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Vol. 8. Issue 5.
Pages 4066-4078 (September - October 2019)
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Vol. 8. Issue 5.
Pages 4066-4078 (September - October 2019)
Original Article
DOI: 10.1016/j.jmrt.2019.07.016
Open Access
Mechanism of microbiologically influenced corrosion of X65 steel in seawater containing sulfate-reducing bacteria and iron-oxidizing bacteria
Meiying Lv, Min Du
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Corresponding author.
, Xia Li, Yongyong Yue, Xuchao Chen
The Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, College of Chemistry and Chemical Engineering, Ocean University of China, Qingdao 266100, P.R. China
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Figures (13)
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Tables (4)
Table 1. The cell counts of sessile SRB and IOB (CFU/cm2) in the biofilm at different culture times.
Table 2. EIS fitting results of X65 steel specimens in different media based on the equivalent circuit in Fig. 10.
Table 3. Tafel parameters of X65 steel specimens after 7 days and 21 days exposure in sterile medium and mixed SRB + IOB media.
Table 4. Fitting parameters for C 1s, O 1s and Fe 2p XPS spectra and the relative quantity of compounds in the corrosion products.
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Sulfate-reducing bacteria (SRB) and iron-oxidizing bacteria (IOB) are one of the typical representatives of anaerobic and aerobic bacteria, which can form a synergistic community (mixed species biofilm) on the surface of material. In this work, the corrosion behavior of X65 steel in seawater containing SRB and IOB was investigated with electrochemical impedance spectroscopy, potentiodynamic polarization, scanning electron microscopy, energy dispersive spectroscopy and X-ray photoelectron spectroscopy. Results showed that the combination of anaerobic SRB and aerobic IOB affected the corrosion behavior of X65 steel greatly, and the corrosion rate was higher than that in single SRB or IOB medium. The corrosion mechanisms of X65 steel in mixed SRB and IOB could be divided into three stages, which were controlled by the metabolic activities of bacteria (SRB and IOB), biofilm structure and metabolic products comprehensively.

Sulfate-reducing bacteria
Iron-oxidizing bacteria
Microbiologically influenced corrosion
Metabolic products
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Corrosion is a world-wide problem that results in tremendous economic consequences to various industries. It is estimated that the cost of corrosion is equivalent to about 1%–4% of the gross national product (GNP) of developed countries [1]. In the marine environment, steels are widely used for offshore oil and gas fields, transportation pipelines, desalination facilities, ship equipment and so on. Marine corrosion is mitigated through measures such as paint, coatings or cathodic protection [2]. Nevertheless, it is still a ubiquitous problem. A significant amount of corrosion is initiated and/or aggravated by microorganisms, a process commonly referred to as “microbiologically influenced corrosion” (MIC) [3]. MIC can take place on almost any metallic surface exposed to non-sterile systems, which is usually associated with metallic dissolution and loss of mechanical properties induced by the direct or indirect activities of microbiological organisms. Several bacteria are implicated in MIC such as sulfate-reducing bacteria (SRB) [4], nitrate-reducing bacteria [5], methanogenic bacteria [6], acid-producing bacteria [7], iron-reducing bacteria [8], iron-oxidizing bacteria (IOB) [9] and sulfur-oxidizing bacteria [10], etc. These microorganisms and their metabolic products, as well as extracellular polymeric substances, can form a biofilm layer that affects the kinetics of cathodic and/or anodic reactions [4]. Moreover, their metabolic activities can facilitate the formation of a wide variety of sites on the biofilm/metal interface that are chemically and physically markedly different from other neighboring sites, leading to accelerate or mitigate the corrosion process of metals [11,12].

SRB are commonly considered the main culprits associated with anaerobic MIC due to the wide availability of sulfate (SO42−) in the aquatic environment (e.g., marine) [13,14]. SRB typically use SO42− as the terminal electron acceptor for energy generation in their metabolism, which indirectly contributes to the accumulation of corrosive sulfide and organic acid end-products causing localized pitting of metals [15]. Numerous mechanisms have been proposed for MIC by SRB, including but not limited to cathodic depolarization [16], local corrosive cell [17], metabolites induced corrosion [18]. The cathodic depolarization theory has been widely accepted by numerous publications, which emphasizes the bacteria’s role in MIC, involving electron transport from the cathodic areas on the steel surface to the SO42− reduction process through a hydrogen intermediate (i.e. hydrogenase) to increase the cathodic current [19,20]. The metal sulfide by the activity of SRB stimulate localized corrosion by establishing the sulfide/metal galvanic couple, even in the absence of hydrogen sulfide, which forms the foundation of the galvanic cell theory [17]. More recently, extracellular electron transfer (EET) theory offers better understanding for the study of metal–microbe interactions [21,22]. It is possible that electrons may be transferred from outside the cell to the cytoplasm inside the cell by crossing the cell wall, leading to more severe corrosion [23].

IOB or so-called metal-depositing microorganisms are commonly referred as causing MIC [24–26]. In an aerobic environment, IOB can deposit iron hydroxides (e.g., Fe(OH)3, FeOOH, Fe2O3) at the extracellular and induce different types of steel corrosion, especially pitting corrosion [27,28]. They generate energy for growth by oxidation of ferrous ions (Fe2+) to ferric ions (Fe3+) with oxygen (O2) as the terminal electron acceptor, that afterward precipitate as ferric hydroxide [29]. Sudek et al. [30] isolated a number of aerobic heterotrophic IOB that oxidized Fe(II) under microaerophilic conditions from Vailulu’u Seamount. Many of these were related to the genera Pseudoalteromonas and Pseudomonas which play a role in precipitation of iron oxides in these marine systems. Under biocatalysis by IOB, the oxidation rate of Fe2+ is a hundred times higher than that in the abiotic process [28,31]. Thus, IOB accelerate the dissolution of metal and the development of localized corrosion [32]. Various explanations of this phenomenon were suggested [27]. Wang et al. [9] have reported that the corrosion process in the presence of IOB occurs via the crevice corrosion mechanism. The role of IOB lies in the formation of condensed oxygen zones and partition of the metal surface into small anodic sites (beneath a dense deposit of iron hydroxides and biomass) and large surrounding cathodic area, which accelerate the conversion of Fe0 to Fe2+, ultimately causing the defects to develop into pits. Nevertheless, O2 consumption by IOB may also generate differential aeration cells that enhance corrosion, and enhanced deoxygenation improves the growth conditions for anaerobic bacteria (e.g., SRB) which can propagate quickly [26,33]. The occurrence of MIC is usually caused by natural populations containing several bacterial species rather than a single species [34–36].

Marine microorganisms are being studied for a couple of decades. Indeed, marine bacterial diversity is vastly understated, which is one of the difficult areas of biodiversity research [37]. There are different groups of bacteria that coexist in the marine environment including but not limited to SRB, methanogenic bacteria, halophilic bacteria and Pseudomonas[38]. These bacteria may exert influence on one another and adhere in biofilm, forming complex consortia that are capable of affecting electrochemical processes through co-operative metabolisms [39]. However, MIC studies conducted to date have focused on pure cultures [20,29]. As a consequence, the influence of microbial interactions on MIC has often been overlooked. Thus, the present study aims to point out the corrosion mechanism of mixed SRB and IOB (mixed SRB + IOB) on X65 steel in seawater, which gives an insight into understanding the importance of mixed bacteria in the study of MIC.

2Experimental2.1Metal specimens

All specimens used in this work were X65 carbon steel with the elemental composition (wt.%) of 0.03 C, 0.17 Si, 1.51 Mn, 0.02 P, 0.17 Ni, 0.04 Cu, 0.16 Mo, 0.06 Nb, 0.02 Al, 0.01 Ti and balance Fe. The specimens used for electrochemical measurements had a dimension of 10 mm × 10 mm × 3 mm, and were sealed in epoxy, leaving a work area of 1 cm2. The specimens of 30 mm × 10 mm × 2 mm in dimension were used for weight-loss testing. The work face of the specimens was abraded with 600, 800 and 1200-grit silicon carbide metallurgical papers sequentially, degreased by anhydrous ethanol, and was then dried in high-purity N2 (99.999%). All specimens were sanitized for 30 min using an ultraviolet (UV) lamp before use to insure no contamination by other bacteria.

2.2Microbe cultivation and inoculation

In this study, both SRB (Desulfovibrio caledoniensis) and IOB (Pseudomonas sp.) were isolated from the rust layers of carbon steel immersed in seawater environments (Qingdao, China) and identified by polymerase chain reaction (PCR) amplification of 16S rDNA. The 16S rDNA sequence was compared with sequences in the GenBank database with BLAST program. SRB cultures were inoculated in sterile Postgate C medium containing the following (per liter of natural seawater): 0.5 g KH2PO4, 0.06 g MgSO4·7H2O, 0.06 g CaCl2·6H2O, 1.0 g NH4Cl, 1.0 g yeast extract, 0.3 g sodium citrate, in addition to 6.0 mL of 70% sodium lactate (pH 7.2 ± 0.1). IOB were grown in Winogradski nutrient medium (per liter of natural seawater): 0.5 g K2HPO4, 0.5 g NaNO3, 0.2 g CaCl2, 0.5 g MgSO4·7H2O, 0.5 g (NH4)2SO4 and 10.0 g ammonium iron citrate (pH 7.2 ± 0.1). Before inoculation, the culture medium was sterilized by autoclaving at 121 °C for 20 min. The initial concentration of dissolved oxygen (DO) in the medium was 4.8 ppm, which was measured using a DO meter (DO200, YSI, USA) after autoclaving. 5 mL SRB seed culture and 5 mL IOB seed culture were kept in an incubator at 30 °C for 5 days, and then were transferred to 500 mL sterilized seawater containing nutrients to prepare the test solution in this work. For the mixed SRB and IOB culture, 5 mL SRB seed culture and 5 mL IOB seed culture were added together to 500 mL test solution. The active cell number of SRB and IOB was estimated by most probable number (MPN) method according to the American Society of Testing Materials (ASTM) Standard D4412-84.

2.3Weight loss measurements

The corrosion rate of X65 steel was measured by the weight loss method using the following Eq. (1). Three parallel specimens were tested under each condition to ensure the reproducibility of the results. Corrosion products were stripped using a pickling solution containing corrosion inhibitor of hexamethylenetetramine for 5 min. The exposed specimen surface was finally rinsed with distilled water, cleaned in absolute ethanol, and dried using high-purity N2. The corrosion rate (Vcorr) of the steel (mm/y) was calculated by:

where △m, ρ, A and t are weight-loss (g), specimen density (g/cm3) and exposed specimen area (cm2) and exposure time (h), respectively.

2.4Surface analysis

Before scanning electron microscopy (SEM, Tescan Vega3, Czech Republic) observation and energy dispersive X-ray spectrum (EDS) analysis of biofilm and corrosion products, the specimens were pretreated by being soaked in phosphate buffered saline (PBS) solution containing 2.5% (v/v) glutaraldehyde for 8 h in order to immobilize cells. The specimens were then dehydrated using serial dilution of ethanol (30%, 50%, 70%, 90% and 100% in v/v), each for 15 min except the final step for 30 min. After that, all the specimens were dried using high-purity N2 and placed in desiccators. Prior to SEM observation, a thin gold film of 0.5 mm in thickness was coated on the specimen surface to provide electrical conductivity. Moreover, SEM was used to characterize the surface morphology of the corroded steel specimens after the corrosion products were removed. X-ray photoelectron spectroscopy (XPS, Thermo Fisher, USA) was used to analyze the composition of corrosion products on the specimen surfaces utilizing monochromatic Al Kα radiation. The specimens were dried and stored in a N2 atmosphere before the XPS analysis.

2.5Electrochemical measurements

All the electrochemical measurements were performed using a Gamry potentiostat (Reference 600, Gamry instrument, Warminster, PA, USA) with a saturated calomel electrode (SCE) as the reference electrode and platinum plate as the counter electrode. Electrochemical impedance spectroscopy (EIS) was tested at the steady-state open circuit potential (OCP) by applying a sinusoidal voltage signal of 10 mV in the frequency range of 10−2–105 Hz. The EIS data were analyzed using Zview2 software (Scribner Inc.) with a suitable equivalent circuit model. Potentiodynamic polarization curves were measured by scanning the potential from −200 mV to +300 mV versus OCP at a sweep rate of 0.5 mV/s. And the polarization curves were analyzed using Cview2 software (Scribner Inc.). All experiments were carried out at 25 °C in airtight system and repeated at least 3 times.

3Results and discussion3.1DO measurements

O2 is an important parameter affecting microbial activity. Fig. 1 shows the variations of the DO in mixed SRB + IOB media with time. It can be seen that the concentration of DO was decreased with time and became depleted to as low as 0.04 ppm after 7 days, almost reaching anaerobic conditions, which could be attributed to the consumption of O2 by aerobic IOB.

Fig. 1.

Variations of the DO in mixed SRB + IOB media with time.

3.2SRB and IOB cell counts

Fig. 2 shows the growth curves of planktonic SRB and IOB in SRB, IOB and mixed SRB + IOB media. In single SRB medium, SRB exhibited a slow linear growth and reached to 7.5 × 106 cells/mL at 7 days. In mixed SRB + IOB media, the active SRB count increased quickly and reached to 1.1 × 108 cells/mL at 3 days, which was higher than that in single SRB culture. This suggested that the consumption of O2 by aerobic IOB favored the growth of anaerobic SRB. In the later culture stage, SRB and IOB counts exhibited a fast decay due to the limitation of essential nutriments.

Fig. 2.

The growth curves of bacterial cells in SRB, IOB and mixed SRB + IOB media.


Table 1 shows the cell counts of sessile SRB and IOB in the biofilm on the specimen surface at different culturing times in mixed SRB + IOB media. The initial count of the sessile IOB cells settled on the specimen surface was to 4.6 × 109 CFU/cm2 at 2 days, which was 4 orders of magnitude higher than that of SRB (7.5 × 105 CFU/cm2). This indicated that at the start of the test, the abundant oxygen content inhibited the anaerobic activity of SRB, but created conditions conducive for aerobic IOB metabolism. With the activity of IOB, the available DO was as low as 0.04 ppm as shown in Fig. 1. Meanwhile, the count of sessile SRB cells on the specimen surface was much higher than that of sessile IOB after 5 days, which further confirmed that the growth and propagation of SRB were closely associated with the low O2 condition created by aerobic IOB.

Table 1.

The cell counts of sessile SRB and IOB (CFU/cm2) in the biofilm at different culture times.

  2 days (Sessile)  5 days (Sessile)  13 days (Sessile)  21 days (Sessile) 
SRB-In mixed media  7.5 × 105  2.4 × 1010  1.5 × 107  2.9 × 105 
IOB-In mixed media  4.6 × 109  2.1 × 107  7.5 × 104  2.3 × 103 
3.3Surface morphology analysis

Fig. 3 shows SEM images of biofilm morphology changes with time on the specimen surfaces exposed to mixed SRB + IOB media. As a control experiment, corrosion analyses were also performed on specimens in sterile medium. The X65 steel specimen showed a relatively coherent and homogenous surface after 5 days of exposure in sterile medium (Fig. 3(a1)), and corrosion product layer became more compact after 21 days of exposure (Fig. 3(a3)). EDS analysis results (Fig. 4(a1–a3)) indicated that the main components of the corrosion products in sterile medium were inorganic compounds (e.g., iron oxides). Numerous SRB and IOB cells (about 2–3 μm), metabolic products and biofilm were accumulated on the specimen surface after 5 days of exposure in mixed culture of SRB + IOB (Fig. 3(b1)). After exposure to mixed media for 13 days (Fig. 3(b2)), corrosion products covering the specimen surface, had a delaminated structure. Then, with the decline of bacteria, the whole biofilm structure was uneven, and pores and cracks increased, which may not be protective to the metal (Fig. 3(b3)). EDS analysis (Fig. 4b) suggested that the corrosion products contained mainly iron oxides, phosphates and sulfides. It was important to point out that the high peak of P was attributed to the presence of K2HPO4 and KH2PO4 as components in the culture media [40].

Fig. 3.

SEM images of X65 steel after 5, 13, 21 days of exposure in (a1, a2 and a3) sterile and (b1, b2 and b3) mixed SRB + IOB media.

Fig. 4.

EDS analysis of X65 steel after 5, 13, 21 days of exposure in (a1, a2 and a3) sterile and (b1, b2 and b3) mixed SRB + IOB media.


Fig. 5 shows the corroded morphologies of X65 steel after removing the corrosion products. In sterile solution, the specimen surface was, in general, smooth and basically no localized corrosion could be observed (Fig. 5(a1–a3)), which indicated that uniform corrosion was the dominant corrosion form throughout exposure period. In the presence of mixed SRB + IOB, no apparent pitting corrosion could be seen in the image (Fig. 5(b1)), indicating that the uniform corrosion dominated the corrosion attack after 5 days of exposure. The obvious annular damages appeared on the specimen surface after 13 days (Fig. 5(b2)), indicating pitting attack. Following exposure of 21 days, the pit numbers increased significantly (Fig. 5(b3)). All these revealed that the biofilm structure, bacterial activity (SRB and IOB) and metabolic products could have a great impact on the corrosion process, resulting in the variation of corrosion mechanisms. A systematic discussion will be discussed later.

Fig. 5.

SEM images of X65 steel after removing corrosion products after exposure to (a1, a2 and a3) sterile and (b1, b2 and b3) mixed SRB + IOB media for 5, 13, 21 days.


Fig. 6 shows surface morphologies of X65 steel after exposure to SRB, IOB medium alone for 21 days. As seen in Fig. 6(a1), the biofilm structure that formed in single SRB medium was heterogeneous and porous. EDS analysis (Fig. 6(a2)) revealed the presence of sulfur and iron, indicating the formation of iron sulfide through the reduction of SO42– by SRB. In IOB medium, the substrate of the specimen could hardly be seen, as it was covered with some spherical granules on the surface (Fig. 6(b1)). EDS analysis showed that iron, oxygen, phosphorus and calcium were the main components (Fig. 6(b2)), indicating that the corrosion products on the specimen surface comprised iron oxides and phosphate precipitates. After the corrosion products film was removed from the steel surface, localized minor pits were observed as shown in Fig. 6(a3) and (b3). By contrast, the pitting damage of metal specimen after 21 days of exposure in mixed SRB + IOB media (Fig. 5(b3)) was more severe than that in single SRB or IOB medium.

Fig. 6.

SEM and EDS analysis of X65 steel after exposure to SRB (a1, a2 and a3), IOB (b1, b2 and b3) medium alone for 21 days: (a1, b1) SEM images of corrosion products; (a2, b2) EDS analysis of corrosion products; (a3, b3) SEM images after removing corrosion products.

3.4Weight loss measurements

Fig. 7 shows the corrosion rate of X65 steel calculated from the weight loss after 7, 21 days of exposure in sterile, SRB, IOB and mixed SRB + IOB media. The highest corrosion rate was recored in mixed SRB + IOB media. This result indicated that the combination of SRB and IOB accelerated the corrosion of the specimen. After 7 days of exposure, the corrosion rate in mixed SRB + IOB media was 0.289 mm/y. With a longer exposure time, the corrosion rate increased to 0.363 mm/y at 21 days. The results confirmed that corrosion in mixed SRB + IOB culture mainly occurred in the later culture stage.

Fig. 7.

Corrosion rate of X65 steel after 7, 21 days of exposure in different media. The errors shown for each data point is the standard deviation obtained from three sets of measurements.

3.5Electrochemical measurements3.5.1Open circuit potential

Fig. 8 shows the variations of the OCP with time in sterile medium and mixed SRB + IOB media. The OCP remained nearly alike at first 2 days under different corrosion conditions. In sterile medium, the OCP shifted negatively at 3 days, and then shifted to positive direction gradually to 10 days. After that, the OCP remained nearly unchanged. In mixed SRB + IOB media, the OCP shifted to positive direction before 11 days, which could be attributed to the formation of dense biofilm and corrosion products on the specimen surface. Then, the OCP shifted to negative direction gradually until 15 days and kept steady at subsequent days. The different changes of OCP suggested that microorganisms surely influenced the electrochemical corrosion process.

Fig. 8.

Variations of the OCP with time in sterile and mixed SRB + IOB media.

3.5.2EIS measurements

The EIS was carried out under the stable OCP. Fig. 9 shows the Nyquist and Bode plots with time in sterile medium and mixed SRB + IOB media. A remarkable difference observed from the Nyquist plots was that the diameter of Nyquist loops in mixed SRB + IOB media was smaller than those in sterile medium. This result demonstrated that the corrosion process was promoted by the combination of SRB and IOB, which was consistent with the results of the corrosion rate test (Fig. 7). The diameter of impedance loops in sterile medium continuously increased with exposure time (Fig. 9(a1)), which was a result of the accumulation of corrosion products on the specimen surface. As seen in Fig. 3a, the corrosion products were more compact with time, which provided a protective effect and slowed down the corrosion of steel. Weight loss measurements also have validated that the corrosion rate of specimen in sterile medium decreased with a longer exposure time. For specimen in mixed SRB + IOB media (Fig. 9(b1)), the diameters of Nyquist loops decreased during the first 3 days, then increased gradually, and afterwards decreased again after 11 days. During the initial period of 1–3 days, the high concentration of DO (>2.2 ppm) in the solution provided better conditions for the metabolic activity of aerobic IOB. The sessile IOB cells attached to the specimen surface were 4 orders of magnitude higher than that of SRB (Table 1). It was possible that aerobic IOB were the dominant bacteria in mixed SRB + IOB culture during this stage, which induced the corrosion process on the steel surface initially. Subsequently (5–11 days), the diameter of the Nyquist loops increased and reached a maximum at 11 days. This fact suggested that the accumulation of bacterial cells (IOB and SRB), metabolic products and the bacterial biofilm on the specimen surface hindered the charge transfer process; that was, it generated a higher charge transfer resistance at this stage. Afterwards (13–21 days), the diameter of the Nyquist loops decreased again, which may have been a result of one or more of the following: (1) Firstly, the space structure of biofilm was more heterogeneous and porous after exposure for 13 days (Fig. 3(b2) and (b3)), which provided the permission channels of corrosive ions (e.g. Cl, HS), facilitating corrosion of specimen. (2) With the consumption of O2 by IOB, the available DO in the solution was as low as 0.04 ppm, which inhibited the aerobic activity of IOB, but promoted the growth of SRB. Also, the relatively high sulfur content in the biofilm indicated the high SRB activity at 21 days (Fig. 4(b3)), producing large amount of ferric sulfide. It has been reported that ferric sulfide can act like cathodes to the metal substrate, thus creating a electrochemical corrosion cell and enhancing the corrosion rate [17]. (3) This decline in Nyquist loops could be attributed to the corrosive H2S metabolically generated by SRB. Many studies reported that the formation of H2S promoted the electrochemical reactions, resulting in severe localized corrosion damage [18,41]. According to the analysis above, it could be inferred that the mixed bacterial activity (SRB and IOB), biofilm structure and metabolic products could together interfere with the electrochemical reactions during steel corrosion. The Bode phase angle vs. log frequency plot showed that the phase angle peak shifted to the low frequency from 1 day to 11 days (Fig. 9(b2)), demonstrating the formation of a dense biofilm as shown in Fig. 3(b1). Afterward, the phase angle peak was followed by a shift in the high frequency side (13–21 days), indicating the breakdown of the biofilm [42].

Fig. 9.

Nyquist and Bode plots of X65 steel in sterile (a1, a2 and a3) and mixed SRB + IOB media (b1, b2 and b3).


The impedance spectra in Fig. 9 were curve-fitted with the Zview2 software satisfactorily (errors <10%). As shown in Fig. 10, one-time and two-time constant model were used to describe the corrosion process of X65 steel, respectively. Experimental data for X65 steel in sterile medium were analyzed using one-time constant. Experimental data for X65 steel in mixed SRB + IOB media were analyzed with two-time constant that showed biofilm and double layer. In view of the inhomogeneous electrode surface, all the capacitances were replaced by constant phase angle elements (CPE). Impedance of CPE is as below:

where ω is angular frequency in rad/s, Y0 and n are the CPE parameters, and n is the dispersion coefficient related to the surface inhomogeneity. A low n value means a high surface roughness [43]. In the equivalent circuits, Rs represents solution resistance. Rf and Qf represent the resistance and the CPE parameter for biofilm and/or corrosion products film, respectively. Rct and Qdl represent the charge transfer resistance and the CPE parameter of double layer capacitance, respectively.

Fig. 10.

Equivalent circuits used for simulate experimental impedance diagrams: (a) One-time constant; (b) Two-time constant.


The fitting results of equivalent circuit elements are listed in Table 2. In the presence of mixed SRB + IOB, the value of Rs was lower than that in sterile medium, which was ascribed to the formation of bacterial soluble metabolites, such as pyruvic acid [43]. Table 2 revealed that double layer capacitance Qdl increased with time, which was far higher than a conventional double-layer capacitance (approx. 10–3–10–2 F/cm2), indicating the accumulation of highly conductive corrosion products (e.g. iron sulfide) [8]. In addition, the biofilm resistance Rf increased and reached the maximum value on the 11 days, indicating that biofilm and corrosion products accumulated on the electrode surface. Subsequently, Rf decreased rapidly, indicating that the films layer adhering to the steel surface became porous and/or the pore sizes increased, which would facilitate the diffusion of aggressive species to the metal substrate. SEM results (Fig. 5(b2) and (b3)) showed that significant pitting occurred after 11 days of exposure in mixed culture of SRB and IOB. The charge transfer resistance Rct is closely related to corrosion rates, and a higher value means a lower corrosion rate [44]. In mixed SRB + IOB, the value of Rct (Table 2) decreased from 1 day to 3 days, then increased gradually and reached the maximum value on the 11 days, and afterwards decreased with exposure time, which corresponded to the changes of Nyquist loops diameter (Fig. 9(b1)). In sterile medium, the change of Rct value was different from that in mixed SRB + IOB. And the value of Rct in sterile medium was higher than that in mixed SRB + IOB, suggesting that the presence of SRB and IOB contributed to a higher corrosion rate.

Table 2.

EIS fitting results of X65 steel specimens in different media based on the equivalent circuit in Fig. 10.

  T(d)  Rs (Ω cm2Rct (Ω cm2Qdl (F cm2ndl  Rf (Ω cm2Qf (F cm2nf 
  7.86  105.6  0.00250  0.859       
  7.32  106.9  0.00876  0.923       
  6.90  128.6  0.01265  0.937       
  7.68  197.5  0.01511  0.944       
Sterile  8.34  341.4  0.01783  0.945       
  11  8.27  594.5  0.01957  0.950       
  13  7.37  655.2  0.02045  0.961       
  15  7.83  784.4  0.02048  0.977       
  17  6.88  991.9  0.02103  0.979       
  19  7.12  1552  0.02138  0.980       
  21  7.07  2278  0.02161  0.987       
  3.77  105.20  0.0035  0.921  0.61  0.05253  0.714 
  3.68  101.50  0.01480  0.920  0.64  0.05584  0.734 
  3.56  133.60  0.03408  0.924  0.65  0.05838  0.761 
  3.57  184.90  0.03479  0.925  0.81  0.07596  0.723 
Mixed  3.53  265.90  0.03488  0.933  18.25  0.06735  0.711 
SRB + IOB  11  3.59  296.30  0.03573  0.944  20.80  0.08713  0.753 
  13  3.66  211.20  0.03882  0.930  7.90  0.07032  0.762 
  15  1.72  34.68  0.08600  0.882  0.45  0.06043  0.781 
  17  2.98  25.56  0.10850  0.871  0.25  0.05062  0.812 
  19  2.01  14.84  0.20100  0.846  0.21  0.08600  0.808 
  21  2.05  12.61  0.20403  0.841  0.21  0.09030  0.798 
3.5.3Polarization measurements

Fig. 11 shows the potentiodynamic polarization curves of X65 steel after 7, 21 days exposure in sterile and mixed SRB + IOB media. The measured polarization curves were fitted through Cview2 software to obtain electrochemical parameters e.g. corrosion potential (Ecorr), corrosion current density (icorr) and anodic and cathodic Tafel slopes (βa and βc), as shown in Table 3. It was observed that the icorr in the presence of SRB and IOB were larger than that in sterile medium, which further confirmed that the synergy of mixed species indeed promoted corrosion of X65 steel. In mixed SRB + IOB media, the corrosion current density increased dramatically and reached a high value of 5.62 × 10–4 A/cm2 after extending the exposure time to 21 days. In contrast, the corrosion current density in sterile medium was reduced to 5.89 × 10–6 A/cm2 at 21 days due to the protective role of the corrosion products formed on the specimen surface. For a corrosion process, corrosion rate was closely related to the cathodic and anodic reaction [45]. The changes in βa and βc indicated that the corrosion mechanisms of anode process and cathode process varied with time. In mixed SRB + IOB media, the value of βa increased from 0.072 V/dec to 0.149 V/dec, indicating a slowdown in the anode kinetics. While, βc decreased from 0.216 V/dec to 0.183 V/dec, and icorr increased from 2.58 × 10–4 A/cm2 to 5.62 × 10–4 A/cm2, suggesting that the corrosion process was promoted by the accelerated cathodic reaction.

Fig. 11.

Potentiodynamic polarization curves of X65 steel after 7 days and 21 days exposure in (a) sterile and (b) mixed SRB + IOB media.

Table 3.

Tafel parameters of X65 steel specimens after 7 days and 21 days exposure in sterile medium and mixed SRB + IOB media.

  T (d)  Ecorr (V) vs. SCE  icorr (A/cm2βa (V/dec)  βc (V/dec) 
Sterile  −0.638  7.58 × 10−5  0.125  0.220 
  21  −0.627  5.89 × 10−6  0.075  0.235 
Mixed SRB + IOB  −0.655  2.58 × 10−4  0.072  0.216 
  21  −0.674  5.62 × 10−4  0.149  0.183 
3.6XPS analysis

Fig. 12a shows the wide XPS spectra of X65 steel exposed to sterile and mixed SRB+IOB media for 21 days. Peaks for Fe 3p, C 1s, O 1s, Fe 2p, Fe LMM Auger peak and O KLL Auger peak were observed in the spectra of the two X65 specimens. Relative proportions of C and O increased after SRB+IOB inoculation compared with those in sterile medium. This result was caused by adsorption of biofilm on the X65 steel surface.

Fig. 12.

XPS spectra of (a) wide scans, (b) C 1s, (c) O 1s and (d) Fe 2p for X65 steel after 21 days of exposure in sterile and mixed SRB + IOB media.


Fig. 12b–d show the high-resolution XPS spectra of C 1s, O 1s and Fe 2p for X65 specimens after 21 days of exposure in sterile and mixed SRB+IOB media, respectively. All spectra were fitted with XPS peak software. The binding energies were calibrated with respect to the signal of C 1s (binding energy = 284.82 eV). XPS spectra could also provide relative quantity of compounds. Elemental atom ratios were calculated from the peak areas. The fitting parameters of C 1s, O 1s and Fe 2p, as well as the atom percentages (At%) of various components, were provided in Table 4. In sterile medium, the C 1s spectrum could be curvefitted with three peaks. The peaks at 284.6, 285.5 and 288.3 eV were attributed to the C–H, C–C and C=O, which indicated the existence of organic compounds (e.g. yeast cream) [31]. In mixed SRB + IOB media, the peaks at 284.6, 285.8 and 288.3 eV corresponded to the C–H, C–N and C=O, respectively. The elements N was the characteristic of proteins [46], indicating the adsorption of biofilm on the specimen surfaces. In sterile and mixed SRB + IOB media, both the O 1s spectra were curve-fitted with three peaks. The peak at 529.9 and 531.3 eV corresponded to Fe2O3 and FeOOH, respectively [47]. The peaks at 532.1 was attributed to organic O [48]. In the presence of SRB and IOB, the increase in the peak area of organic O further confirmed the adsorption of biofilm. In sterile medium, the Fe 2p3/2 spectrum could be curve-fitted with three peaks. The peaks at 710.5, and 710.9 eV both corresponded to Fe2O3, while the peak at 711.8 eV was attributed to FeOOH [49]. In the presence of SRB + IOB, the Fe 2p3/2 spectrum could be curve-fitted with four peaks. The peaks at 710.0 corresponded to FeS [50], the peaks at 710.7 and 711.7 eV corresponded to Fe2O3 and FeOOH, respectively, and the peak at 712.8 eV corresponded to FePO4[48].

Table 4.

Fitting parameters for C 1s, O 1s and Fe 2p XPS spectra and the relative quantity of compounds in the corrosion products.

Valence state  Sample  Binding energy (eV)  Proposed components  (At%) 
C 1 s  Sterile  284.6  C–H  49.3 
    285.5  C–C  32.6 
    288.3  C=O  18.1 
  Mixed  284.6  C–H  49.6 
  SRB + IOB  285.8  C–N  27.3 
    288.3  C=O  23.1 
O 1 s  Sterile  529.9  Fe2O3  34.9 
    531.3  FeOOH  48.7 
    532.1  Organic O  16.4 
  Mixed  530.0  Fe2O3  30.1 
  SRB + IOB  531.3  FeOOH  42.7 
    532.1  Organic O  27.1 
Fe 2p  Sterile  710.5  Fe2O3  14.7 
    710.9  Fe2O3  67.6 
    711.8  FeOOH  17.7 
  Mixed  710.0  FeS  18.2 
  SRB + IOB  710.7  Fe2O3  54.0 
    711.7  FeOOH  18.2 
    712.8  FePO4  9.6 
3.7Corrosion mechanism discussion

The present results confirmed that compared to single SRB or IOB medium, the coexistence of SRB and IOB in mixed species biofilm promoted the corrosion process of the steel. The corrosion mechanisms of X65 steel in mixed SRB + IOB media varied with time and could be divided into three stages as shown in Fig. 13.

Fig. 13.

Schematic representation of corrosion mechanism by mixed SRB + IOB at different stages: (a) accumulation of iron oxides initiated by DO and IOB activity, (b) formation of mixed species biofilm, and (c) formation and propagation of pits.


In the first stage (1–3 days), the corrosion process was initiated by the high DO concentration and high IOB activity in natural seawater with mixed SRB + IOB culture (Fig. 13a). IOB are aerobic microorganisms that are able to oxidize Fe2+ to Fe3+ with O2 as the terminal electron acceptor to obtain energy for growth. The metabolic activity for aerobic IOB depended strongly on DO and matrix material [32]. Thus, the relatively higher DO concentration before 3 days (>2.2 ppm) provided a favorable condition for the growth of IOB. As shown in Table 1, the IOB count in the biofilm was 4.6 × 109 CFU/cm2 at 2 days, which was 4 orders of magnitude higher than that of SRB (7.5 × 105 CFU/cm2). Thus, at this stage, the metal was corroded by the dominant IOB in the mixed culture. EDS and XPS analysis results indicated that the main corrosion products were iron oxides (FeOOH, Fe2O3). So, the corrosion mechanism for aerobic IOB can be expressed as follows:

Anodic reaction:

Fe → Fe2+ + 2e (3)
Fe2+ → Fe3+ + e (4)

Cathodic reaction:

O2 + 2H2O + 4e → 4OH (5)

Corrosion product:

2Fe2+ + 4OH + 1/2O2 → 2FeOOH + H2O (6)

The unstable FeOOH could decompose into Fe2O3.

2FeOOH → Fe2O3 + H2O (7)

With the growth and proliferation of IOB, the respiration of aerobic IOB scavenged O2 and provided better growth conditions for anaerobic SRB. Then, numerous bacterial cells (SRB + IOB), biofilm matrix and corrosion products adhered on the specimen surface (Fig. 13b), which hindered the corrosion process. The EIS results (Fig. 9(b1)) also confirmed this conclusion, the diameters of Nyquist loops gradually increased from 5 days to 11 days. Chongdar et al. [51] also reported that microbial biofilm as a protective barrier had an inhibitory effect on the metal dissolution.

Finally, the decrease of corrosion rate in the third stage (13–21 days) was attributed to the high metabolic activity of settled SRB and the porous biofilm structure (Fig. 13c). With the mixed culture of SRB + IOB, after 21 days, the count of SRB in the biofilm outnumbered the IOB by approximately 100 times (Table 1). This suggested that in mixed culture, the limitation of DO (<0.04 ppm) hindered the metabolism of IOB, but provided better optimal conditions for the anaerobic activity of SRB. Thus, at the later stage of the test, SRB was the main contributor of MIC in the seawater with mixed culture, leading to increased corrosion rate. Anaerobic SRB can efficiently facilitate the reduction of SO42– to sulfide, promoting the electrochemical reaction, as follows [13]:

Anodic reaction:

Fe → Fe2+ + 2e (3)

Cathodic reaction:

SO42− + 8H+ + 8e → HS + OH + 3H2O (8)

Corrosion product:

Fe2+ + HS → FeS + H+ (9)
HS + H+ → H2S (10)

Potentiodynamic polarization tests (Fig. 11b) also suggested that the increase of corrosion current at 21 days was associated with the appearance of the accelerated cathodic reaction. It was also evidenced that the mechanism through which SRB could act involves the formation of hydrogen sulfide with the precipitation of iron sulfide, which promoted the formation of pits [17,52]. Romero et al. [53] reported that the bacteria in the SRB biofilm produced enough corrosive hydrogen sulfide which reduced the local pH in the biofilm, thereby causing serious local corrosion. In addition, the porous biofilm structure also played an important role in the corrosion process. Due to the breakdown of the biofilm (Fig. 3(b3)), the protective effect on the metal surface was poor and large part of the activated surface are exposed to the corrosive ions (e.g. Cl, HS). Consequently, all these factors collectively resulted in the formation and propagation of pits as shown in Fig. 5(b3). And the corrosion rate increased sharply to 0.363 mm/y at 21 days (Fig. 7).


The experimental results in this work showed that the combination of SRB and IOB caused more severe corrosion. In mixed SRB + IOB media, the consumption of O2 by aerobic IOB promoted the growth of anaerobic SRB. EIS and potentiodynamic polarization measurements confirmed the significant variation of corrosion mechanisms with time in mixed culture of SRB + IOB. In general, the corrosion process was controlled by the metabolic activities of the bacteria (SRB and IOB), biofilm structure and metabolic products comprehensively, which facilitated the formation of localized pitting corrosion and increased the corrosion damage degree.

Conflicts of interest

The authors declare no conflicts of interest.


This work was supported by National Natural Science Foundation of China (No. 51871204). We are indebted to Jizhou Duan, Fang Guan, Yan Ma and Yimeng Zhang from Marine Corrosion and Protection Centre, Institute of Oceanology, Chinese Academy of Sciences for their help in microbial culture.

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