and P. aeruginosa inoculated media. The
RACE (relative atomic concentrations of elements) values of the sur-
faces are summarised in Table 4. C and O were the primary constituent
elements of the surface, comprising ~ 90% for both the specimens ex-
posed to the sterile medium and to the P. aeruginosa inoculated medi-
um. However, it is noteworthy that the RACE values of Cr and Fe for
the specimen in the inoculated medium were several times higher
than those in the sterile medium.
Fig. 5(b) and (c) show high-resolution 2p3/2 spectra for the 2205 DSS
Inoculated
surface after 14 days of immersion in sterile and P. aeruginosa inoculated
14.0 media, respectively. The spectrum for Cr 2p3/2 presented in Fig. 5(b) can
11.6 ± 2.2
be fitted into three main peaks, corresponding to Cr, Cr2O3, and Cr3+ on
6 D. Xu et al. / Bioelectrochemistry 113 (2017) 1–8

Table 4
RACE of 2205 DSS surfaces after soaking in sterile and P. aeruginosa inoculated medium for
14 days.

Atomic concentration (%)

Samples
Cl C N O Cr Mn Fe Ni

Sterile 2.12 67.68 6.11 23.62 0.26 – 0.21 –

Inoculated 1.08 56.80 5.43 33.21 1.36 0.15 1.80 0.17

medium, observed at the binding energies of 578.3 eV and 575.3 eV,

respectively.
In the presence of P. aeruginosa, the pH only changed slightly from
7.9 to 8.1 after 14 days, indicating that the accelerated pitting corrosion
was not caused by organic or inorganic acids secreted by P. aeruginosa.
In this study, the appearance of CrO3 in the P. aeruginosa inoculated me-
dium suggests that the removal of Cr from the 2205 DSS surface was ac-
celerated by the P. aeruginosa biofilm because CrO3 is soluble in water
[34]. P. aeruginosa may catalyze the oxidation of Cr to CrO3, resulting
in a more severe dissolution of 2205 DSS and accelerating pitting under-
neath the biofilm. Similar bacterial activity has been previously reported
for sulphate-reducing bacteria (SRB) which was shown to be conducive
to Cr6+ formation and therefore led to degradation of the passive film of
the 2205 DSS [35]. In addition to the formation of Cr6+, another influ-
ence of P. aeruginosa was the presence of CrN, which can give rise to
chromium-depleted regions, thereby decreasing the corrosion resis-
tance [36]. The biofilm of P. aeruginosa may reduce the activation energy
and enhance the kinetics of the reactions to form Cr6+ and CrN, which is
detrimental to the passive film and leads to the acceleration of pitting
corrosion of the 2205 DSS [37].
According to Zhang et al., electron shuttles such as FAD and ribofla-
vin were capable of accelerating the MIC process caused by SRB [38].
Electron shuttles carried the electrons released from the metal matrix,
and transferred these electrons to the membrane bound proteins such
as cytochrome, which assisted these electrons to enter the cytoplasm
where the reduction reactions occurred to produce energy. It has been
reported that P. aeruginosa can secrete pyocyanin (PYO), a water soluble
electron shuttle, and possess electron transfer proteins like cytochrome
[13,39,40]. Schematic 2 illustrates the possible MIC mechanism of 2205
DSS in the presence of P. aeruginosa. The secretion of PYO by
P. aeruginosa may accelerate the electron transfer between the metal
matrix and the sessile P. aeruginosa, resulting in the severe MIC pitting.
The improved electron transfer efficiency by PYO may reasonably ex-
plain that P. aeruginosa can catalyze the cathodic oxygen reduction reac-
tion [18,19].

Fig. 5. Wide-scan XPS spectra (a) and high-resolution XPS spectra observed for the surface
of 2205 DSS exposed to sterile (b) and P. aeruginosa inoculated (c) medium for 14 days.

the surface of the specimen exposed to the sterile medium [32,33]. The
primary difference between Fig. 5(b) and (c) is the presence of CrO3 Schematic 2. Schematic illustration of the MIC mechanism of 2205 Cu-DSS in the presence
(Cr6 +) and CrN on the specimen from the P. aeruginosa inoculated of P. aeruginosa.
 D. Xu et al. / Bioelectrochemistry 113 (2017) 1–8
4. Conclusion
This study focused on the MIC behavior of 2205 DSS caused by the
marine aerobic P. aeruginosa biofilms. The results of electrochemical
analyses (LPR and EIS) and pit depth measurements all supported that
2205 DSS was susceptible to an accelerated pitting corrosion in the pres-
ence of P. aeruginosa biofilms. After incubation with P. aeruginosa, the
XPS analysis revealed that CrN and a soluble compound of CrO3 were
formed on the surface of 2205 DSS, attributing to the accelerated disso-
lution of the passive film. The mechanisms behind the CrN and CrO3 for-
mation and the accelerated pitting corrosion are still unclear. Further
study is required to investigate the role of P. aeruginosa biofilm in pitting
initiation, the growth of the stable pits and its extracellular electron
transfer pathways.
Acknowledgments
This work was financially supported by the National Natural Science
Foundation (No. 51501203), the National Basic Research Program of
China (973 Program No. 2014CB643300), the National Environmental
Corrosion Platform (NECP), and the “Young Merit Scholars” program
of the Institute of Metal Research, Chinese Academy of Sciences.
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Dake Xu is currently an associate professor in the Institute of Metal Research of Chinese
Academy of Sciences. He received his PhD degree in Chemical Engineering from Ohio Uni-
versity in 2013. His PhD dissertation work was in the area of MIC and its mitigation. He has
published more than 30 journal articles.
Jin Xia is a master student in Department of Chemistry, Liaoning University, Shenyang,
China. His current research includes MIC and anti-MIC stainless steel.
Enze Zhou is a master student in the School of Metallurgy of Northeastern University,
Shenyang, China. His research interest is MIC of stainless steel.
Dawei Zhang is currently a professor at the Corrosion & Protection Center of University of
Science and Technology Beijing. He obtained his PhD in Materials Science and Engineering
from Texas A&M University in 2013. His main research focuses are biomaterials and corro-
sion.
Huabing Li is an associate professor in the School of Metallurgy of Northeastern Universi-
ty, Shenyang, China.
8 D. Xu et al. / Bioelectrochemistry 113 (2017) 1–8
Chunguang Yang is an associate professor in the Institute of Metal Research, Chinese
Academy of Sciences. He received the PhD in Ferrous Metallurgy from Northeastern Uni-
versity in 2009. His main research interests focus on mechanical property and corrosion
property of antibacterial stainless steel.
Qi Li is an associate professor in Department of Chemistry, Liaoning University, Shenyang,
China.
Hai Lin is a professor at school of Civil and Environment Engineering, University of Science
and Technology Beijing, Beijing, China.
Xiaogang Li is a professor at the Corrosion & Protection Center of University of Science and
Technology Beijing and also the Principal Scientist of the National Basic Research Program
of China (973 Program) in marine corrosion. His main research interests are corrosion and
its control in natural environments.
Ke Yang received his PhD degree in Materials Science from the Institute of Metal Research,
Chinese Academy of Sciences in 1989. He was awarded a Royal Society Fellowship and
worked in the Department of Materials, University of Oxford, UK between 1991 and 1993.
He is currently a full professor in the Institute of Metal Research, Chinese Academy of Sci-
ences. His research interests focus on novel materials including antimicrobial stainless steels.