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The influence of Bacillus subtilis on tin-coated

Cite this: RSC Adv., 2018, 8, 4671
copper in an aqueous environment
Open Access Article. Published on 25 January 2018. Downloaded on 26/01/2018 00:57:43.

Ruilin Xiong,†a Kui Xiao, †*a Pan Yi,a Yuting Hu,a Chaofang Dong, a
Junsheng Wua
and Xiaogang Liab

The influence of Bacillus subtilis (BS) on tin-coated copper in an aqueous environment was investigated by
exposing the sample to a culture medium inoculated with BS. Scanning electron microscopy,
electrochemical measurements and chemical analyses were performed to study the corrosion
mechanism. The experimental results show that BS can adhere and gather on the surface of the sample,
Received 17th July 2017
Accepted 10th January 2018
resulting in oxygen consumption at the place where the bacteria are densely attached. Increases in the Rct
values after the initial immersion showed that corrosion was inhibited, while decreases in the Rct values
DOI: 10.1039/c7ra07864a
after the later immersion showed that corrosion was accelerated. Our results suggest that differences in
rsc.li/rsc-advances oxygen concentration due to activity of BS are the main reason for corrosion of tin-coated copper.

by BS in the initial corrosion of CRS in AS. The protection effect

1. Introduction of the biolm predominates later in the process because the
Copper is a common material widely used in residential, biolm can consume oxygen and produce a metabolic product
commercial and industrial plumbing devices due to its useful that acts as a corrosion inhibitor for the CRS. Jayaraman et al.24,25
properties.1 However, copper suffers from corrosion damage studied the corrosion inhibition of carbon steel coupons
due to chlorides, sulphides, particulates and microorganisms in immersed in a complex liquid medium (LB broth) and
its environment.2–5 Coating copper with another kind of metal a synthetic seawater (VNSS) medium with seven diverse bacterial
can improve its conductivity and welding properties. Coating genera through oxygen depletion. It is possible that the different
copper with tin by using hot air solder levelling, as was per- culture media led to different bacterial distributions and
formed in this study, is widely applied in the fabrication of different corrosion mechanisms in Javed's studies.26
commercial electronic devices because of the low cost, good The aim of this study was to try to investigate the inuence of BS
solderability, and reliability of tin.6 on the corrosion behaviour of copper with a tin coating. BS is the
Although copper has some antimicrobial properties, micro- predominant strain separated from the surface of tin-coated
bial corrosion of copper still occurs.7–9 Bacillus subtilis (BS) has copper exposed to an atmospheric environment in Xishuang-
been studied in recent years because it has been isolated from banna. To clearly illustrate the effects of the biolm on the corro-
many damaged industrial devices.10–14 Yang et al.15–17 found that sion behaviour of the tin-coated copper, a sodium nitrate culture
microorganisms can attach to and destroy communication medium was used to assess the corrosion effects of chloride.
equipment and circuit boards, and BS is the predominant strain Tryptone in the LB culture medium was dissolved into ammonia
found on corroded surfaces. Currently, microbial corrosion due during the bacterial metabolism process, and the alkaline envi-
to BS on steel and alloys is being studied.18–21 Zuo22 studied the ronment protected the sample from the acidic environment. X-ray
corrosion behaviour of Al 2024 exposed to articial seawater (AS) photoelectron spectroscopy (XPS) and energy-dispersive spectrom-
in the presence of a protective biolm of BS WB600 and found etry (EDS) in this experiment were used to analyse the corrosion
that the corrosion protection of Al 2024 in AS occurs only in the products of tin and copper in the presence of BS. Scanning envi-
presence of a live biolm. This is because the negatively-charged ronmental microscopy (ESEM) and uorescence microscopy (FM)
bacteria cause the biolm to repel chloride ions, thereby were used to characterise the corrosion morphology. Electro-
increasing the Epit. Qing23 demonstrated that the corrosion of chemical impendence spectroscopy (EIS) was performed to eval-
cold rolled steel (CRS) is accelerated by the lactic acid produced uate the effects of BS on the corrosion behaviour of the sample.

a
Corrosion and Protection Center, University of Science and Technology Beijing, 2. Experimental methods
Beijing, 100083, P. R. China
2.1 Materials
b
Ningbo Institute of Material Technology & Engineering, Chinese Academy of Sciences,
Ningbo, 315201, P. R. China The sample was nished by coating the surface with lead-free
† These authors contributed equally to this work. spray tin and levelling it with heated and compressed air. The

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cross-sectional view of the sample is presented in Fig. 1. The tin of green uorescent dye (SYTO-9), which easily stains live cells,
layer was 1.4 mm thick. Each specimen was sterilised in a 75% and 3 mL of iodinated pyridine (PI), which stains dead cells, were
ethanol solution for 2 h and then exposed to UV light for 30 min mixed into a mixture when staining. Images of the specimens
prior to use. with immobilised bacterial cells were taken at 100 magni-
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The culture medium consisted of the following components: cation using an inverted uorescence microscope (DSY5000)
10 g L 1 of tryptone, 5 g L 1 of yeast extract, and 10 g L 1 of equipped for epiuorescence with a mercury lamp. The live cells
NaNO3. The solution was sterilized by autoclaving it for 20 min exhibited green uorescence and the dead cells exhibited red
at 121  C at 100 kPa. uorescence.
BS was isolated and puried from the corrosion area of the
tin-coated copper, which was exposed to a semi-enclosed 2.4 Growth curve measurement
atmospheric environment in Xishuangbanna for a month. The
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BS was inoculated in an Erlenmeyer ask with 50 mL of steri- Growth curve experiments were performed to determine the
lised culture medium and incubated at 37  C. The initial cell growth tendency of BS in culture medium. BS was inoculated in
concentration of the BS was adjusted to approximately 106 cells a 50 mL Erlenmeyer ask with sterile culture medium and was
per mL. active cultured for 10 h. Three 100 mL samples of culture
medium were sucked inside a 1.5 mL EP tube. 200 mg L 1 of
Cu2+ was added to one sample, and 200 mg L 1 of Sn4+ was
2.2 Elemental analysis (XPS) added to another sample. 2 mL of active cultured BS medium
For the elemental analysis, the specimens were quickly removed was added to the 1.5 mL EP tube. Next, the 1.5 EP tube was
from the culture media aer immersion for 14 days and gently placed into an automatic growth curve analyser (Bioscreen C).
rinsed three times with sterilised water. Aer blow-drying with The automatic growth curve analyser measured the turbidity of
pure nitrogen, the specimens were stored in an airtight vacuum the sample and automatically detected the optical density (OD)
desiccator prior to use. of the medium inoculated with BS at 30  C.
Scanning electron microscopy (SEM, FEI Quanta 250) was
used to observe the morphology of the surface corrosion, and 2.5 Surface morphology
energy-dispersive spectrometry (EDS) analysis was used to
determine the composition of the corrosion products. Each sample was immersed in media, both with and without BS
Elemental mapping of the enlarged map was used to obtain the inoculation, in a 37  C incubator. Aer immersion for 7 and 14
distribution of elements on the surface. X-ray photoelectron days, the samples were taken out and washed with PBS solution
spectroscopy (XPS) measurements were obtained on an X-ray to remove the oating bacteria. The samples were then
photoelectron spectroscope (Thermo escalab 250Xi). immersed in 2.5% glutaraldehyde for 10 hours and dehydrated
using a series of aqueous ethanol solutions (15%, 30%, 50%,
70%, 95% and 100%) for 15 min each. They were then coated
2.3 Fluorescence microscopy (FM) with gold, and observed using eld emission environment
Aer exposure to the culture medium inoculated with BS and scanning electron microscopy (QUANTA FEG 250, USA).
without renewing the media for 7 and 14 days in the 37  C
incubator, the sample was taken out and washed twice with 2.6 Electrochemical measurements
sterile phosphate buffered saline (PBS) solution to remove the
A three-electrode system including a working electrode, an
dead and loosely attached bacteria. The samples were then
auxiliary electrode and a reference electrode was used for the
stained with a colouring agent called Live-Dye for 15 min. 3 mL
electrochemical measurements. The working electrodes were
made of tin-coated copper, connected with copper wire and
mounted in silica gel with an exposed area of 1.2 cm2. They were
then washed twice with sterile water, sterilised with 75%
ethanol solution for 2 h and nally exposed to UV light for
30 min to further sterilise them. The auxiliary electrode
comprised platinum foil, and the reference electrode was
a saturated calomel electrode (SCE) with a lugging capillary
positioned close to the working electrode surface in order to
minimise ohmic potential drop.
EIS measurements were conducted at the end of the open
circuit potential (OCP) with a frequency range of 0.01–105 Hz
using a PAR2273 advanced electrochemical system from
Princeton Applied Research. All experiments were performed in
the culture medium in an incubator. The experimental
temperature was kept at 37  C throughout the entire process
using a thermostatically controlled water tank. Each experiment
Fig. 1 Cross-sectional view of the sample. was repeated at least three times to ensure reproducibility.

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3. Results and discussion

3.1 Surface chemical analysis
Fig. 2 shows the wide-scan XPS results for the sample surfaces
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aer immersion in culture media with BS for 14 days. The tin

peak of the sample surface aer immersion in culture media
with BS for 14 days appeared as shown in Fig. 2a, but the copper
peak did not. This indicates that the copper substrate of the
sample did not corrode aer immersion in sterilised culture
media, but the copper substrate of the sample did corrode aer
immersion in culture media with BS. Fig. 2b shows that the Fig. 3 SEM image of the surface of the sample immersed for 14 days.
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corrosion product under the sterile aqueous environment was

SnO2. The corrosion products under the aqueous environment
with BS were SnO2 and copper oxide. Cu(I) existed mainly in the Table 1 EDS of tin-coated copper after immersion for 14 days as
form of Cu2O, while Cu(II) was mainly in the form of CuO. The shown in Fig. 5 (at%)
presence of Cu2O indicates that the copper was not completely
Element C Cu Na O P Sn
oxidised, which can be seen in Fig. 2d. The XPS results
demonstrate that the tin-coated copper under the aqueous A 23.75 6.28 5.86 43.00 03.20 17.91
environment with BS was damaged more severely. B 29.98 27.96 0.99 14.69 0.26 26.11
Fig. 3 shows the SEM image of the sample surfaces aer
immersion in culture media with BS for 14 days. The RACE
(relative atomic concentrations of elements) values of the The amount of carbon and phosphorus found in the corro-
surfaces are summarised in Table 1. Fig. 4 shows that the sion products on the sample under the sterile aqueous envi-
surface contained the elements P, C, N, Sn, O, Cu, and Na. ronment was minimal, but the amount of carbon and
Phosphorus may have originated from the metabolites of the phosphorus found in those under the aqueous environment
bacteria. Carbon and nitrogen may have originated partly from with BS was large. This implies that the corrosion products from
the metabolites and partly from the culture medium. the sample immersed in BS mainly originated from the

Fig. 2 Wide-scan XPS spectra (a) and high-resolution XPS spectra observed for the surface of the tin-coated copper exposed to sterile (b) and
Bacillus subtilis (c and d) media for 14 days.

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Fig. 4 EDS mapping results of (a) C, (b) Cu, (c) Na, (d) O, (e) P, and (f) Sn (at%).

metabolites of the bacteria. Sodium mainly originated from the 14 days (c and d). From the image of the sample immersed for 7
sodium salt in the culture medium. The elemental mapping days, it can be seen that only a few live bacteria along with some
results in Fig. 4a and e show that the metabolites were widely dead bacteria were attached to the material surface. The surface
distributed on the surface of the sample. Sn and Cu were the of the tin-coated copper was covered with small pits. From the
base elements of the sample. The amounts of oxygen and tin in surface image of the tin-coated copper immersed for 14 days, it
A were much higher than those of the other elements, which can be seen that more bacteria were attached to the sample. BS
indicates that more water-insoluble tin oxide was generated. covered the surface in layers and gradually aggregated into
a thick biolm within an extracellular matrix containing poly-
saccharides, proteins and nucleic acids. The pitting gradually
3.2 Bacterial colonisation study with FM expanded, and the surface of the sample showed large corrosion
Fig. 5 shows the uorescence images of the tin-coated copper product particles with many live and some dead bacteria accu-
under the aqueous environment with BS for 7 days (a and b) and mulated on the material surface.

Fig. 5 Fluorescence images of bacterial colonies on the sample in the culture media after 7 days (a and b) and 14 days (c and d).

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3.3 Surface morphology with BS for 14 days, as shown in Fig. 6e and f. When the corro-
sion products were removed, there were some larger holes on the
Fig. 6 shows the SEM images of the sample aer immersion in
sample under the aqueous environment with BS for 14 days, as
sterile culture medium for 14 days and with BS for 7 and 14 days.
shown in Fig. 6h. A more serious corrosion phenomenon was
No signicant cracks or corrosion pits appeared on the surface of
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observed on the sample under the aqueous environment with BS

the sample under the aqueous environment with BS for 7 days.
(Fig. 6h) compared to the sterile aqueous environment (Fig. 6g).
Some bacteria surrounded by a small porous agglomeration of
corrosion products were attached on the surface of the sample.
There were also some small pits on the surface of the sample. 3.4 EIS results
More and more bacteria and corrosion products attached EIS is frequently used as a non-destructive technique to study
themselves onto the sample under the aqueous environment electrochemical reactions at metal/biolm interfaces, as well as
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Fig. 6 SEM images of the tin-coated copper exposed to sterile culture medium for 14 days (a and b) and culture medium with BS for 14 days (c
and d) and 7 days (e and f). SEM images of the sample exposed to the sterile culture medium with removal of the corrosion products and culture
medium with BS for 14 days (g and h).

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Fig. 7 EIS of the tin-coated copper immersed for different times in the Fig. 8 EIS of the tin-coated copper immersed for different times in the
sterile culture medium at 37  C: (a) Nyquist plot, (b) Bode modulus culture medium with BS at 37  C: (a) Nyquist plot, (b) Bode modulus
diagram and (c) Bode phase angle diagram. diagram and (c) Bode phase angle diagram.

Table 2 Fitting parameters of the impedance spectra of tin-coated copper in sterile medium

T
(day) Rs Qf N1 Rf Qp N2 Rp Qdl N3 Rct pH

1 17.04 1.635  10 5
0.896 3.008  104 6.97
4 15.48 1.574  10 5
0.9008 5.145  104 6.803  105 0.8331 4.942  104 6.92
7 16.32 0.000153 0.6923 3.982  104 1.328  10 5 0.9279 8.32  104 7.01
14 17.91 0.0001555 0.7592 82.24 1.651  10 5 0.8516 1.579  105 7.05

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the formation of corrosion products and biolms in microbial

corrosion.27,28 EIS results and the tting parameters of the
impedance spectra of the tin-coated copper under the sterile
aqueous environment are shown in Fig. 7 and Table 2. In
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addition, the EIS results and the tting parameters of the

impedance spectra of the tin-coated copper under the aqueous
environment with BS are shown in Fig. 8 and Table 3.
As shown in Fig. 7c and 8c, the Bode plot shows that one
time-constant was present when under the sterile aqueous
environment with and without BS for 1 day, which ts well with
the circuit (a) in Fig. 9. The Bode plot shows that two time-
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constants were present when under the sterile aqueous envi-

ronment without BS for 4 days, which is tted with the equiv-
alent electrical circuit (b) shown in Fig. 9. The physical model
(R(QR)(QR)) corresponding to Fig. 9b represents a layer of dense
oxide lm. As the immersion time increased, the oxide lm
became denser, hindering the transfer between the surface of Fig. 10 Growth tendency of BS in sterile culture medium.

the material and the solution. There is a single impedance loop

that increased in diameter in Fig. 7a, which is consistent with
the increase in the charge transfer resistance (Rct) in Table 2. shown in Fig. 8c, which shows that these metabolites hinder the
The Bode plots of the sample under the aqueous environ- corrosion process. More and more bacteria attached onto the
ment with BS for 4 days in Fig. 8c have two time-constants. The surface with time and the biolm was formed. The diameters of
corresponding equivalent circuit (R(Q(R(QR)))) in Fig. 9c the impedance loops in the Nyquist plots in Fig. 8a decreased
represents a layer of nonuniform lm. The attachment of within the rst 4 days and then markedly increased, indicating
bacteria on the surface is reversible in the beginning. The single that BS accelerates the corrosion process. The reduction in
impedance loop increased in diameter from 1 day to 4 days, as charge transfer resistance (Rct) and the increase in electric

Table 3 Fitting parameters of the impedance spectra of tin-coated copper in medium inoculated with bacteria subtilis

T
(day) Rs Qf N1 Rf Qb N2 Rb Qdl N3 Rct pH

1 16.68 1.416  10 5
0.8655 1.727  104 7.01
4 16.62 2.35  10 5
0.9267 7.006  104 3.306  10 5
0.5958 4.259  104 8.43
7 15.67 2.27  10 5
0.9284 4247 7.891  10 5
0.5018 1.208  104 8.73
14 18.73 0.0001197 0.7911 6708 0.003658 0.8257 1134 8.96

Fig. 9 Physical models and equivalent electrical circuits simulating the EIS diagrams based on (a) a single-layer model, (b) a double-layer model
and (c) a double-layer model.

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Fig. 11 Schematic diagram for the corrosion process of tin-coated copper in the culture media with Bacillus subtilis.

double layer capacitance (Qdl) indicate a decrease in resistance, 2Cu 2e / 2Cu+ (6)
which can be seen in Table 3. Rct is indicative of the magnitude
of the interface reaction resistance and is commonly used to 4Cu+ + 2OH / Cu2O + H2O (7)
characterise the rate of corrosion. The charge transfer resis-
tance (Rct) was less for the sample under the aqueous environ- Cu2O 2e + 2OH / 2CuO + H2O (8)
ment with BS than that in the sterile environment, indicating
that the sample under the aqueous environment with BS was
Corrosion products in the culture media with BS included
more susceptible to corrosion.
Cu(I), Cu(II) and SnO2. The copper was not completely oxidised,
which is probably due to the presence of copper ions. Copper
ions have a certain inhibitory effect on bacteria, which can be
3.5 Mechanism
seen in Fig. 10. The pH of the BS aqueous solution increased
Oxygen under the aqueous environment without BS loses elec- from 7.01 to 8.96 with immersion time, indicating that the
trons to produce hydroxide ions, and tin loses electrons to microbial acid production mechanism is not the main reason
produce tin ions. The hydroxide ions and the tin ions react and for the dissolution of the tin layer in the corrosion process.
form a tin oxide layer, which is insoluble in water. The tin oxide Differences in oxygen concentration are the main reason for
layer hinders the transfer between the solution and sample, corrosion. Another factor is the formation of the non-uniform
which results in the inhibition of the corrosion reaction. biolm layer, which contains aerobic bacteria, leading to
different oxygen concentrations. Another factor is that the bio-
O2 + 2H2O + 4e / 4OH (1) lm acts as a barrier, preventing the diffusion of oxygen to the
metal surface.
Sn 2e / Sn2+ (2)

Sn2+ + 2OH / Sn(OH)2 (3)

4. Conclusion
Sn(OH)2 + 2OH 2e / SnO2 + 2H2O (4)
This study focused on the corrosion behaviour of tin-coated
The corrosion process of the tin-coated copper has four copper caused by BS biolms. The eld emission and XPS
stages, which are shown in Fig. 11. The bacteria are reversibly data indicated that the tin layer of the sample, which can
adsorbed on the surface in the beginning, while some metab- improve the conductivity and welding properties of copper, was
olites are adsorbed on the metal surface, which inhibits corro- not complete anymore. The FM and the SEM images showed
sion. In the second stage, the metabolites are suitable for the that the BS adhered to the surface and aggregated into an
bacteria due to their hydrophilicity. In the meantime, the tin agglomeration. The EIS results show that the metabolites
ions on the metal surface do not affect the metabolism of the inhibited the corrosion process in the initial stage, while the
bacteria, which can be seen from the growth tendency of BS respiration of BS accelerated the corrosion process and the
under the aqueous environment aer adding 200 mg L 1 of tin oxygen-starved zone prior to corrosion. This study removed the
ions (Fig. 10). Lots of bacteria accumulate on the surface and possible inuence of acid production corrosion and the chlo-
the metabolism of bacteria causes a difference in the oxygen ride corrosion. Meanwhile, the effect of bacterial respiration on
concentration in this area with time. Prior corrosion occurs in the metal was revealed, especially when the biolm was
the area that is starved of oxygen. In the third stage, more considered to have the ability to hinder the corrosion process.
bacteria accumulate on the surface, which consume more However, the mechanisms behind the effects of the bacterial
oxygen and accelerate the corrosion process. metabolites on the sample are still unclear. Further study is
required to investigate the composition of bacterial metabolites
O2 + 2H2O + 4e / 4OH (5) and the role of the composition.

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12 T. M. Roane, K. L. Josephson and I. L. Pepper, Appl. Environ.

Conflicts of interest
Microbiol., 2001, 67, 3208–3215.
There are no conicts to declare. 13 G. O. Oyetibo, M. F. Chien and W. Ikeda-Ohtsubo, Int.
Biodeterior. Biodegrad., 2017, 120, 143–151.
This article is licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported Licence.

Acknowledgements 14 L. H. Chen, R. Han, H. Zhang, et al., Appl. Soil. Ecol., 2017,

113, 127–134.
This work was supported by the National Natural Science 15 Y. Hong, H. Yongqing and Z. Lantao, Manned Space Flight,
Foundation of China (No. 51671027 & 51271032 & 51131005); 2013, 19, 38–46.
National Basic Research Program of China (973 Program) (No. 16 L. Fei, Y. Hui and Z. Hui, Manned Space Flight, 2014, 5, 465–
2014CB643300); and the National Environmental Corrosion 473.
Platform (NECP). 17 B. Fanlu, W. Chuanfeng and Z. Lantao, Life Science
Open Access Article. Published on 25 January 2018. Downloaded on 26/01/2018 00:57:43.

Instruments, 2015, 3, 16–22.

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