Food and Chemical Toxicology 50 (2012) 3251–3255
Contents lists available at SciVerse ScienceDirect
Food and Chemical Toxicology
journal homepage: www.elsevier.com/locate/foodchemtox
Review
Antimicrobial effect of phlorotannins from marine brown algae
Sung-Hwan Eom a, Young-Mog Kim b, Se-Kwon Kim a,c,⇑
a
Marine Bioprocess Research Center, Pukyong National University, Busan 608-737, Republic of Korea
Department of Food Science and Technology, Pukyong National University, Busan 608-737, Republic of Korea
c
Marine Biochemistry Laboratory, Department of Chemistry, Pukyong National University, Busan 608-737, Republic of Korea
b
a r t i c l e
i n f o
Article history:
Received 25 April 2012
Accepted 18 June 2012
Available online 23 June 2012
Keywords:
Antimicrobial activity
Brown algae
Phlorotannins
a b s t r a c t
Marine organisms exhibit a rich chemical content that possess unique structural features as compared to
terrestrial metabolites. Among marine resources, marine algae are a rich source of chemically diverse
compounds with the possibility of their potential use as a novel class of artificial food ingredients and
antimicrobial agents. The objective of this brief review is to identify new candidate drugs for antimicrobial activity against food-borne pathogenic bacteria. Bioactive compounds derived from brown algae are
discussed, namely phlorotannins, that have anti-microbial effects and therefore may be useful to explore
as potential antimicrobial agents for the food and pharmaceutical industries.
Crown Copyright Ó 2012 Published by Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
4.
Introduction . . . . . . . . . . . . . . . . . . . . . . .
Phlorotannins from marine brown algae
Antibacterial effect of phlorotannins . . .
Conclusion . . . . . . . . . . . . . . . . . . . . . . . .
Conflict of Interest . . . . . . . . . . . . . . . . . .
Acknowledgement . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
Since the 1970s, more than 21,855 structurally diverse, bioactive natural products with an astounding array of biological activities have been discovered from marine microbes, algae and
invertebrates (Blunt et al., 2012). Even though, the ocean covers
more than 70% of the earth’s surface, we only use less than 10%
of the total ocean area (Schultes, 1978). In particular, many marine
organisms live in complex habitats exposed to extreme conditions
and in adapting to new environment surroundings, they produce a
wide variety of secondary metabolites which cannot be found in
other organisms. Moreover, considering its great taxonomic diversity, investigations related to the search for new bioactive compounds from the marine environment can be seen as an almost
unlimited field. In addition, since the biological productivity of terrestrial ecosystems has also perhaps reached what it can achieve;
⇑ Corresponding author. Tel.: +82 516297094; fax: +82 516297099.
E-mail address: [email protected] (S.-K. Kim).
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the marine biodiversity of the ocean can be expected to yield
new therapeutic agents (Bugni and Ireland, 2004).
Increasing resistance of clinically important bacteria to existing
antibiotics is a major problem throughout the world (Kaplan and
Mason, 1998). Over the past 20 years, investigators from virtually
every corner of the world have documented that increasing proportions of Staphylococcus aureus are resistant to penicillin and
other antibiotics. As a result, the majority of S. aureus are swamped
with methicillin-resistant S. aureus (MRSA). In spite of the available
effective treatments against serious infections due to MRSA, high
mortality rates are still a major concern. There are a few new
agents in development that can be expected to benefit the situation in the next decade (Gould et al., 2009). Over the past 50 years,
S. aureus has become resistant to most antibiotics except vancomycin and other glycopeptides. Recently, these antibiotics have been
the mainstay of treatment for the multi drug-resistant S. aureus
and therefore the possibility that vancomycin resistance might
transfer from vancomycin-resistant enterococci to multi drugresistant S. aureus has been extremely worrying (Weigel et al.,
0278-6915/$ - see front matter Crown Copyright Ó 2012 Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.fct.2012.06.028
3252
S.-H. Eom et al. / Food and Chemical Toxicology 50 (2012) 3251–3255
terrestrial metabolites (Larsen et al., 2005). In the marine environment, where all surfaces are constantly exposed to the threat of
surface colonisation, sessile organisms remain relatively free from
biofouling (Rhimou et al., 2010). Furthermore, the chemical compounds produced by marine organisms are less well known than
those of their terrestrial counterparts. Among marine organisms,
edible seaweeds have been identified as an under-exploited plant
resource and a source of functional foods. It is believed that the
physiological and genetic characteristics of seaweeds differ compared to those of terrestrial plants. They are extensively used in
food and medicine (Lee et al., 2008). The ability of seaweeds to produce secondary metabolites of antimicrobial value, such as volatile
2003). Moreover, the emergence of several newly discovered MRSA
showed antibiotic resistance to vancomycin and teicoplanin
(Schito, 2006). As an alternative to vancomycin for treatment of
S. aureus infection, the new antimicrobial agents such as linezolid,
quinupristin/dalfopristin, daptomycin, tigecycline, and fidaxomicin
are being used for the most severe infections (Bush, 2011).
One of the ways of preventing antibiotic resistance is by using
new compounds which are not based on the existing synthetic
antimicrobial agents. Thus, the search for novel natural sources
from marine ecosystems could lead to the isolation of new antibiotics (Tan and Zou, 2001). Many organisms produce marine natural
products that possess unique structural features as compared to
HO
HO
OH
OH
OH
OH
HO
OH
O
O
OH
1
HO
O
O
OH
O
OH
O
O
OH
OH
OH
2
HO
OH
OH
3
OH
O
OH
OH
O
OH
O
HO
O
O
HO
HO
O
OH
O
O
O
OH
OH
5
HO
OH
4
HO
OH
OH
HO
OH
O
OH
HO
O
O
O
O
OH
OH
OH
HO
OH
O
6
OH
O
O
O
O
OH
OH
HO
HO
O
OH
OH
OH
OH
OH
O
HO
HO
O
O
O
OH
HO
OH
O
OH
O
OH
HO
8
OH
7
Fig. 1. Structures phlorotannins derived from marine algae [ phloroglucinol (1), eckol (2), fucofuroeckol-A (3), phlorofucofuroeckol-A (4), dioxinodehydroeckol (5), 8,80 bieckol(6), 7-phloroeckol (7), & dieckol (8)].
3253
S.-H. Eom et al. / Food and Chemical Toxicology 50 (2012) 3251–3255
components (phenols, terpenes) (Cox et al., 2010; Demirel et al.,
2009; Gressler et al., 2011; Gupta and Abu-Ghannam, 2011; Kotnala et al., 2009; Patra et al., 2008), steroids (Shanmughapriya et al.,
2008), phlorotannins (Wang et al., 2009) and lipids (Shanmughapriya et al., 2008) has been already studied. Among these,
phlorotannins as polyphenolic secondary metabolites are found
only in brown algae (Heo and Jeon, 2005).
Thus, the screen for antimicrobial agents as safe alternatives
and secondary metabolites from marine algae is attracting attention in the food industry. This review focuses on phlorotannins derived from marine algae and presents their potential application as
antimicrobial agents.
phlorotannin compounds such as eckol, phlorofucofuroeckol A
and dieckol, and 8,80 -bieckol have been isolated from E. kurome
and E. bicyclis (Nagayama et al., 2002). Phlorotannins in E. Arborea
possess a strong anti-allergic effect and their structures were elucidated as eckol, 6,60 -bieckol, 6,80 -bieckol, 8,80 -bieckol, phlorofucofuroeckol-A, and phlorofucofuroeckol-B (Sugiura et al., 2006).
Moreover, 6,60 -Bieckol diphlorethohydroxycarmalol, and phloroglucinol have been isolated from brown algae I. okamurae (Zou
et al., 2008). Collectively, phlorotannins can be used functional
ingredients in the food and pharmaceutical industries.
2. Phlorotannins from marine brown algae
Some synthetic preservatives and additives used in the food
industry have been evaluated as toxic to various cells and organs,
mutagens and tumor promoters over long-term use (Kahl and Kahl,
1983; Sasaki et al., 2005). Therefore, recently there has been a great
deal of interest in searching for novel natural antibiotics and these
studies have shown that phlorotannins in brown algae can act as
potential antimicrobial agents that may be useful in the food
industry and pharmaceutical industries (Choi et al., 2010; Eom,
2012; Lee et al., 2008).
The isolated and characterized phlorotannins (1–8) from brown
algae with antimicrobial activity are presented in Fig. 1., such as
phloroglucinol (1), eckol (2), fucofuroeckol-A (3), phlorofucofuroeckol-A (4), dioxinodehydroeckol (5), 8,80 -bieckol (6), 7-phloroeckol
(7), and dieckol (8). In addition, triphloroethol A, 6,60 -bieckol and
8,4000 -dieckol have been reported. These isolated phlorotannins have
been shown to have antimicrobial effect against food-borne
pathogenic bacteria, antibiotic resistance bacteria, and human tinea
pedis fungus (Table 1).
Dieckol purified from E. cava has fungicidal activity (Lee et al.,
2010). It has shown a potent antifungal activity against Trichophyton rubrum associated with dermatophytic nail infections in humans. In addition, it has shown a potent inhibition of cell
membrane integrity as well as cell metabolism against T. rubrum.
The MIC (minimum inhibitory concentration) values for eckol from
E. cava indicates potent antimicrobial activity against methicillinresistant S. aureus (MRSA) in the range of 125–250 lg/mL (Choi
et al., 2010). Dieckol isolated from E. stolonifera may possess stronger anti-MRSA activity than eckol and the MICs of dieckol were in
Marine algae have become an important source of pharmacologically active metabolites. Also, they are widely distributed and
abundant throughout the coastal areas of many countries. In addition, they are a source of useful secondary metabolites such as
agar, carragenean and alginate with interesting pharmaceutical
properties (Taskin et al., 2007). Among marine algae, brown algae
have been reported to contain higher phlorotannin contents as
marine phenolic compounds (Heo and Jeon, 2005). Phlorotannins
consist of polymers of phloroglucinol (1,3,5-tryhydroxybenzene)
units and are formed in the acetate–malonate pathway in marine
algae. Furthermore these phlorotannins are highly hydrophilic
components with a wide range of molecular sizes (126–650 kDa)
(Ragan and Glombitza, 1986; Wijesekara and Kim, 2010).
Several phlorotannins purified from brown seaweeds such as
Ecklonia cava, E. kurome, E. stolonifera, Eisenia aborea, Eisenia
bicyclis, Ishige okamurae, Pelvetia siliquosa have medicinal and pharmaceutical benefits and have shown strong anti-oxidant, antiinflammatory, anti-viral, anti-tumor, anti-diabetes and anti-cancer
properties (Cha et al., 2011; Eom et al., 2011; Gupta and
Abu-Ghannam, 2011; Kim et al., 2009).
Eckol, dieckol, and phloroglucinol from E. cava have shown potential for skin whitening effect (Heo et al., 2009) and anti-hypertensive effect (Wijesinghe et al., 2011). E. cava also contains other
phlorotannins including 6,60 -bieckol, 8,80 -bieckol, 8,4000 -dieckol,
dioxinodehydroeckol, fucodiphlorethol G, phlorofucofuroeckol-A,
triphlorethol-A (Ahn et al., 2004; Li et al., 2009). In addition,
3. Antibacterial effect of phlorotannins
Table 1
Phlorotannin compounds with antibacterial effect.
Source
Phlorotannin
Antimicrobial activity
IC50a
References
Eisenia
bicyclis
Eckol (2)
dieckol (8)
dioxinodehydroeckol
(5)
fucofuroeckol-A (3)
7-phloroeckol (7)
PhlorofucofuroeckolA (4)
Eckol (2)
Inhibition of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA)
32–64 lg/mL Eom (2012)
Inhibition of S. aureus, MRSA, Salmonella sp.
125–250 lg/
mL 148 mg/mL 96.5–
>800.8 lg/mLà
22.3>800.8 lg/mLà
Choi et al. (2010)
32–64 lg/mL 128–256 lg/
mL Lee et al. (2008)
Ecklonia cava
Ecklonia cava
Ecklonia
kurome
Ecklonia
stolonifera
a
à
Dieckol (8)
8,80 -Bieckol (6)
eckol (2)
dieckol (8)
phlorofucofuroeckolA (4)
phloroglucinol (1)
Dieckol (8)
Trichophyton rubrum inhibition
Inhibition of MRSA and bacillus cereus
. Inhibition of Campylobacter jejuni, Escherichia coli, Salmonella enteritidis, Salmonella
typhimurium, Vibrio parahaemolyticus
Inhibition of S. aureus and MRSA, bacillus subtilis.
Inhibition of Acinetobacter sp. Klebsiella pneumonia,
Legionella birminghamensis, Salmonella typhimurium, Shigella flexneri
IC50: concentration of a compound required for 50% inhibition in vitro.
MIC: minimum inhibitory concentration.
MBC: minimum bactericidal concentration.
Lee et al. (2010)
Nagayama et al.
(2002)
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S.-H. Eom et al. / Food and Chemical Toxicology 50 (2012) 3251–3255
the ranges of 32–64 lg/mL (Lee et al., 2008). Although the current
knowledge on the relationship between the structure and activity
of the active phlorotannins is limited, the physiological activity
may depend on the degree of polymerization of phlorotannin
derivatives (Ragan and Glombitza, 1986; Eom et al., 2012). In
addition, in a comparison of other phlorotannins, using catechin
derivatives as positive control, it has been reported that the MICs
of ()-epigallocatechin, ()-EGCg, (+)-gallocatechin and ()-gallocatechin from green tea (Camellia sinensis) against MRSA were
64 lg/mL (Stapleton et al., 2004). Thus, the anti-MRSA activity of
phlorotannins isolated E. bicyclis was superior to or equal to those
of catechins derived from green tea (Eom, 2012).
Phlorotannins from E. kurome have been reported to show bactericidal activity against food-borne pathogenic bacteria (Ahn
et al., 2004). Moreover, the oral administration of the phlorotannins at a dosage rate of 170–1500 mg/kg bw/day for 14 days in
mice ‘‘did not report any cytotoxic effect’’. The interactions between bacterial proteins and phlorotannins were considered to
play an important role in the bactericidal action of phlorotannins
(Ahn et al., 2004). Therefore it is thought that phlorotannins from
brown algae could be very useful in the food and pharmaceutical
industries as antibiotic agents. In addition to phlorotannins, brown
algae include various health enhancing compounds such as fucoxanthin, sulphated polysaccharides, sterols, polyunsaturated fatty
acids, and soluble fibers (Kim et al., 2002).
4. Conclusion
Marine natural products provide a rich source of chemically diverse compounds that can be used to develop novel, potential, and
useful therapeutic agents. Certain marine products have been reported to exhibit antimicrobial effects against several pathogens.
Hence, in an effort to discover an alternative antibiotic, marine
organisms have attracted much attention since more pathogens
are becoming resistant to antibiotics due to over-prescription. In
this brief review, phlorotannins derived from brown algae have
been considered from the perspective of their potential antimicrobial activity. Further work will be necessary to show whether they
can be effective as broad spectrum antibiotics against food-borne
pathogenic bacteria.
Conflict of Interest
The authors declare that there are no conflicts of interest.
Acknowledgement
This study was supported by a grant from The Marine Bioprocess Research Center of the Marine Bio 21 Project funded by The
Ministry of Land, Transport and Maritime, Republic of Korea.
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