Salvia officinalis extract mitigates the microbiologically influenced corrosion of 304L stainless steel by Pseudomonas aeruginosa biofilm

Bioelectrochemistry 128 (2019) 193–203

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Salvia officinalis extract mitigates the microbiologically influenced corrosion of 304L stainless steel by Pseudomonas aeruginosa biofilm Yassir Lekbach a,b, Zhong Li a, Dake Xu a,⁎, Soumya El Abed b, Yuqiao Dong a, Dan Liu a, Tingyue Gu d, Saad Ibnsouda Koraichi b, Ke Yang c, Fuhui Wang a a

Shenyang National Laboratory for Materials Science, Northeastern University, Shenyang 110819, China Laboratory of Microbial Biotechnology, Faculty of Science and Technology, Sidi Mohamed Ben Abdellah University, B.P. 2202 Fez, Morocco Institute of Metal Research, Chinese Academy of Sciences, Shenyang 110016, China d Department of Chemical and Biomolecular Engineering, Institute for Corrosion and Multiphase Technology, Ohio University, Athens, OH 45701, USA b c

a r t i c l e

i n f o

Article history: Received 4 January 2019 Received in revised form 26 March 2019 Accepted 8 April 2019 Available online 11 April 2019 Keywords: 304L stainless steel Biofilm Microbiologically influenced corrosion Pseudomonas aeruginosa Green inhibitor

a b s t r a c t The mitigation of microbiologically influenced corrosion (MIC) of 304L stainless steel (SS) against Pseudomonas aeruginosa by a Salvia officinalis extract was investigated using electrochemical and surface analysis techniques. The extract was characterized by HPLC-Q-TOF-MS and its antibiofilm property was evaluated. The data revealed the presence of well-known antimicrobial and anticorrosion compounds in the extract. The S. officinalis extract was found effective in preventing biofilm formation and inhibiting mature biofilm. Electrochemical results indicated that P. aeruginosa accelerated the MIC of 304L SS, while the extract was found to prevent the MIC with an inhibition efficiency of 97.5 ± 1.5%. This was attributed to the formation of a protective film by the adsorption of some compounds from the extract on the 304L SS surface. © 2019 Elsevier B.V. All rights reserved.

1. Introduction Microbiologically influenced corrosion (MIC) is known as an electrochemical process in which microorganisms adhere to the surfaces of metals or other materials. This can induce or accelerate corrosion reactions of these materials through the interfacial interaction with the metabolic activities of these microorganisms [1,2]. Microbial corrosion occurs for metals exposed to fresh water, seawater, soils, gas and oil fluids [3]. In the marine environment, many types of microorganisms can initiate and/or induce corrosion of materials including bacteria, fungi and archaea [4,5]. Among these microorganisms, a pioneer bacterium for biofilm formation in seawater environment, Pseudomonas aeruginosa, is capable of forming biofilm on different types of metals and their alloys [6–8]. P. aeruginosa is a ubiquitous bacterium associated with nosocomial infections to biocorrosion，and even biofouling [9]. Many previous studies have reported the corrosive effects of P. aeruginosa on metals and alloys [10–12]. Several possible mechanisms have been published to explain the corrosion induced by P. aeruginosa under aerobic conditions. Yuan et al. [13] suggested that creation of differential aeration cells by P. aeruginosa biofilm led to the initiation of pit formation on the 304 stainless steel (SS) surfaces. This mechanism was confirmed ⁎ Corresponding author. E-mail address: [email protected] (D. Xu).

https://doi.org/10.1016/j.bioelechem.2019.04.006 1567-5394/© 2019 Elsevier B.V. All rights reserved.

by Hamzah et al. [14]. Furthermore, a recent study by Huang et al. [15] explained the corrosion influenced by this bacterium at the genetic level. They found that phenazine-1-carboxamide, which is a watersoluble electron mediator encoded by the gene PhzH, was responsible for the accelerate corrosion of 2205 duplex stainless steel by facilitating the extracellular electron transfer (EET) between the bacterial cells and the metal. Considering the fact that stainless steel is widely employed in various industries, many studies have been carried out to study the corrosion and biofouling of these materials [16]. 304L SS is known for its good mechanical properties, and corrosion resistance due to the formation of a thin, but dense protective film that covers the surface [17]. However, many studies have reported that 304L SS was susceptible to MIC. Zhang et al. [18] reported that Desulfovibrio vulgaris accelerated the corrosion rate of 304 SS by facilitating EET between the biofilm and SS. Durmoo et al. [19] studied the behavior of 304L SS in contact with sugar cane juices. They found that bacteria can form biofilm on the surface and the products of their metabolisms affected the passive film. Several mitigation techniques have been proposed to address MIC problems, including chemical, biological and physical methods [20–22]. Among these techniques, the use of biocides as chemical treatment is in the forefront for mitigation of MIC [23]. However, as a result of the increasing awareness of environmental risks caused by biocides, there is a need to seek cheap, eco-friendly and highly efficient MIC

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inhibitors [24]. Natural products, such as aromatic and medicinal plants, present an enormous source of environmentally benign organic compounds which are readily available and renewable. Aromatic and medicinal plants have many secondary metabolic pathways that secrete active compounds, such as phenols, flavonoids, alkaloids, tannins, terpenes, etc., which are known for their antimicrobial, antioxidant, antifouling and anticorrosion activities [25–28]. The ability of these active molecules to inhibit corrosion is due to their molecular structures which are similar to the conventional organic corrosion inhibitors. It is well known that plant extracts contain organic compounds such as heterocyclic compounds which contain polar functional groups like O\\H, C\\O, C_O, C_C, C\\N, N\\H [29,30]. These compounds possess the ability to adsorb on metal surfaces and to form a protective layer that protects them from corrosion [31]. Seeking eco-friendly and non-toxic natural compounds that could be used for MIC protection of 304L SS, a Salvia officinalis extract was selected for the present study. S. officinalis belongs to the family of Lamiaceae and it is widely used in medicine preparation, cosmetic formulations, food flavoring and insecticides [32]. Many previous studies reported the richness of S. officinalis plant in phenolic compounds which makes it a suitable source of potential inhibitors for MIC mitigation [33,34]. Therefore, the present study focused on the evaluation of the antibacterial, antibiofilm and anticorrosion activities of the S. officinalis extract for 304L SS against P. aeruginosa in simulated seawater environment. 2. Materials and methods

95% A. F5: 0 min, 10% A; 5 min, 15% A; 25 min, 40% A; 35 min, 40% A; 40 min, 95% A. The injection volume in the HPLC system was 10 μL and the UV–vis detection was performed in the 254–330 nm wavelength range. The MS was equipped with an electrospray ionization (ESI) interface. The optimized parameters for MS were: temperature (180 °C), capillary voltage (−4500 V), nebulizer gas pressure (1.2 bar), gas flow (0.8 mL/min), and negative ionization. The spectra were obtained at 2 s per spectrum and began from m/z 50 to m/z 1500. Finally, the Bruker Daltonics Data Analysis V. 3.4 software (Bruker Co., Germany) was used to analyze the data. 2.3. Media and growth conditions The P. aeruginosa strain used in this study was MCCC 1A00099 (Marine Culture Collection of China, Xiamen, China). The medium used was 2216E (Qingdao Hope Bio-technology Co. Ltd., Qingdao, China) which contained (per liter): 0.008 g NaH2PO4, 0.0016 g NH4NO3, 0.0024 g NaF, 0.004 g Na2SiO3, 0.022 g H3BO3, 0.08 g SrBr2, 0.034 g SrCl2, 0.08 g KBr, 0.16 g Na2CO3, 0.55 g KCl, 1.8 g CaCl2, 3.24 g Na2SO4, 5.98 g MgCl2, 19.45 g NaCl, 0.1 g ferric citrate, 1.0 g yeast extract and 5.0 g peptone. P. aeruginosa cells were cultured aerobically at 37 °C for 24 h, then the initial concentrations of bacterial cells were diluted to 106 cells/mL using fresh medium and measured at 585 nm by using a UV–Visible spectrophotometer. All the tests were conducted in abiotic, biotic and inhibited media. The sterile medium is referred to the abiotic medium and the inoculated one is called the biotic medium. The inhibited medium was inoculated with the S. officinalis extract.

2.1. Materials and sample preparation 2.4. Antibacterial assay 304L SS coupon samples with chemical composition of (mass %): 18.95 Cr, 7.93 Ni, 1.36 Mn, 1.11 Si, 0.02C, and the balance of Fe, were supplied by the Institute of Metal Research, Chinese Academy of Sciences (Shenyang, China). The coupon surfaces were abraded with different grades of silicon carbide papers (150, 240, 400, 600, 800, 1000 and 1200 grits), washed with distilled water and ultrasonically degreased by using ethanol and finally air dried. For electrochemical tests, the 304L SS coupons were connected with copper wire and then sealed by using an epoxy resin to expose a surface area of 1 cm2. Prior to each experiment, the electrodes and coupons were sterilized in 75% (v/v) ethanol solution and dried under UV light for 30 min. The ethanolic extract from S. officinalis leaves was obtained by following the procedure described by Lekbach et al. [28]. The S. officinalis extract was subjected to column chromatography on silica gel 60 (Fluka Chemie, Buchs, Switzerland) and then eluted with n-hexane-ethyl acetate (50:50), followed by ethyl acetate (100%) and finally ethanol (100%). As results, 5 fractions were obtained and were used for the identification of phytochemicals.

The lowest inhibitory concentration (LIC) was determined by the microdilution method described by Balouiri et al. [35] with minor modifications. The S. officinalis extract was suspended in 2% DMSO (v/v) to yield a concentration of 20 mg/mL. Then 100 μL was transferred to the first well of a 96-well microtiter plate. Next, the sequential dilutions were done by transferring 50 μL of the extract from the 1st well to the 2nd well and so on, through the 10th well. Initially, the 1st-10th wells all contained 50 μL of LB medium. Finally, aliquots of 50 μL of bacterial suspension adjusted to 106 cells/mL, were added into the 1st-10th wells. The positive control (11th well) contained only 50 μL of LB broth and 50 μL of bacterial suspension while the 12th well contained LB broth with 2% DMSO and 50 μL of bacterial suspension which was considered as a negative control. Following incubation for 20 h at 37 °C, 15 μL of resazurin solution (0.015%) for cell viability indication was added into each well and then incubated for 2 h to examine the change of the color [36]. In order to determinate the minimum bactericide concentration (MBC) values, the content of the wells that contained higher concentrations than LIC values were spread on LB agar plates and then incubated for 24 h at 37 °C [37].

2.2. HPLC-Q-TOF-MS analysis 2.5. Biofilm inhibition and inactivation tests The identification of phytochemicals in each fraction was carried out using an Agilent 1200 series system (Agilent Technologies, CA, USA) coupled to hybrid quadrupole time-of-flight mass spectrometry (Q-TOF-MS, Bruker Corporation, Billerica, MA). Then, a Venusil C18 column (1.8 μm, 150 × 4.6 mm, Bonna-Agela Technologies, China) was used for HPLC to separate the 1st, 2nd, 3rd, 4th, and the 5th fractions (labeled as F1, F2, F3, F4 and F5, respectively) with a gradient elution program at a flow rate of 0.5 mL/min for F1 and 0.25 mL/min for F2, F3, F4 and F5. The mobile phases consisted of acetonitrile 0.1% A and 0.1% formic acid-water B. The following multi-step gradient profile was applied for F1: 0 min, 50% A; 15 min, 95% A; 50 min, 95% A. F2: 0 min, 60% A; 15 min, 70% A; 40 min, 95% A; 45 min, 95% A. F3: 0 min, 60% A; 15 min, 70% A; 40 min, 95% A. F4: 0 min, 20% A; 10 min, 40% A; 20 min, 40% A; 30 min, 60% A; 40 min, 60% A; 50 min, 95% A; 70 min,

The inhibition of the P. aeruginosa biofilm formation and the mitigation of mature biofilms by the S. officinalis extract were investigated under confocal laser scanning microscopy (CLSM, C2 Plus, Nikon, Japan). The live/dead BacLight Bacterial Viability Kit (Invitrogen, Thermo Fisher Scientific, USA) was employed to stain the biofilms on the 304L SS coupons. The kit contained two dyes, propidium iodide (PI) and SYTO9, mixed in a saline solution. Before each observation, the 304L SS coupons were immersed in 2 mL of this dye mixture in the dark for 20 min before CLSM examination. 2.5.1. Prevention of biofilm formation The inhibition of P. aeruginosa biofilm formation was revealed through the CLSM analysis [38]. 304L SS coupons were placed

Y. Lekbach et al. / Bioelectrochemistry 128 (2019) 193–203 Table 1 Retention time (Rt), pseudomolecular ion ([M-H]−), molecular formula, error (ppm) and the tentative identification of the phenolic compounds in the studied S. officinalis ethanolic extract fractions. Fraction Rt [M-H]− (min)

Molecular formula

Error Tentative identification (ppm)

F1 F3 F4

13.78 27.98 29.70

295.2139 C13H12O8 345.1706 C20H26O5 327.2125 C18H32O5

0.7 0.4 4.9

F5

33.35 9.47

329.2348 C18H34O5 343.0826 C18H16O7

−4.4 0.7

Coutaric acid Rosmanol isomer Oxo-dihydroxy-octadecenoic acid Trihydroxy-octadecenoic acid Eupatorin

separately in flasks containing 50 mL of inoculated 2216E medium with and without the S. officinalis extract at MBC, and then the flasks were incubated at 37 °C for 1, 7 and 14 days. After incubation, the biofilms formed on the 304L SS coupons were stained and visualized under CLSM.

195

2.5.2. Mitigation of well-established biofilms The effect of S. officinalis extract on the mature biofilms was determined as previously described by Upadhyay et al. [38] with minor modifications. Briefly, P. aeruginosa biofilms were grown on the 304L SS coupon surfaces for 3 days at 37 °C in 50 mL 2216E medium. Next, the coupons were rinsed with sterile distillated water to remove non-adherent cells before being transferred to a sterile 6-well plate containing 10 mL of 2216E medium with and without the plant extract at MBC, and then incubated at 37 °C for 30, 60 and 120 min. After incubation, the coupons were taken out and rinsed with sterile distillated water. Next, the biofilms on the coupons were stained and observed under CLSM. The surface morphologies of biofilms were observed using scanning electron microscopy (SEM). Fresh 304L SS coupons were retrieved and gently rinsed with a phosphate-buffered saline (PBS) solution to remove non-adherent bacterial cells and culture medium. Next, the samples were prepared according to Li et al. [6] for observation under SEM (Ultra-Plus, Zeiss, Germany).

Fig. 1. CLSM 3-D images of 304L SS coupon surfaces after 1 day, 7 days and 14 days of incubation in the biotic (a, b and c) and inhibited media (d, e and f), respectively.

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2.6. Hydrophobicity and surface free energy The physico-chemical properties of 304L SS coupon surfaces were determined using a goniometer (GBX instruments, France) connected to a video-camera system and desktop computer. The 304L SS coupons were immersed in 20 mL of the S. officinalis extract for 1 h. Then, three contact angle measurements were taken on the surface of the coupons for three liquids (water, diiodomethane and formamide). The energy characteristics of the used liquids are listed in Table S1 [39]. The Lifshitz-van der Waals components (γLW), the electron acceptor (γ+) and electron donor (γ−) properties of 304L SS coupon surfaces were estimated by Young's equation [40]:
1
1
1 LW =2 − =2 þ =2 þ 2 γþ þ 2 γ− γL ð cosθ þ 1Þ ¼ 2 γLW S γL S γL S γL

ð1Þ

where subscript S and L indicate solid surface and liquid phases respectively. The Lewis acid and Lewis base properties were obtained according to the following equation:
− þ 1 = 2 γAB S ¼ 2 γS γS

ð2Þ

The degrees of hydrophobicity of the 304L SS surfaces were evaluated qualitatively by measuring the contact angles and by the approach of Van Oss and Giese [41]. This approach suggested that the free energy of interaction (ΔGiwi) between two entities of this material can be evaluated according to the following formula: ΔGiwi

The 304L SS surfaces were considered hydrophobic when ΔGiwi was lower than 0, and they were hydrophilic when ΔGiwi was higher than 0 [42]. 2.7. Electrochemical tests The electrochemical measurements were monitored using a Gamry potentiostat-galvanostat (Reference 600, Gamry instrument, USA). The electrochemical cells (500 mL) were composed of 304L SS as working electrode, a saturated calomel electrode (SCE) as reference electrode and a platinum sheet (10 mm × 10 mm × 1 mm) as auxiliary electrode. The linear polarization resistance (LPR) measurements were conducted with a scan rate of 0.125 mV/s over the range of −10 to 10 mV vs. the stable open circuit potential (OCP), with a 1 s as sampling interval. A frequency range of 0.01 to 100,000 Hz was used for electrochemical impedance spectroscopy (EIS) measurements and the software ZSimDemo (V. 3.30d, EChem Software, USA) was used to analyze the impedance data. For potentiodynamic polarization experiment, the scan rate used was 0.5 mV/s and the potential range was from −500 to 1500 mV with respect to OCP. From the obtained analytical parameters of Tafel polarization curves, the inhibition efficiency (IE) was calculated according to the equation [43]: IE ¼

0 icorr −icorr  100% icorr

ð4Þ

where icorr and i'corr are the corrosion current densities of the working electrode in the absence and presence of the extract, respectively. The ¼ −2γ iw " # 2 
LW 1 =
LW 1 =
1
þ − 1 =
þ − 1 =
þ − 1 =  − =2 2 2 2− γ γ 2− γ γ 2 ¼ −2 γi − γw þ 2 γþ γ þ γ γ w w w i i i i w ð3Þ

Fig. 2. CLSM 3-D images of P. aeruginosa biofilm before treatment (a) and after treatment with S. officinalis extract for: (b) 30 min, (c) 60 min and (d) 120 min.

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Table 2 Contact angle values, surface energies and their components of untreated and treated 304L SS. Substrate

Untreated surface Treated surface

Surface free energy components (mJ/m2)

Contact angles (°) θw

θf

θd

γLW

γ+

γ−

ΔGiwi

77.0 ± 0.8 23.2 ± 0.1

61.7 ± 0.2 20.1 ± 0.2

41.6 ± 0.1 36.2 ± 0.2

38.7 ± 0.1 41.4 ± 0.1

0.1 ± 0.1 0.8 ± 0.1

10.6 ± 0.8 49.5 ± 0.1

−40.3 ± 2.6 26.8 ± 0.2

volume of culture medium was 300 mL in all electrochemical cells. For the biotic one, the medium was inoculated with P. aeruginosa culture to reach an initial concentration of 106 cells/mL. 2.8. Analysis of pits depth The 304L SS coupons were taken out of the three media after incubation for 14 days, and then biofilms and corrosion products on the coupon surfaces were removed according to the Chinese National Standards GB/T4334.4–2000. The maximum pit depths were measured by using a CLSM (LSM 710, Zeiss, Germany). 3. Results 3.1. HPLC-Q-TOF-MS analysis The data from HPLC-Q-TOF-MS revealed the presence of phenolic compounds in the five peaks fractions (Fig. S1). Five active compounds were identified by comparing the pseudomolecular data to those reported in published literature and taking in consideration of the error bar (b10 ppm) (Table 1). In F1, the coutaric acid was identified as a phenolic acid which was previously reported in some Salvia species by Zengin et al. [44]. In F3, a rosmanol isomer belonging to phenolic diterpene was identified [45]. Two compounds were identified in F4, Oxodihydroxy-octadecenoic acid and Trihydroxy-octadecenoic acid, both belonging to the oxylipins family, as reported by Zengin et al. [44]. A flavone compound was characterized in F5 as eupatorin according to the information reported for several Salvia species from Southeast Europe [45]. 3.2. Antibacterial assay LIC was defined as the lowest concentration of the extract that can prevent the visible growth of P. aeruginosa. Whereas, the MBC was known as the lowest concentration that is capable to kill the initial bacterial inoculum. LIC was determined by results obtained from the resazurin colorimetric assay. The lowest concentration of S. officinalis

extract at which resazurin changed color from blue to purple was the LIC, while the plate that showed no bacterial growth after 24 h of incubation was considered as MBC. The LIC of the extract against P. aeruginosa was 1.25 mg/mL and the MBC was 2.5 mg/mL. The DMSO negative control showed no change in resazurin color which means that it had no toxic effect for bacteria. 3.3. Biofilm inhibition assay 3.3.1. Prevention of biofilm formation Biofilm formation on a metal surface is the key step of microbial corrosion process [46]. In the current study, the S. officinalis ethanolic extract was tested for its ability to prevent the formation of P. aeruginosa biofilms. Fig. 1 shows the three-dimensional CLSM images obtained from Nis-Elements Viewer software (V. 3.20, Nikon, Tokyo, Japan). It can be seen from the images that the biofilm formation in biotic medium was a continuous process. The biofilm thickness was 38.7 ± 2.6 μm after 1 day of incubation, then it increased in thickness and density to reach 43.1 ± 1.8 μm on the 7th day. After 14 days, the biofilm decreased in thickness and few dead cells appeared, this could be attributed to the depletion of essential nutrients in the medium. Whereas, the CLSM images revealed the absence of biofilm formation in the presence of the extract during the 14 days of exposure time, which indicates that S. officinalis extract inhibited the P. aeruginosa biofilm formation on the coupon surfaces (Figs. 1d, e and f). 3.3.2. Mitigation of pre-established biofilms The control biofilms exhibited 30.2 ± 0.9 μm thickness after 3 days of incubation (Fig. 2a). After treatment with the plant extract, the thickness of preformed P. aeruginosa biofilms was reduced with increasing contact time to reach 10.9 ± 0.8 μm after 120 min. The presence of red fluorescence indicated the presence of dead cells throughout biofilms which have increased significantly with increasing time of treatment (Figs. 2b, c and d). These findings suggested that active compounds in the plant extract had a dual-action: (i) prevent the biofilm formation, (ii) disintegrate the biofilm architecture and kill the sessile bacteria.

Fig. 3. Variations of (a) OCP and (b) characteristic corrosion rate (1/Rp) vs. time during the 14 days of incubation in the abiotic, biotic and inhibited media. ( Biotic medium; Inhibited medium)

Abiotic medium;

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Fig. 4. Nyquist and Bode plots of 304L SS in (a, a’) abiotic, (b, b’) biotic and (c, c’) inhibited media after 1, 4, 7, 10 and 14 days of incubation. ( 1d; 4d; 7d; 10d;

14d; –––Fitted curves)

Table 3 EIS fitting results of 304L SS in abiotic medium. Day

Rs (Ω cm2)

Co (μF cm−2)

Ro (Ω cm2)

Cf (μF cm−2)

Rf (kΩ cm2)

Cdl (μF cm−2)

Rct (kΩ cm2)

Χ2 × 10−3

1 4 7 10 14

12.4 ± 3.3 12.9 ± 3.9 12.6 ± 3.7 11.3 ± 3.2 11.5 ± 3.3

9.9 ± 0.4 9.1 ± 0.1 9.0 ± 0.1 9.1 ± 0.3 9.8 ± 1.1

246 ± 48 284 ± 75 301 ± 89 278 ± 92 269 ± 110

11.2 ± 0.1 9.8 ± 0.3 9.4 ± 0.6 9.3 ± 0.8 10.6 ± 2.2

7.1 ± 0.8 8.9 ± 2.1 9.3 ± 2.6 9.3 ± 2.7 8.5 ± 3.0

15.1 ± 1.4 12.4 ± 0.3 11.7 ± 0.1 11.4 ± 0.6 13.6 ± 2.9

1744 ± 412 2362 ± 277 2589 ± 198 2529 ± 103 2106 ± 152

6.5 ± 0.3 5.7 ± 0.1 5.4 ± 0.1 5.4 ± 0.1 5.3 ± 0.2

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199

when θw b65°. Based on this, the hydrophobicity can be assessed qualitatively. Therefore, the approach of Van Oss et al. [40] was used to evaluate the hydrophobicity degree quantitatively. Table 2 shows the contact angles and surface energy components of the coupon surfaces before and after treatment with the S. officinalis extract. It can be seen that before the treatment, the 304L SS coupon surfaces were hydrophobic (θw N 65°, ΔGiwi b 0). After treatment, the water contact angle values decreased from 77.0 ± 0.8° to 23.2 ± 0.1°. Meanwhile, the values of ΔGiwi increased from −40.3 ± 2.6 mJ/m2 to 26.8 ± 0.2 mJ/m2, these changes suggested a modification in the hydrophobicity of the surfaces which became hydrophilic. Table 2 shows that the electron acceptor character (γ+) of the 304L SS treated surfaces increased slightly, while the donor electron character (γ−) increased significantly from 10.9 ± 0.8 mJ/m2 to 49.5 ± 0.1 mJ/m2. 3.5. Electrochemical data Fig. 5. Potentiodynamic polarization curves of 304L SS coupons in the abiotic, biotic and inhibited media after 14 days of incubation. (––– Abiotic medium; Biotic medium; Inhibited medium)

3.4. Contact angle and surface energy components Contact angle technique is a tool to indicate the hydrophobicity of material surfaces. According to Vogler [47], a surface is hydrophobic if the water contact angle (θw) is larger than 65°, and it is hydrophilic

3.5.1. OCP and corrosion rate results Fig. 3a shows the OCP evolution of 304L SS immersed in the three media during the 14 days of incubation. The OCP of the biotic medium shifted considerably to a negative direction and reached −573 ± 8 mV vs. SCE after 1 day of incubation. Then, OCP continuously decreased until the 6th day and remained stable at approximatively −595 ± 11 mV vs. SCE. After the 11th day, OCP started to increase slightly until the end of the experiment. On the contrary, OCP values remained relatively constant in the abiotic medium throughout the

Fig. 6. Largest pit depth measured by CLSM on 304L SS coupon surfaces after 14 days of incubation in: (a) abiotic, (b) biotic and (c) inhibited media.

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Table 4 EIS fitting results of 304L SS in biotic medium. Day

Rs (Ω cm2)

Qb (10−6 Ω−1 Sn cm−2)

nb

Rb (Ω cm2)

Qdl (10−6 Ω−1 Sn cm−2)

ndl

Rct (kΩ cm2)

Χ2 × 10−3

1 4 7 10 14

8.6 ± 0.3 8.3 ± 0.4 8.4 ± 0.5 8.3 ± 0.8 9.0 ± 0.7

37.4 ± 3.5 34.7 ± 4.8 38.2 ± 1.0 37.3 ± 0.3 34.2 ± 0.5

0.86 ± 0.03 0.83 ± 0.01 0.82 ± 0.01 0.81 ± 0.02 0.81 ± 0.01

76.5 ± 50.0 189 ± 45 311 ± 60 375 ± 100 707 ± 281

12.3 ± 7.7 8.7 ± 3.6 4.9 ± 0.6 5.3 ± 0.3 5.0 ± 0.7

0.87 ± 0.01 0.93 ± 0.04 0.98 ± 0.01 0.97 ± 0.01 –

122 ± 65 54.6 ± 5.6 52.1 ± 4.3 59.3 ± 3.1 92.1 ± 14.9

1.1 ± 0.7 2.1 ± 0.1 2.1 ± 0.1 1.8 ± 0.2 1.6 ± 0.6

Table 5 EIS fitting results of 304L SS in inhibited medium. Day

Rs (Ω cm2)

Qp (10−6 Ω−1 Sn cm−2)

np

Rp (kΩ cm2)

Cdl (μF cm−2)

Rct (kΩ cm2)

Χ2 × 10−4

1 4 7 10 14

11.3 ± 0.1 11.7 ± 0.4 11.6 ± 0.7 11.5 ± 0.9 11.6 ± 1.3

64.1 ± 12.6 69.9 ± 21.9 61.2 ± 12.3 60.6 ± 13.7 64.2 ± 10.0

0.78 ± 0.01 0.77 ± 0.04 0.80 ± 0.01 0.81 ± 001 0.81 ± 0.01

54.8 ± 8.9 65.5 ± 32.7 61.0 ± 25.1 69.1 ± 30.6 57.4 ± 18.5

31.3 ± 6.0 26.6 ± 5.2 27.3 ± 5.1 25.6 ± 3.4 24.2 ± 4.4

998 ± 124 1507 ± 763 1328 ± 544 1474 ± 431 1777 ± 685

6.5 ± 2.0 5.5 ± 4.0 8.5 ± 6.5 3.8 ± 2.6 4.8 ± 2.4

period of exposure. Whereas, the OCP in the inhibited medium shifted gradually towards more positive values and remained constant after 9 days of incubation at approximatively 162 ± 6 mV vs. SCE. Polarization resistance (Rp) is an important parameter to evaluate the corrosion rate qualitatively, a higher Rp corresponds to a lower corrosion rate. Fig. 3b exhibits the variation of the characteristic corrosion rate (based on 1/Rp), during 14 days of incubation in the three media. It can be seen that the corrosion rates tendency of 304L SS coupons exposed to bacterial medium were higher (14-fold) than that of the abiotic control, suggesting an acceleration in corrosion rate tendency by P. aeruginosa. In contrast, the corrosion rate tendency in the inhibited medium was reduced by approximatively 20-fold compared to the untreated biotic working electrode. This suggests that the inhibition of MIC by S. officinalis extract was impressive. 3.5.2. Electrochemical impedance spectroscopy results Fig. 4 shows Nyquist and Bode plots for 304L SS in the abiotic, biotic, and inhibited media at different immersion times. Equivalent electrical circuits (Fig. S2) were obtained by analyzing the impedance spectra of the samples. The three-time constant model, Rs(Co (Ro (C fRf)(Cdl Rct))), was used to fit the EIS data in abiotic medium. The two-time constant models Rs (Q b (Rb (Q dl Rct ))) and Rs(Q b (R b (CdlRct))) (applicable to 14-day data) were used for the 304L SS coupon in biotic medium. The two-time constant model Rs (Q p R p ) (CdlRct) was used for the inhibited medium. In these circuits, Rs represents the solution resistance. Cf and Rf are the capacitance and the resistance of the passive film, respectively. Co and Ro stand for the capacitance and the resistance of the conditioning film, respectively, which is the result of the adsorption of the organic compounds present in the medium. Q b and Rb represent the capacitance and the resistance of the biofilm and the corrosion product film, respectively. Q p and Rp are the capacitance and the resistance of the protective film formed due to the adsorption of the S. officinalis extract compounds on 304L SS surfaces, respectively. Q dl and Rct represent the double layer capacitance and the charge transfer resistance, respectively. Table 3 to 5 show the quantitative fitting parameters of EIS measurements in the abiotic, biotic and inhibited media,

Table 6 Corrosion parameters from the polarization curves for 304L SS in the biotic, abiotic and inhibited media after 14 days. Sample

icorr (μA cm−2) Ecorr (V) vs. SCE Epit (V) vs. SCE IE (%)

Abiotic medium 0.22 ± 0.09 Biotic medium 6.19 ± 1.28 Inhibited medium 0.06 ± 0.02

−0.30 ± 0.10 −0.73 ± 0.04 0.14 ± 0.01

0.63 ± 0.18 0.13 ± 0.24 0.74 ± 0.16

– – 97.5 ± 1.5

respectively. Rf increased slightly with exposure time and reached a maximum of 9.3 ± 2.6 kΩ cm2 after 7 days of incubation in the abiotic medium indicating the good stability of the passive film on 304L SS in the 2216E sterile medium. The Rct values exhibited a similar trend to those of Rf during incubation. In contrast, the Rct values in the biotic medium decreased with exposure time and reached a minimal value of 52.1 ± 4.3 kΩ cm 2 on the 7th day, confirming the accelerated corrosion rate in the presence of P. aeruginosa. After the 10th day, the values of Rct underwent an increase to reach 92.1 ± 14.9 kΩ cm2 after 14 days of incubation. In the inhibited medium, the Rct values were significantly higher compared to the biotic medium and increased with increasing time to reach a value of 1777 ± 685 kΩ cm2 on the 14th day. The values of Cdl started to decrease gradually from 31.3 ± 6.0 μF cm−2 at the 1st day to reach 24.2 ± 4.4 μF cm−2 at the 14th day. 3.5.3. Potentiodynamic polarization measurements Potentiodynamic polarization was used to evaluate the corrosion rates of 304L SS exposed to the abiotic, biotic and inhibited media. The obtained curves after exposure for 14 days are presented in Fig. 5, and electrochemical parameters icorr, corrosion potential (Ecorr), pitting potential (Epit) and inhibition efficiency were calculated and summarized in Table 6. It can be observed in Fig. 5 that the polarization curve shifted to a larger current density region and Ecorr moved to the negative direction in the presence of P. aeruginosa which confirmed the conclusion drawn from other electrochemical techniques above that the bacterial P. aeruginosa accelerated the corrosion rate of 304L SS. In the presence of the extract, Ecorr and Epit values shifted in the positive direction for about 0.14 ± 0.01 V vs. SCE and 0.74 ± 0.16 V vs. SCE, respectively, compared to the biotic medium. Moreover, the icorr values were much smaller than that in the biotic medium which indicated an excellent MIC inhibition efficiency of the S. officinalis extract which reached 97.5 ± 1.5%. 3.6. Analysis of pit depth Fig. 6 shows the CLSM images of the pits formed on the 304L SS coupon surfaces after 14 days of incubation in the three media. The coupon surface in the abiotic medium were relatively smooth and the average pit depth was 1.8 ± 0.6 μm. In the biotic medium, the largest pit depth on the coupon surfaces reached 13.2 μm and the average pit depth was 10.7 ± 3.1 μm, which suggests that P. aeruginosa accelerated the pitting corrosion of this material. The coupons incubated in the inhibited medium showed an absence of pits on the surface. This finding confirmed the excellent corrosion protection by the plant extract.

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Fig. 7. SEM images of P. aeruginosa cells and biofilm after exposure to: (a) biotic medium and (b) inhibited medium, after 14 days of incubation.

4. Discussion It is well known that biofilms are responsible for microbial corrosion [48,49]. The CLSM images show that P. aeruginosa formed patchy biofilms on the 304L SS coupon surfaces after 1 day of incubation which started to increase in thickness and density to reach 40.9 ± 1.7 μm after 14 days (Figs. 1a, b and c). The colonization of 304L SS by biofilms was accompanied by its changing electrochemical behavior. The decrease in the OCP values after 1 day of incubation in the biotic medium could be attributed to the activity and growth of P. aeruginosa biofilms [50]. The increase of OCP after the 11th day was due to the formation of corrosion products on the metal surface [51]. This was in agreement with the increase in the resistance of biofilms and the corrosion product film (Rb) during the incubation time, from 76.5 ± 50.0 Ω cm2 at the 1st day to 707 ± 281 Ω cm2 on the 14th day (Table 4). The corrosion parameters obtained from the polarization curves confirmed the EIS data trends. The negative shift of Ecorr and the larger value of icorr compared to those in the abiotic medium indicated an acceleration of the corrosion rate of 304L SS in the presence of P. aeruginosa. This increase could be due to the creation of aeration cells because of the heterogeneous biofilms formed on the metal surface [51]. Moreover, the presence of Cl− in the 2216E medium (1.7%) facilitated the formation of localized

corrosion on the metal surface. This is consistent with the pit depth analysis of 304L SS coupon surfaces incubated in the abiotic medium, which showed the presence of small pits on the coupon surfaces (Fig. 6a). The synergistic effect of P. aeruginosa and Cl− present at the metal/solution interface might explain the initiation of 304L SS pitting corrosion. Furthermore, the secretion of phenazines by P. aeruginosa accelerated the corrosion by mediating electron transfer between the metal surface matrix and sessile cells [11,15]. Aromatic and medicinal plants have sophisticated defense mechanisms that give them the necessary protection in their ecosystems. Therefore, they constitute a rich source of bioactive compounds that have been widely studied for their antimicrobial and anticorrosion activities [52,53]. In this study, the HPLC-Q-TOF-MS results showed that the S. officinalis extract contained different types of active compounds mainly belonging to the phenolic family. The adsorption of these compounds on the 304L SS coupon surfaces was confirmed by the contact angle measurement which showed a decrease in the hydrophobicity (77.0 ± 0.8 to 23.2 ± 0.1°) and an increase in the electron donor character (10.6 ± 0.8 to 49.5 ± 0.1 mJ/m2) of this surface after treatment with the extract (Table 2). These phenolic compounds in their functional groups contain different elements such as, O, N and S which are well known for their high basicity and electron density. In fact, the increase in the electron donor character of a surface makes it more

Scheme 1. Illustration of corrosion acceleration of 304L SS in the presence of P. aeruginosa and MIC inhibition mechanism by S. officinalis extract.

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negatively charged. Therefore, the adhesion of bacteria on the surface decreased after the extract treatment and hence the biofilm formation was inhibited. This was confirmed experimentally by CLSM and SEM analyses (Figs. 1 and 7) which showed an inhibition of biofilm formation on the coupon surfaces during the period of incubation in the presence of the extract. These results are in agreement with previous data obtained by Sadiki et al. [42], wherein Thymus vulgaris extract fractions, modified the physic-chemical properties of cedar wood (decreased hydrophobicity and increased electron donor character) and thereby reduced the attachment of Penicillium spores on this surface. In the inhibited medium, OCP and Ecorr both underwent a positive shift, while icorr decreased compared to the biotic medium. This trend in OCP in the presence of the extract have been reported in previous studies for other plant extracts. Shabani-Nooshabadi and Ghandchi [54] found that the OCP values of 304 SS shifted positively and the corrosion rate was reduced in the presence of a Santolina chamaecyparissus extract. EIS results also confirmed this MIC inhibition, the variation of Rct and Qdl could be attributed to the displacement of water molecules and other ions originally adsorbed on the coupon surfaces by the molecules in the S. officinalis extract leading to the formation of a protective layer that inhibited the bacterial adhesion and decreased the active sites needed for the MIC process [30,54]. This protective layer inhibited the formation of pits on the surface of 304L SS coupons as shown in Fig. 6. The 304L SS coupon surfaces were found to be mostly covered by P. aeruginosa biofilms after 14 days of incubation in the biotic medium (Fig. 7.a). The bacterial cells showed rod shaped, smooth and intact morphology. After exposure to S. officinalis extract, the SEM images showed significant morphological alterations of bacterial cells (Fig. 7. b). The cell membrane of bacteria was gradually degraded and the cell contents were leaked. Similar morphological features have also been observed for other bacteria when treated with aromatic and medicinal plants [55–57]. These data suggested that the antimicrobial mechanism of the S. officinalis extract was by acting on the membrane integrity of P. aeruginosa cells. It is known that active compounds from aromatic and medicinal plants can inhibit the bacterial growth and biofilms via other mechanisms such as reducing production of important quorum sensing regulated virulence factors [58] and down-regulating the expression of critical genes involved in formation of biofilms [38]. All these mechanisms could possibly explain the way by phenolic compounds in the investigated extract which inhibited the growth and the biofilm formation of P. aeruginosa. Scheme 1 illustrates the 304L SS behaviors in the biotic and inhibited media. 5. Conclusion This study revealed that S. officinalis extract compounds possess excellent biocidal and corrosion inhibition properties for stainless steel type 304L against the corrosive P. aeruginosa biofilm. The HPLC-Q-TOF-MS results revealed that the major compounds of the extract belonged to phenolic and oxylipins families. The adsorption of these compounds decreased the hydrophobicity and increased the electron donor character of the 304L SS coupon surfaces. The data obtained from CLSM and electrochemical studies confirmed the protection of the coupon surfaces against pitting corrosion. To the best of our knowledge, this is the first study reporting the antiMIC activity of S. officinalis leaves extract. Accordingly, these findings present a scientific basis to promote the value-added of the active compounds from this extract as eco-friendly and inexpensive inhibitors for the prevention of MIC. Acknowledgement This work was supported by the National Natural Science Foundation of China (Nos. U1660118 and 51871050), the Fundamental Research Funds for the Central Universities of Ministry of Education of

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