Volume 6 Preprint 27
A Comparison of Biotic and Inorganic Sulphide Films on Alloy 400
J.S. Lee, R.I. Ray, and B.J. Little
Keywords: microbiologically influenced corrosion, nickel-copper alloys, sulphate reducing bacteria, sulphide attack
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Volume 6 Paper C057
A Comparison of Biotic and Inorganic Sulphide
Films on Alloy 400
J.S. Lee, R.I. Ray, and B.J. Little
Naval Research Laboratory, Code 7303 / 7330, Stennis Space Center,
MS 39529, email@example.com
Distribution, tenacity and chemical composition of sulphide films
produced by bacteria within biofilms were compared with those
produced by waterborne inorganic sulphides. Attempts were made to
differentiate corrosion mechanisms of alloy 400 (70Ni-30Cu) exposed
to seawater in the presence or absence of sulphate-reducing bacteria
(SRB). Experiments were conducted in an anaerobic environment in
the presence of inorganic sulphide and sulphate-reducing bacteria
(SRB) either freely corroding or coupled to an external cathode (alloy
400) exposed to air. Sulphur concentration in the films increased in
the presence of SRB as well as when samples were coupled to an
external cathode. Bacteria encrusted with corrosion products and
integrated into the sulphide film were only observed in the presence of
SRB in addition to coupling with an external cathode.
Keywords: microbiologically influenced corrosion, nickel-copper
alloys, sulphate reducing bacteria, sulphide attack
Determination of specific mechanisms for corrosion due to
microbiologically mediated oxidation and reduction of sulphur is
complicated by (1) the variety of potential metabolic/energy sources
and by-products, (2) the coexistence of reduced and oxidized sulphur
species, (3) competing reactions with inorganic and organic
compounds, and (4) the versatility and adaptability of microorganisms
in biofilms. The physical scale over which the sulphur cycle influences
corrosion varies with environment. As illustrated in Figure 1, the
complete sulphur cycle of oxidation and reduction reactions can take
place in macro (bulk) environments, including sewers and polluted
harbours or within the microenvironment of biofilms.
Figure 1. Possible reactions within a biofilm. Sulphur cycle highlighted.
Most of the literature on sulphide induced corrosion of copper and
nickel alloys does not differentiate between corrosion due to
waterborne sulphides and sulphides produced by sulphate-reducing
bacteria (SRB) within biofilms. The problem of accelerated corrosion of
copper/nickel and nickel/copper alloys by waterborne sulphides was
identified in the 1970’s and early 1980’s [1-3]. In most cases,
investigators used laboratory experiments in which 90/10 or 70/30
copper/nickel alloys were exposed to artificial or natural seawater with
sodium sulphide. Gudas and Hack  demonstrated that inorganic
sulphide films enhanced galvanic corrosion under some
circumstances. In the 1980’s, Syrett [5-7] demonstrated that
deaerated seawater containing dissolved inorganic sulphides did not
immediately lead to accelerated corrosion. Instead, a porous sulphide
corrosion product interfered with the formation of an oxide film on
subsequent exposures to oxygenated seawater. In the mid 1980’s
investigators recognized that most failures of copper and nickel alloys
in actual seawater service were related to in situ sulphide production
by SRB in biofilms.
Nickel/copper alloy 400 (Monel 400), nominally containing 66.5%
nickel, 31.5% copper and 1.25% iron, is used for seawater and brackish
water handling because of its resistance to chloride-ion stress
corrosion cracking and erosion corrosion. However, alloy 400 is prone
to pitting in chloride-containing environments where the passive film
can be disturbed. Under stagnant conditions chlorides penetrate the
passive film at weak points and cause pitting attack. Sulphides can
cause either a modification of the oxide layer as described for copper
or breakdown of the oxide film of nickel alloys. Pit initiation and
propagation depend on depth of exposure, temperature and presence
of surface deposits. Friend  established that nickel/copper alloys
containing more than 30% nickel formed a passive film similar in
structure to that formed on pure nickel. Localized corrosion of alloy
400 in seawater service is related to stagnation and/or intermittent
flow [9, 10].
Disk shaped alloy 400 coupons (1.58 cm diameter x 0.158 cm thick)
were purchased with an as-mill finish (Metal Samples, Munford,
Alabama, USA). Chemical composition provided with the samples can
be seen in Table 1. 100 cm long wire leads were electrically attached
to the back of the samples by carbon tape and silver adhesive.
Connections were strengthened by applying a bead of hot-glue.
Samples were embedded in EpoThin epoxy (Buehler Ltd, Lake Bluff, IL,
USA) with the bare surface facing down. The epoxy created a
watertight seal at the connections. Samples were wet-polished to a
1200 grit finish, sonicated in acetone for 5 minutes, rinsed with
ethanol, and blown dry with nitrogen gas.
Table 1. Chemical composition of alloy 400 in wt%.
Description of microbial cultures
SRB used in the current study have been described previously [10-12].
P10 - isolated from a 4140 steel coupon with a 5 step iron phosphate
primer (no topcoat) in a constant immersion flume tank (marine water)
at the Naval Surface Warfare Center (NSWC)/Ft. Lauderdale, FL.
P14 - isolated from a 4140 steel coupon with a 5 step iron phosphate
primer + an epoxy topcoat in a constant immersion flume tank
(marine water) at NSWC/Ft. Lauderdale, FL.
49Z - isolated from a 4140 steel coupon with a zinc primer (no
topcoat) in a constant immersion flume tank (marine water) at
NSWC/Ft. Lauderdale, FL.
CG59 - isolated from the seawater piping system of a surface ship at
Long Beach Naval Station, Long Beach, CA (marine water).
C130 - isolated from aluminium alloy with an epoxy primer +
polyurethane topcoat from moisture trapped under the cargo ramp of
a C-130 transport plane at the Naval Air Depot (Cherry Point, NC).
All isolates are positive for desulfoviridin (characteristic of
Desulfovibrio sp.). 100-ml stock cultures of SRB were maintained in
liquid growth medium (Postgate's B)  supplemented with NaCl (3%
w/v). Cultures were kept in glass bottles fitted with rubber septa and
aluminium crimped tops and were placed in glass canisters with an
anaerobic gas generating system (BBL™ Gas Pak Plus™; Becton
Dickinson Co., Sparks, MD) at 30°C until use.
Sulphide Concentration Measurements
Dissolved sulphide (S2-) was determined by the methylene blue method
. Briefly, 0.5 ml of an amine-sulphuric acid solution and 0.15 ml
of concentrated FeCl3 solution was added to 7.5 ml of fresh sample in
a clean cuvette. The mixture was capped and inverted one time. After
3 minutes, 1.6 ml of 50% (NH4)2HPO4 was added and the mixture
inverted one time. After 5 minutes, the cuvette was placed in a Hach
Model DR/2500 spectrophotometer (Hach Co., Loveland, CO) and S2-
concentrations were determined by a factory-installed program (#
690) for sulphide determination.
Three 1.5 litre glass jars were filled with 1350 ml of artificial seawater
(ASW) (35 ppt salinity, pH = 8.2). 150 ml of Postgate’s B media was
also added to make a suitable environment for bacterial growth. Jars
were labelled ‘+SRB’, ‘uninoculated’, and ‘aerobic’. In each of the first
two jars, two mounted alloy 400 samples were placed with the
exposed sample face in the vertical orientation. Three samples were
similarly placed in the aerobic jar. Nitrogen gas was bubbled through
the first two jars for 15 minutes to purge oxygen. The first two jars
were then placed in an anaerobic hood which contained an atmosphere
of 5% carbon dioxide, 10% hydrogen, and the balance nitrogen (Figure
2). A single saturated calomel reference electrode (SCE) was placed
inside the anaerobic chamber in a beaker of saturated KCl solution.
KCl salt bridges extending from each jar were placed into this beaker
for continuous solution conductivity between the jars. Each electrode
was connected to a data logger which measured the corrosion
potential vs. SCE every 10 minutes. No attempt was made to insure
sterile conditions throughout the experiment. The anaerobic chamber
was maintained at 30 ºC which has been shown to be the optimum
temperature for SRB growth [9, 15].
Figure 2. Schematic of the experimental set-up. Anaerobic chamber contained 5%
carbon dioxide, 10% hydrogen, and the balance nitrogen. A septum on the outside
wall of the anaerobic chamber provided access for wire connections and salt bridges
3 ml of each of the five SRB cultures were added to the +SRB jar.
Initial dissolved sulphide concentration in the bulk solution was
measured to be 3.67 ppm. An attempt was made to keep the initial
dissolved sulphide concentration of the two jars by adding 4 ppm Na2S
to the uninoculated jar for a final concentration of 3.72 ppm sulphide.
One sample from each jar in the anaerobic hood was electrically
coupled (by wire) to a corresponding sample in the ‘aerobic’ jar. After
40 hrs, bulk dissolved sulphide concentrations of the bulk solution
were measured: 4.17 ppm for +SRB, 0.57 ppm for uninoculated. 4
ppm Na2S was added to uninoculated jar for a final bulk concentration
of 3.67 ppm sulphide. Sulphide concentrations were taken again at t
= 68, 140, and 184 hrs (concentrations are listed in Figure 3). After
70 hrs the coupled anaerobic samples were disconnected from their
corresponding aerobic samples and left to freely corrode. At t = 184
hrs, all samples were removed, rinsed through a series of ASW and
distilled water dilutions to remove salts. Sample surfaces were
examined using an environmental scanning electron microscope
(ESEM), and corrosion products were characterized by energy
dispersive spectroscopy (EDS).
Figure 3 indicates the dependence of potential vs. time over the 184 hr
experimental duration. The non-coupled sample in the aerobic jar
(black curve) started at ~-550 mV and a rose to ~-300 mV over the
first 18 hours. For the duration of the experiment, potential values
(black curve) ranged from –275 to – 425 mV. The freely corroding (not
coupled) +SRB sample (blue curve) started at –600 mV, dropped to –
650 mV in the first day and remained between –650 and –700 mV for
the duration of the experiment. The freely corroding uninoculated
sample (orange curve) started at –640 mV, rose to –570 mV over the
first day, dropped to –650 mV when sulphide was added at t = 40 hrs,
and remained stable until the end of the experiment. Both coupled
samples, +SRB (green curve) and uninoculated (pink curve) initially
followed the potential rise of the aerobic sample (black curve) to –400
mV over the first 18 hours. At t = 18 hours the curves began to
diverge, with the aerobic sample rising to –300 mV, the +SRB curve
sample dropping to –650 mV and the uninoculated sample dropping to
–500 mV. At 40 hrs, the bulk dissolved sulphide concentration in the
uninoculated case was raised to 3.67 ppm and potential dropped to –
600 mV. Over the next 30 hrs, potential rose to –550 mV. At t=68
hrs, bulk sulphide concentrations of the +SRB and uninoculated cases
were 4.17 and 2.58 ppm respectively. Also at 70 hrs, the couples were
disconnected and both anaerobic samples potential immediately
decreased by 50 mV. Over the next day, the uninoculated sample
continued to drop to –650 mV at which time it followed the freely
corroding uninoculated sample (orange curve) out to the end of the
experiment, ending with potential of –640 mV. The +SRB sample also
follows this trend but matches +SRB sample which was freely
corroding with a final potential = ~-660 mV. Final dissolved sulphide
concentration in ppm was 1.54 (+SRB) and 1.06 (uninoculated).
Figure 3. Potential dependence and sulphide concentrations over the course of 184
hrs. Light blue line indicates when the couples were disconnected at 40hrs.
Sulphide concentrations (ppm) taken at t = 0, 40, 68, 140 and 184 are black
numbers with +SRB case on top and uninoculated case below.
At the conclusion of the experiment, each sample was examined
visually. +SRB samples had very dark and uniform surface deposits
which were very adherent, with the coupled sample being the darkest.
The uninoculated samples had patching dark surface deposits which
easily flaked off during removal of salts. As mentioned previously,
sterile conditions were not maintained in any way. This can be seen in
Figure 4, which includes ESEM micrographs of the freely corroding
samples in both +SRB and uninoculated conditions. Cells can be
readily seen in each picture as cylindrical dark spots indicating
microorganisms not associated with any corrosion products. The blue
arrow in the +SRB picture indicates an individual SRB identified by its
comma shape. Microorganisms can be seen in the uninoculated case
as well, but no attempt was made to determine the types. At low
magnification, both cases looked very similar with numerous bacteria
and the polishing lines still visible. At higher magnification differences
arose. In the +SRB case, the micrographs indicate that the surface is
completely vitrified and contained high contrast slivers (seen as white
lines). EDS indicated that the white slivers were of the same
composition as the surrounding darker deposit. In the uninoculated
case, the surface was covered with small, distributed deposits spread
over the surface. EDS determined the +SRB surface deposit to be
composed of 8% sulphur, while the uninoculated distributed deposits
consisted of 2% sulphur. It should be noted that none of the
microorganisms were coated by corrosion products.
Figure 4. ESEM micrographs and corresponding EDS of surface deposits after 184
hrs exposure to +SRB and uninoculated conditions with freely corroding samples
(not coupled) at two magnifications. Distribution, structure, and composition of
sulphides can be seen to be different for the two cases. Important to notice that the
sulphide concentration in the “+SRB’ was 4x larger than the uninoculated case. Blue
arrow indicates individual SRB. No encrusted cells seen.
Figure 5 includes ESEM micrographs of the initially coupled samples in
both +SRB and uninoculated conditions. At low magnification, cells
are seen as dark spots in each case indicating microorganisms not
associated with any corrosion products. In the +SRB case, large cracks
can be seen running through the surface deposit. In the uninoculated
case, a large deposit covering the left of the image can be seen with
corrosion products appearing from under the deposit. At higher
magnification in the +SRB case, the surface deposit appeared vitrified
with encrusted cells embedded in the deposit (blue arrow). In the
uninoculated case, the surface was covered with small, distributed
deposits spread over the surface with a large deposit covering the
bottom part of the image. EDS determined the +SRB surface deposit
to be composed of 16% sulphur, while the uninoculated distributed
deposits consisted of 9% sulphur. Notice the microorganisms in the
uninoculated case are associated with the corrosion products but are
Figure 5. ESEM micrographs and corresponding EDS of surface deposits after 184
hrs exposure to +SRB and uninoculated conditions initially coupled for the first 70
hrs at two magnifications. Distribution, structure, and composition of sulphides can
be seen to be different for the two cases. Sulphide concentration in the “+SRB’ has
increased to 16%. Blue arrow indicates individual SRB encrusted with corrosion
It is well established that alloy 400 is susceptible to SRB influenced
corrosion [9, 15, 16]. The process is as follows: as a result of
microbial respiration, SRB within a biofilm reduce the sulphate in
seawater (2 gm L-1) to sulphide. The sulphides react with the
copper/nickel oxides to produce a sulphur-rich layer. Sulphide layers
on alloy 400 form rapidly, causing acceleration in the corrosion rate
during its formation. Maxwell  and later Hamilton and Maxwell
 demonstrated the presence of SRB in anaerobic niches of biofilm
exposed to aerobic seawater. They surmised that upon exposure to
oxygenated flowing seawater the sulphide layer would peel away in
patches leaving bar metal exposed, thus creating an oxygen
concentration cell which would provide new metal for corrosion attack.
In this model, the aerated seawater supplies oxygen as a cathodic
reactant to push the corrosion rate higher. However, this is often
difficult to reproduce in the laboratory because of the unpredictability
of sloughing, and the subsequent destruction of the biofilm’s integrity.
It was with this idea that the current authors designed this experiment
in which cathodic current would be supplied remotely to a sample of
alloy 400 exposed to dissolved sulphides produced by SRB. This
experiment was designed to simulate the affect of oxygen on the
corrosion behaviour without removing the biofilm. Removal of the
couple after 40 hrs (thus removing the remote cathodic current) was
meant to simulate the decrease in oxygen as a closed environment
transforms from aerobic to anaerobic conditions.
Gouda et al.  studied the electrochemical behaviour of coppercontaining alloys in seawater exposed to sulphides and SRB. Using
polarization resistance (Rp) and anodic polarization scans, they
demonstrated that passivation of the metal surface occurred upon
initial exposure of alloy 400 to an SRB environment. As seen in Figure
3, ennoblement of the coupled samples followed the rising potential of
the aerobic sample over the first 18 hrs. While these data may indicate
passivation of the alloy 400 surface, they more likely indicate the
coupled samples were catholically controlled over this time (by the
aerobic electrode), corresponding with the build-up of dark surface
deposits seen on both “+SRB’ and “inoculated’ surfaces in the first 18
hours. This process seems to be independent of whether SRB are
present or not. However, at 18 hrs, differences are observed. The
+SRB potential drops from –440 mV down to –650 mV while the
uninoculated potential drops from –410 mV only down to –500 mV.
The difference in magnitude for the potential drops between +SRB and
uninoculated cases is possibly due to the formation of a patching SRB
biofilm in the +SRB case which allowed the sulphide concentration at
the metal/biofilm interface to increase, thereby, decreasing the
potential. In contrast, the uninoculated case which did not contain
intentionally inoculated SRB, would not decrease in potential as much
due to the lower sulphide concentration. Bulk sulphide concentration
increasing over the first 40 hrs in the +SRB case indicated the
presence of growing SRB and the presence of a dark surface film
indicates the incorporation of sulphide into the alloy 400 surface
oxide. However, dissolved sulphide concentration in the uninoculated
case declined steeply over the first 40 hrs indicating sulphide was not
being produced. It should be noticed that throughout the experiment,
the potential of the coupled +SRB case was always lower than the
coupled ‘inoculated’ case. This trend was also observed in the freely
Differences in sulphides produced by bacteria within biofilms and
waterborne inorganic sulphides were identified. Sulphide layers
formed in biofilms during exposure to ASW + SRB covered the entire
surface of the sample. In contrast, exposure to uninoculated ASW and
inorganic sulphides resulted in only localized sulphide deposits
covering a fraction of the metal surface. Sulphide layers formed in
biofilms were also more tenacious towards removal during rinsing with
distilled water than those formed in the uninoculated case. The
tenacity of the SRB sulphide layers may be due to the extra cellular
polymeric substances (EPS) produced within the SRB biofilm. EPS may
act as an adhesive that thereby strengthens the sulphide layer against
sloughing. Lee et al.  found similar results in the corrosion of alloy
400 in the presence of SRB.
Chemical composition of sulphide layers produced by exposure to
uninoculated and SRB containing seawater also differed. Figure 6
demonstrates the difference found in sulphur concentration between
the different cases. In the case of freely corroding samples, the +SRB
corrosion products had a high sulphur concentration of 8%, while
uninoculated products were composed of only 3% sulphur. In the case
of the coupled samples, the sulphur concentration increased to 16 and
9% for the +SRB and uninoculated cases, respectively. The higher
concentration of sulphur in the SRB containing media as probably due
to the production of sulphides at the biofilm/metal interface. The
higher concentration of sulphur due to coupling can be attributed to a
combined affect of increased reactivity at the metal surface due to a
driving cathodic current, increased activity of metal ions bound to SRB
(see below) and the attraction of bacteria to the anodic electrode by
electrostatic forces . Sulphur concentration in the +SRB layer is
especially high considering the bulk solution had a sulphide
concentration of ~4 ppm. These findings indicate a connection
between bacterial activities and the resulting surface morphology
found in this system. Active bacterial surface-mediated mineralisation
occurs either by the direct transformation of metals (i.e., methylation,
redox reactions) or by the formation of metal-reactive by-products
(i.e., sulphate reduction producing sulphide). Experimental work with
cultures of SRB has shown that metal ions sorbed to bacterial cells
tend to be more chemically active than when they are in solution 
and reduced iron and other base metals are commonly precipitated on
dissimulatory SRB cell surfaces as sulphides .
Figure 6. Comparison of sulphur concentration in the corrosion layers as a function
of coupling and the presence of SRB.
Another observation related to the SRB on the surface of alloy 400 was
that cells were encrusted in copper/nickel sulphides only when the
sample was initially coupled to the external cathode and SRB were
present. Bacteria require Cu and Ni as trace inorganic nutrients but
excessive quantities are inhibitory or lethal. Microorganisms
immobilize, mobilize or transform metals by extra cellular
precipitation reactions, intracellular accumulation, oxidation and
reduction reactions, methylation and demethylation, and extra cellular
binding. These mechanisms impede toxic metals from entering
and killing the cell. Bacteria can react with soluble metals by binding
and precipitating metal ions on their surface, producing minerals.
Precipitation reactions can be divided into two general categories:
passive and active mineralization . Passive mineralisation, or
surface catalysis, is caused by the net negative charge on most
bacterial cell surfaces which nucleates the precipitation of metallic
cations from solution. In many bacteria, capsules or slime, consisting
of extra cellular polymers, represent the outermost layer of the cell
surface. Capsules consist of linear polymers of polysaccharides or
repeating amino acid units and contain over 90% water. They may
contain anionic moieties such as carboxyl groups, and occasionally
phosphate and sulphate groups, which enable them to bind metals
[24, 25]. Bacterial extra cellular polymers have been proposed as
carriers for metals in aquatic environments . Binding sites for
metals are also found in proteins, nucleic acids and specialized .
Complexing ligands may be necessary for binding of specific metals;
in aqueous solutions, metals ions are often hydrated and can be
attracted to a number of dissolved, colloidal or solid organic or
inorganic substances . Metal binding to cell surfaces is pH and
temperature dependent due to their influence on metal and cell wall
chemistry [28-30]. Passive metal binding by bacterial surfaces
represents an electrostatic interaction; consequently, it is not
necessary that the cells be viable, only that their surfaces remain intact
Gouda et al. [9, 15] examined the susceptibility of alloy 400 towards
microbial attack in Arabian Gulf seawater. Results indicated that SRB
attack is initiated beneath black sulphur-rich deposits. The deposits
were found to be mostly iron nickel sulphides. No corrosion was
detected after 3 weeks of exposure under anaerobic SRB conditions,
but upon addition of aerated solution, the corrosion rate increased
significantly. The authors stated that failure of alloy 400 heat
exchanger tubes could take place if SRB are present irrespective of
their concentration. Also, their results indicated that alloy 400 is
highly susceptible to SRB attack when compared to 70/30 Cu-Ni alloy,
brass or N08825 under the same conditions. The mode of SRB attack
was intergranular corrosion that was accompanied by selective
dealloying of nickel and iron. Using EDS they found that under black
iron and nickel sulphides severe intergranular corrosion had taken
place. The attacked regions were copper-rich while the regions
around the active sites had higher Ni concentrations. Black deposits
were also found to be devoid of appreciable copper compounds which
indicated preferential attack of nickel and iron. However, a green
corrosion layer, found on top of these black deposits, was composed
of mainly copper chloride indicating that copper corrosion took place
after the initial sulphide attack.
Further experiments are needed to better understand the mechanisms
behind this type of corrosion such as characterization of the different
minerals produced during corrosion using an x-ray diffraction
spectrometer. EDS provides chemical composition but not phase
identification. Also, a Fourier Transform infrared microscope could be
used to identify organic compounds which are produced only in the
presence of an SRB biofilm. Finally, removal of the corrosion products
to characterize the resulting corrosion morphology in each case is a
Distribution, tenacity and chemical composition of sulphides produced
by SRB within biofilms are different from those produced by
waterborne inorganic sulphides. In an anaerobic environment, SRB
within biofilms produce sulphides at the metal surface which lead to
an increase in sulphur content of the corrosion products. Coupling to
an external cathode exposed to aerobic conditions increase the
sulphur content further. Because bacteria enmeshed in biofilms
produce extra cellular polymeric materials the tenacity of sulphide
layers produced by SRB may differ from those produced in the absence
of SRB. In the experiments described, only the sample exposed to SRB
and coupled to an external cathode had encrusted bacteria embedded
within the sulphide layer.
The authors wish to thank J. Jones-Meehan for supplying the bacterial
samples and K. I. Lowe for the maintaining of the bacterial cultures.
The work was performed under program element 0601153N,
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