Food Control 40 (2014) 58e63
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Food Control
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Degradation of histamine by the halotolerant Staphylococcus carnosus
FS19 isolate obtained from fish sauce
Muhammad Zukhrufuz Zaman a, Fatimah Abu Bakar a, *, Jinap Selamat a, Jamilah Bakar b,
Swi See Ang c, Cheong Yew Chong a
a
b
c
Department of Food Science, Faculty of Food Science and Technology, Universiti Putra Malaysia, UPM Serdang 43400, Selangor D.E., Malaysia
Department of Food Technology, Faculty of Food Science and Technology, Universiti Putra Malaysia, UPM Serdang 43400, Selangor D.E., Malaysia
Institute of Bioscience, Universiti Putra Malaysia, UPM Serdang 43400, Selangor D.E., Malaysia
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 26 February 2013
Received in revised form
13 November 2013
Accepted 19 November 2013
Histamine is found in many fermented food products and may have detrimental effects on the health of
its consumers. Histamine and other amines are degraded by the oxidative deamination activity of certain
microorganisms. In this study, the growth characteristics and histamine-degrading activity of a Staphylococcus carnosus FS19 isolate derived from fish sauce were investigated. This bacterium exhibits
optimal growth at 35 C, pH 8 and 9% sodium chloride when cultivated in tryptic soy broth. The
histamine-degrading activity of the S. carnosus FS19 isolate was optimised at 40 C and pH 6 in 9%
buffered sodium chloride. When added to fish sauce samples, this bacterium exhibits remarkable
histamine-degrading activity. The histamine concentration was reduced by approximately 15.1% and
13.8% in the fish sauce samples that contained 18% and 21% salt, respectively. However, no histamine
degradation was observed in samples with a salt content greater than 21%. In addition, a slight degradation of other amines, including putrescine and cadaverine, was also observed in some of the samples.
In contrast, tyramine degradation did not occur in any of the samples. Therefore, S. carnosus FS19 is a
culture that could potentially reduce the histamine content of fermented fish products.
Ó 2013 Elsevier Ltd. All rights reserved.
Keywords:
Histamine
Biogenic amines
Histamine degradation
Staphylococcus carnosus
Fish sauce
1. Introduction
Histamine is a biologically active amine compound that is present in various food products due to the bacterial decarboxylation
of free histidine. High levels of histamine in foods are undesirable
because they may have adverse effects on the health of consumers
(Shalaby, 1996). Fish and its fermented products are rich in free
amino acids, rendering them vulnerable to bacterial decarboxylase
activity; thus, they might contain high levels of biogenic amines,
especially histamine. The Food and Drug Administration (FDA)
suggested 50 ppm and 500 ppm as the levels of toxic and defectinducing levels of histamine in fish products, respectively (Lehane
& Olley, 2000). Other amines, including tyramine, putrescine,
cadaverine and tryptamine, are also present in foods and their
significance for the safety and quality of food have been extensively
studied. Histamine is an odourless compound that is undetectable
even by panellists trained in organoleptic analysis (Tapingkae,
Parkin, Tanasupawat et al., 2010). Histamine and other biogenic
* Corresponding author. Tel.: þ60 3 8946 8368; fax: þ60 3 8942 3552.
E-mail address:
[email protected] (F.A. Bakar).
0956-7135/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.foodcont.2013.11.031
amines are also heat-stable, and even the autoclaving temperature
does not destroy them (Luten et al., 1992). Various approaches, such
as modified atmosphere packaging, irradiation, high hydrostatic
pressure, food additives and preservatives, as well as the use of
negative-amine producer starter cultures have been tested to
control the accumulation of biogenic amines in food products
(Latorre-Moratalla et al., 2010; Naila, Flint, Fletcher, Bremer, &
Meerdink, 2010). However, the mechanism underlying those
methods for controlling the content of amines is mainly the inhibition of the growth of amine-producing bacteria and amino acid
decarboxylase activities. Irradiation is an effective process for
degrading histamine molecules, but it has the potential health
hazardous of generating free radical compounds as the major
drawback (Kim et al., 2004; Kim, Kim, Ahn, Park, & Byun, 2005).
Therefore, efforts to degrading biogenic amines in foods without
posing detrimental effects on safety and quality remain an important issue.
Histamine is physiologically degraded through the oxidative
deamination process, catalysed by either histamine oxidase or
histamine dehydrogenase. Histamine oxidase catalyses the conversion of histamine, in the presence of water and oxygen, to
imidazole acetaldehyde, ammonia and hydrogen peroxide
M.Z. Zaman et al. / Food Control 40 (2014) 58e63
(Sekiguchi, Makita, Yamamura, & Matsumoto, 2004). Previous
studies have demonstrated the presence of histamine oxidase in
many bacterial species (Martuscelli, Crudele, Gardini, & Suzzi,
2000; Murooka, Doi, & Harada, 1979; Yamashita, Sakaue, Irawata,
Sugiono, & Murooka, 1993; Zaman, Bakar, Selamat, & Bakar, 2010).
In addition, several bacteria also utilise histamine dehydrogenase
to degrade histamine (Hacisalihoglu, Jongejan, & Duine, 1997).
Recently, the application of bacteria possessing histaminedegrading enzyme has become an emerging technology for
reducing the histamine concentration in foods, especially fermented products (Mah & Hwang, 2009; Naila et al., 2010). Nevertheless, certain food products pose restrictions on this activity in
terms of bacterial growth and enzyme activity at a low pH, high
temperature or high salinity. These restrictions should be eliminated to ensure the efficacy of this activity in foods with a high salt
content, such as fish sauce and shrimp sauce. However, only a few
available reports have focused on bacteria that exhibit biogenic
amine-degrading activity in such extreme environments. For
instance, Arthrobacter crystallopoietes KAIT-B-007, which was isolated from soil, was found to possess a thermophilic histamine
oxidase (Sekiguchi et al., 2004), and Natrinema gari, which was
isolated from fish sauce, exhibited histamine degradation activity
in a high-salt environment (Tapingkae, Parkin, et al., 2010;
Tapingkae, Tanasupawat, Parkin, Benjakul, & Visessanguan, 2010).
In our previous study, S. carnosus FS19 isolated from fish sauce is
known to be a histamine degrader. Therefore, this study is aimed to
evaluate the effects of different conditions on the histaminedegradation activity of S. carnosus FS19.
2. Materials and methods
2.1. Preparation of inoculums
S. carnosus FS19 used in this study is isolated from fish sauce
samples from north-eastern part of Malaysia. It is exhibited the
ability to degrade histamine in considerable strength, as well as
putrescine and cadaverine to a lesser strength (Zaman et al., 2010).
A loop-full of a tryptic soy agar slant culture of S. carnosus FS19 was
inoculated into 10 mL of tryptic soy broth and incubated at 37 C for
24 h. Five millilitres of this culture was then transferred to 100 mL
of tryptic soy broth and incubated at 37 C for 24 h. The culture was
centrifuged at 10,000 g for 10 min at 4 C. The cell pellet was
washed by centrifugation in sterile 0.05 M phosphate buffer (pH
7.0). The cell suspension was then adjusted to a concentration of
1 107 cells/mL in sterile 0.05 M phosphate buffer (pH 7.0) and
used as an inoculum. To study the effect of the pH value on histamine degradation, the pH of the phosphate buffer was adjusted
with the appropriate buffer solution. Sterile distilled water was
used instead of phosphate buffer in the study of histamine degradation in the fish sauce samples.
2.2. Effect of pH on the growth and histamine degradation activity
of S. carnosus FS19
To study the effect of pH on the growth of S. carnosus FS19, 5 mL
of the inoculums was added to 45 mL of tryptic soy broth with the
pH adjusted to 4, 5, 6, 7, 8, 9 or 10 using 1 M HCl and 1 M NaOH. The
inoculated broth was incubated at 37 C for 24 h with shaking at
150 rpm (Infors, Bottmingen, Switzerland). The cells present on
plate count agar (supplemented with 3% NaCl w/v) after growth at
37 C for 48 h were counted, and the number of cells was expressed
as the log of the colony-forming units (CFU)/mL.
The effect of pH on histamine degradation by S. carnosus FS19
was investigated by adding 2 mL of the inoculum to 18 mL of sterile
buffer medium. It is including 0.05 M acetate buffer (acetic acid and
59
sodium acetate) for pH 4e5, 0.05 M phosphate buffer (mono and
dibasic sodium phosphate) for pH 6e7 and 0.05 M Tris buffer for pH
8e9. Each buffer was supplemented with histamine dihydrochloride to 100 ppm and NaCl to 3% (w/v) in the final volume. The
mixed solutions were then incubated (Infors, Switzerland) at 35 C
for 24 h with shaking at 150 rpm. Samples (5 mL) were taken and
added to an equal amount of 1 M HCl (Merck, Darmstadt, Germany). These mixtures were boiled for 10 min and centrifuged
(Sigma 3-18K, Sartorius, Goettingen, Germany) at 9000 g for
10 min. The supernatant was frozen at 20 C prior to the analysis
of biogenic amines.
2.3. Effect of salt concentration on the growth and histamine
degradation activity of S. carnosus FS19
To study the effect of the salt concentration on the growth of
S. carnosus FS19, 5 mL of inoculum was added to 45 mL of tryptic
soy broth that was supplemented with 0%, 3%, 6%, 9%, 12%, 15% or
18% NaCl. The inoculated broth was incubated at 37 C for 24 h with
shaking at 150 rpm. The cells present on plate count agar (supplemented with 3% NaCl w/v) after growth at 37 C for 48 h were
counted, and the number of cells was expressed as the log of the
CFU/mL.
The effect of the salt concentration on histamine degradation by
S. carnosus FS19 was studied by adding 2 mL of inoculum to18 mL of
sterile 0.05 M phosphate buffer (pH 7.0) medium that was supplemented with 100 ppm of histamine hydrochloride. Sodium
chloride was added to achieve final concentrations of 0%, 3%, 6%, 9%,
12%, 15% or 18% (w/v). The mixtures were then incubated at 35 C
for 24 h with shaking at 150 rpm. Samples (5 mL) were taken and
added to an equal amount of 1 M HCl. These mixtures were boiled
for 10 min and centrifuged at 9000 g for 10 min. The supernatants
were frozen at 20 C prior to the analysis of biogenic amines.
2.4. Effect of temperature on the growth and histamine degradation
activity of S. carnosus FS19
To study the effect of temperature on the growth of S. carnosus
FS19, 5 mL of inoculum was added to 45 mL of tryptic soy broth that
was supplemented with 3% salt. The inoculated broth was incubated at 25, 30, 35, 40, 45 or 50 C for 24 h with shaking at 150 rpm.
The cells present on plate count agar (supplemented with 3% NaCl
w/v) after growth at 37 C for 48 h were counted, and the number of
cells was expressed as the log of the CFU/mL.
The effect of temperature on histamine degradation by
S. carnosus FS19 was investigated by adding 2 mL of inoculum to
18 mL of sterile 0.05 M phosphate buffer (pH 7.0) medium supplemented with 100 ppm of histamine dihydrochloride and 3%
NaCl (w/v) in the final volume. The mixed solutions were then
incubated at 30, 35, 40, 45 or 50 C for 24 h with shaking at
150 rpm. Samples (5 mL) were taken and added to an equal amount
of 1 M HCl. The mixtures were then boiled for 10 min and centrifuged at 9000 g for 10 min. The supernatants were frozen
at 20 C prior to the analysis of biogenic amines.
2.5. Degradation of histamine in fish sauce samples by S. carnosus
FS19
Five millilitres of inoculum was added to a 100 mL Erlenmeyer
flask containing 45 mL of fish sauce samples obtained from a
market in Serdang, Selangor, Malaysia. All of fish sauce samples
were made from anchovies and contain different percentage of salt
content (Sample A: 18%, B: 28%, C: 30% and D: 22%). For the control
samples, instead of starter culture, 5 mL of sterile distilled water
was added to 45 mL of fish sauce. The mixtures were then
60
M.Z. Zaman et al. / Food Control 40 (2014) 58e63
incubated (Infors, Bottmingen, Switzerland) at 37 C for 24 h with
shaking at 150 rpm. The incubation time was prolonged to five days
for a separate batch to study the time course of histamine degradation. The samples were subjected to an extraction procedure
prior to the analysis of biogenic amines.
2.6. Determination of pH and salt concentration
The pH value of the fish sauce samples was determined directly
using an electronic pH meter (Mettler Toledo 8603, Switzerland).
The salt concentration of a tenfold dilution of each sample was
determined using a salt meter (Atago ES-421, Japan).
2.7. Determination of biogenic amines
Determination of the biogenic amine contents was performed
by high-performance liquid chromatography (HPLC) according to
the method proposed by Hwang, Cahng, Shiua, and Chai (1997) and
modified by Ozogul, Taylor, Quantick, and Ozogul (2002). Briefly,
each fish sauce sample was transferred to a 50 mL centrifuge tube
and homogenised with 20 mL of 6% trichloroacetic acid for 3 min.
The homogenates were centrifuged (Sigma 3-18K, Sartorius, Germany) at 10,000 g at 4 C for 10 min and filtered through
Whatman paper No.1. The filtrates were then transferred to a
volumetric flask, and 6% trichloroacetic acid was added to a final
volume of 50 mL. A series of mixed standard amine solutions of
histamine dihydrochloride, putrescine dihydrochloride, cadaverine
dihydrochloride and tyramine hydrochloride was prepared to
obtain the standard curve for each of these amines. To each 1 mL of
a standard amine solution and each extracted sample, 1 mL of 2 M
sodium hydroxide was added, followed by 10 mL of benzoyl chloride. The solutions were mixed using a vortex mixer and then
incubated at 30 C for 40 min. The benzoylation reaction was
stopped by adding 2 mL of a saturated sodium chloride solution and
the solution was extracted with 3 mL of diethyl ether. After
centrifugation, the upper layer was transferred to a tube and
evaporated to dryness in a steam of nitrogen. The residue was then
dissolved in 1 mL of acetonitrile, and 20 mL aliquots were injected
into an HPLC apparatus. The HPLC analysis was performed with a
Waters 600 controller and pump, a Waters in-line degasser and a
Waters 2996 photodiode array detector (set at 254 nm). The
chromatographic column used was a SunfireÔ C18, 5 mm,
150 4.0 mm (Waters, Milford, USA). Water and acetonitrile were
used for gradient elution with a flow rate of 1 mL/min.
2.8. Statistical analysis
All of the experiments were conducted with three replications.
The data were subjected to an analysis of variance (ANOVA) and are
reported as the mean values the standard deviation. The mean
comparison was performed using Duncan’s Multiple Range Test
(DMRT). The significant difference was set at P < 0.05. All of the
statistical analyses were performed using the Statistical Package for
Social Sciences, SPSS Version 16.0 for windows (SPSS Inc., Chicago,
Illinois).
3. Results and discussion
3.1. Effect of pH on the growth and histamine degradation activity
of S. carnosus FS19
S. carnosus FS19 exhibited tolerance to a broad range of pH
values, but its optimal growth was observed at pH 8 (Fig. 1A). A
decrease in the viable cell count of approximately 5 log cycles
(compared to that at the optimal pH) was observed in medium
Fig. 1. Effect of pH on the growth (A) and histamine degrading activity (B) of Staphylococcus carnosus FS19. Error bars represent standard deviation of three replicates.
Bars labelled with different letters are significantly different (P < 0.05).
with pH 4. The pH value also influenced the histamine degradation activity of S. carnosus FS19. The results suggested that the
greatest histamine degradation occurred within the pH range of
5e7 (Fig. 1B). The highest histamine degradation activity was
observed at pH 6, degrading up to 32.5% of the histamine with
24 h of incubation at 37 C. However, more acidic and more
alkaline conditions markedly inhibited the degradation activity of
this isolate. S. carnosus FS19 degraded only 5.3% and 1.7% of the
histamine in medium at pH 8 or pH 9, respectively. Similar results
have been reported for histamine degradation by Natrinema gari
BCC 24369, which was isolated from fish sauce (Tapingkae, Parkin,
et al., 2010). This halophilic archaeon exhibited optimal degradation activity at pH 6.5e7.5, but it loses 90% and 30% of this activity
at pH 4 and pH 9, respectively. In contrast, the histamine oxidase
activity of Arthrobacter crystallopoietes KAIT-B-007 was found to be
optimal at pH 9 (Sekiguchi et al., 2004). The histamine degradation activity of this bacterium was found to be catalysed by an
endogenous enzyme (Murooka et al., 1979). Hence, the activity
occurs within the cell, where the pH is constant while the cell
remains intact and viable. The fact that the pH of the medium
influenced the histamine degradation activity may be attributable
to the loss of cell viability in acidic and alkaline conditions. Thus,
the profile for the histamine degradation activity of S. carnosus
FS19 is consistent with its growth profile across the range of
various pH values.
M.Z. Zaman et al. / Food Control 40 (2014) 58e63
3.2. Effect of salt on the growth and histamine degradation activity
of S. carnosus FS19
61
Montriwong, Rodtong, and Yongsawatdigul (2010) also found that
histamine degradation by Brevibacillus sp. SK35 isolated from fish
sauce was optimal in medium containing 10% salt. The optimal
activity of the histamine-degrading enzymes of Natrinema gari BCC
24369 and Natrinema gari HDS3-1 was observed in the presence of
4e5 M sodium chloride (Tapingkae, Parkin, et al., 2010; Tapingkae,
Tanasupawat, et al., 2010). Moreover, S. carnosus FS19 exhibited the
ability to degrade 22.1% of histamine in the presence of 18% salt.
This might be explained by its adaptability to high salinity, which
influences its enzymatic properties. In general, many salt-loving
(halophilic) enzymes require the presence of sodium chloride or
potassium chloride within the range of 1e4 M for their optimal
activity and stability (Mevarech, Frolow, & Gloss, 2000).
S. carnosus FS19 grew in the absence and presence of a high level
of salt (Fig. 2A), with optimal growth in 9% salt (9.35 log CFU/mL).
The number of cells obtained was significantly reduced to
5.96 log CFU/mL in medium containing 18% salt. Probst et al. (1998)
also found that some strains of S. carnosus isolated from fermented
fish and shrimp tolerated 15% salt, and some could even grow in
medium containing as much as 20% salt. Bacteria will lose their
turgor pressure when cultivated in a high-salt medium, leading to
physiological and metabolic disturbances (Liu, Asmundson, Gopal,
Holland, & Crow, 1998). Regulation of the osmotic pressure between the inside and outside of a cell is the mechanism that allows
some bacteria to overcome the effects of a high-salt environment
(Kashket, 1987). This trait is found only in halotolerant and halophilic bacteria that can grow in solutions containing as much as 5%
salt and even more than 12% salt (Frazier & Westhoff, 1988). Thus,
S. carnosus FS19 may be considered a halotolerant or halophilic
bacterium.
A high rate of histamine degradation activity by S. carnosus FS19
occurred in the presence of salt. Nevertheless, this activity was also
observed, although at a much lower rate, in the absence of salt. The
highest level of activity occurred in the presence of 9% salt, in which
up to 39.1% of the histamine was degraded (Fig. 2B). Sinsuwan,
As shown at Fig. 3A, S. carnosus grew well at temperatures
ranging from 30 C to 40 C. The highest viable count (9.01 log CFU/
mL) of this bacterium was observed at 35 C. The growth was
almost completely inhibited at temperatures above 45 C. In
agreement with these results, Probst et al. (1998) reported that
S. carnosus could grow at 42 C but could not grow at 45 C.
The histamine degradation activity of S. carnosus FS19 is temperature dependent. The highest activity occurred at 40 C, and at
Fig. 2. Effect of salt concentration on the growth (A) and histamine degrading activity
(B) of Staphylococcus carnosus FS19. Error bars represent standard deviation of three
replicates. Bars labelled with different letters are significantly different (P < 0.05).
Fig. 3. Effect of temperature on the growth (A) and histamine degrading activity (B) of
Staphylococcus carnosus FS19. Error bars represent standard deviation of three replicates. Bars labelled with different letters are significantly different (P < 0.05).
3.3. Effect of temperature on the growth and histamine degradation
activity of S. carnosus FS19
62
M.Z. Zaman et al. / Food Control 40 (2014) 58e63
this temperature, 23.5% of the histamine was degraded after incubation for 24 h (Fig. 3B). This activity was markedly inhibited by
temperatures higher than 40 C. When the incubation temperature
was increased to 45 C and 50 C, only 6.1% and 3.3% of the histamine was degraded in the cultures, respectively. In accordance with
this result, Sinsuwan et al. (2010) found that histamine is optimally
degraded by Brevibacillus sp. SK35 at 35 C. The histaminedegrading archaeon Natrinema gari BCC 24369 exhibited its
optimal degradation activity at 40e50 C in a buffer system when
applied as free or immobilised cells, but the activity rapidly
decreased at temperatures higher than 55 C (Tapingkae, Parkin,
et al., 2010). Enzyme activity is inhibited by high temperature
due to protein denaturation unless the enzyme is thermostable.
Sekiguchi et al. (2004) observed that the histamine oxidase from
Arthrobacter crystallopoietes KAIT-B-007 is thermostable because it
retained its full activity at 60 C. Most of the growth-associated
enzymes are known to exhibit the optimal activity at the same
temperature as optimal growth occurs. The fact that the growth of
S. carnosus FS19 is retarded at 50 C might explain why of its histamine degradation activity is inhibited at that same temperature.
3.4. Degradation of histamine in fish sauce samples by S. carnosus
FS19
The ability of S. carnosus FS19 to degrade histamine was
expressed in several fish sauce products (Fig. 4A). Fish sauce samples have different salt contents, as shown in Table 1. S. carnosus
FS19 also exhibited the ability to degrade approximately 14.6% and
11.4% of the putrescine and cadaverine contents (Fig. 4B and C),
respectively, of sample A. Nevertheless, tyramine degradation was
not observed in any of the fish sauce samples (Fig. 4D). It seems that
Table 1
pH values and salt content of fish sauce samples treated with Staphylococcus carnosus FS19 and control after incubated at 37 C for 24 h.
Fish sauce
pH
A
B
C
D
Salt concentration (%)
A
B
C
D
S. carnosus FS19
Control
4.97
5.64
4.76
4.87
0.03
0.01
0.01
0.03
5.16
5.61
4.81
4.82
0.01
0.01
0.06
0.04
18.50
28.17
29.87
21.93
0.20
0.55
0.15
0.32
18.57
28.07
29.73
21.77
0.12
0.21
0.25
0.21
All values are means SD of three replications. Control samples are treated with
sterile distilled water instead of the culture.
the degradation activity was restricted by salt concentration in the
samples. The histamine concentration was reduced by approximately 15.1% and 13.8% in fish sauce A (18% salt) and D (21% salt),
respectively. Nevertheless, histamine degradation was not
observed in samples B and C that contain 29% salt. This might be
due to the growth inhibition of this bacterium at very high salinity.
Moreover, the ability of bacteria to degrade histamine in pure
medium and in food samples is often different. The time course of
histamine degradation was investigated in fish sauce A that contains a high level of histamine. S. carnosus FS19 degraded histamine
continuously throughout the incubation period (Fig. 5). Nevertheless, the histamine level increased from the third to the fifth day of
incubation, which might be due amine formation by histamineproducing bacteria that were likely present in the samples. This
would be verified by observing an increase in the concentration of
Fig. 4. Biogenic amines degradation in fish sauce (white: Staphylococcus carnosus FS19, black: control). A) histamine, B) putrescine, C) cadaverine, D) tyramines. Error bars represent
standard deviation of three replicates.
M.Z. Zaman et al. / Food Control 40 (2014) 58e63
63
References
Fig. 5. Histamine concentration of fish sauce during incubation at 35 C for five days.
-: fish sauce treated with Staphylococcus carnosus FS19, ,: fish sauce without
treatment (control).
histamine in the treated and control samples. However, histamine
degradation was not observed in the control samples and the histamine concentration slowly increased during the incubation. On
the fifth day of incubation, the histamine level was 441.8 and
514.6 ppm in the treated and the control samples, respectively.
S. carnosus FS19 also exhibited the ability to degrade putrescine
and cadaverine by approximately 14.6% and 11.4% (Fig. 4B and C),
respectively in sample A. Degradation of either of these amines was
not observed in fish sauce samples with a salt content higher than
18%. This bacterium is known to have a poor ability to degrade
putrescine and cadaverine (Zaman et al., 2010). Nevertheless,
tyramine degradation was not observed in any of the fish sauce
samples (Fig. 4D). This could be due to the absence of tyramine
degrading enzymes in the culture. Other possibilities, such as the
environmental condition of samples not being suitable for tyramine degrading enzyme activity may also explain this result.
Tyramine degrading enzymes have been found in several strains of
Micrococcus varians and Brevibacterium linens (Leuschner, Heidel, &
Hammes, 1998). They reported that the tyramine oxidase activity of
M. varians LTH 1540 was strongly inhibited below pH 5. As shown at
Table 1, most of samples have pH values lower than 5, which may
further explain why a tyramine degradation activity was not
observed in this study.
4. Conclusion
In conclusion, S. carnosus FS19 can be considered a halotolerant
histamine-degrading bacteria. In this study, the highest viable
count of this bacterium was observed at pH 8, with a salt concentration of 9% and a temperature of 35 C. S. carnosus FS19 exhibited
the highest histamine degradation at pH 6, with a salt concentration of 9% and a temperature of 40 C. This degradation activity is
quite remarkable in a medium with a salt level up to 18%. Thus,
S. carnosus FS19 can potentially be used to reduce the accumulation
of histamine during the fermentation of food in high-salt conditions. To understand the effect of environmental factors on histamine degradation, further studies of more factors and with other
histamine-degrading bacteria are required.
Frazier, W. C., & Westhoff, D. C. (1988). Food Microbiology (4th ed.). New York:
McGraw-Hill, Inc.
Hacisalihoglu, A., Jongejan, J. A., & Duine, J. A. (1997). Distribution of amines
oxidase and amine dehydrogenase in bacteria grown in primary amines and
characterization of the amine oxidase from Klebsiella oxytoca. Microbiology,
143, 505e512.
Hwang, D. F., Chang, S. H., Shiua, C. Y., & Chai, T. J. (1997). High performance liquid
chromatographic determination of biogenic amines in fish implicated in food
poisoning. Journal of Chromatography B, 693, 23e30.
Kashket, E. R. (1987). Bioenergetics of lactic acid bacteria: cytoplasmic pH and
osmotolerance. FEMS Microbiology Reviews, 46, 233e244.
Kim, J. H., Ahn, H. J., Jo, C., Park, H. J., Chung, Y. J., & Byun, M. W. (2004).
Radiolysis of biogenic amines in model system by gamma irradiation. Food
Control, 15, 405e408.
Kim, J. H., Kim, D. H., Ahn, H. J., Park, H. J., & Byun, M. W. (2005). Reduction of the
biogenic amine contents in low salt-fermented soybean paste by gamma irradiation. Food Control, 16, 43e49.
Latorre-Moratalla, M. L., Bover-Cid, S., Talon, R., Garriga, M., Zanardi, E., Ianieri, A.,
et al. (2010). Strategies to reduce biogenic amine accumulation in traditional
sausage manufacturing. LWT e Food Science and Technology, 43, 20e25.
Lehane, L., & Olley, J. (2000). Histamine fish poisoning revisited. International
Journal of Food Microbiology, 58, 1e37.
Leuschner, R. G., Heidel, M., & Hammes, W. P. (1998). Histamine and tyramine
degradation by food fermenting microorganisms. International Journal of Food
Microbiology, 39, 1e10.
Liu, S. Q., Asmundson, R. V., Gopal, P. K., Holland, R., & Crow, V. L. (1998). Influence of
reduced water activity on lactose metabolism by Lactococcus lactis subsp. cremoris at different pH values. Applied and Environmental Microbiology, 64, 2111e
2116.
Luten, J. B., Bouquet, W., Seuren, L. A. J., Burggraaf, M. M., Riekwel-Booy, G.,
Durand, P., et al. (1992). Biogenic amines in fishery products: standardization
methods within EC. In H. H. Huss (Ed.), Quality assurance in the fish industry (pp.
427e439). Amsterdam: Elsevier Science Publishers B.V.
Mah, J. H., & Hwang, H. J. (2009). Inhibition of biogenic amine formation in a salted
and fermented anchovy by Staphylococcus xylosus as a protective culture. Food
Control, 20, 796e801.
Martuscelli, M., Crudele, M. A., Gardini, F., & Suzzi, G. (2000). Biogenic amine formation and oxidation by Staphylococcus xylosus strains from artisanal fermented sausages. Letters in Applied Microbiology, 31, 228e232.
Mevarech, M., Frolow, F., & Gloss, L. M. (2000). Halophilic enzymes: proteins with a
grain of salt. Biophysical Chemistry, 86, 155e164.
Murooka, Y., Doi, N., & Harada, T. (1979). Distribution of membrane bound
monoamine oxidase in bacteria. Applied and Environmental Microbiology, 38,
565e569.
Naila, A., Flint, S., Fletcher, G., Bremer, P., & Meerdink, G. (2010). Control of biogenic
amines in food e existing and emerging approaches. Journal of Food Science, 75,
R139eR150.
Ozogul, F., Taylor, K. D. A., Quantick, P., & Ozogul, Y. O. (2002). Biogenic amines
formation in atlantic herring (Clupea harengus) stored under modified atmosphere packaging using rapid HPLC method. International Journal of Food Science
& Technology, 37, 515e522.
Probst, A. J., Hertel, C., Richter, L., Wassill, L., Ludwig, W., & Hammes, W. P. (1998).
Staphylococcus condimenti sp. nov., from soy sauce mash, and Staphylococcus
carnosus (Schleifer and Fischer 1982) subsp. utilis subsp. nov. International
Journal of Systematic Bacteriology, 48, 651e658.
Sekiguchi, Y., Makita, H., Yamamura, A., & Matsumoto, K. (2004). A thermostable
histamine oxidase from Arthrobacter crystallopoietes KAIT-B-007. Journal of
Bioscience and Bioengineering, 97, 104e110.
Shalaby, A. R. (1996). Significance of biogenic amines to food safety and human
health. Food Research International, 29, 675e690.
Sinsuwan, S., Montriwong, A., Rodtong, S., & Yongsawatdigul, J. (2010). Biogenic
amines degradation by moderate halophile, Brevibacillus sp. SK35. Journal of
Biotechnology, 150, 316, 316.
Tapingkae, W., Parkin, K. L., Tanasupawat, S., Kruenate, J., Benjakul, S., &
Visessanguan, W. (2010). Whole cell immobilisation of Natrinema gari BCC
24369 for histamine degradation. Food Chemistry, 120, 842e849.
Tapingkae, W., Tanasupawat, S., Parkin, K. L., Benjakul, S., & Visessanguan, W. (2010).
Degradation of histamine by extremely halophilic archaea isolated from high
salt-fermented fishery products. Enzyme and Microbial Technology, 46, 92e99.
Yamashita, M., Sakaue, M., Iwata, M., Sugino, H., & Murooka, Y. (1993). Purification
and characterization of monoamine oxidase from Klebsiella aerogenes. Journal of
Fermentation and Bioengineering, 76, 289e295.
Zaman, M. Z., Bakar, F. A., Selamat, J., & Bakar, J. (2010). Occurrence of biogenic
amines and amines degrading bacteria in fish sauce. Czech Journal of Food Sciences, 28, 440e449.