전체메뉴
검색
Article Search

JMB Journal of Microbiolog and Biotechnology

QR Code QR Code

Research article

Bioactive Compounds and Chemical Biology

Inhibitory Effects of Brown Algae Extracts on Histamine Production in Mackerel Muscle via Inhibition of Growth and Histidine Decarboxylase Activity of Morganella morganii

Dong Hyun Kim 1, Koth Bong Woo Ri Kim 2, Ji Young Cho 3 and Dong Hyun Ahn 4*

1Hydro colloid Div., MSC Co., Ltd, Yangsan, Kyeongnam 626-280, Republic of Korea, 2Institute of Fisheries Sciences, Pukyong National University, Busan 619-911, Republic of Korea, 3Department of Marine Biotechnology, Soonchunhyang University, Asan 336-900, Republic of Korea, 4Department of Food Science & Technology/Institute of Food Science, Pukyong National University, Busan 608-737, Republic of Korea

Received: September 26, 2013; Accepted: January 5, 2014

J. Microbiol. Biotechnol. 2014; 24(4): 465-474

Published April 28, 2014 https://doi.org/10.4014/jmb.1309.09071

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

This study was performed to investigate the inhibitory effects of brown algae extracts on histamine production in mackerel muscle. First, antimicrobial activities of brown algae extracts against Morganella morganii were investigated using a disk diffusion method. An ethanol extract of Ecklonia cava (ECEE) exhibited strong antimicrobial activity. The minimum inhibitory concentration (MIC) of ECEE was 2 mg/ml. Furthermore, the brown algae extracts were examined for their ability to inhibit crude histidine decarboxylase (HDC) of M. morganii. The ethanol extract of Eisenia bicyclis (EBEE) and ECEE exhibited significant inhibitory activities (19.82% and 33.79%, respectively) at a concentration of 1 mg/ml. To obtain the phlorotannin dieckol, ECEE and EBEE were subjected to liquid-liquid extraction, silica gel column chromatography, and HPLC. Dieckol exhibited substantial inhibitory activity with an IC50 value of 0.61 mg/ml, and exhibited competitive inhibition. These extracts were also tested on mackerel muscle. The viable cell counts and histamine production in mackerel muscle inoculated with M. morganii treated with ≥2.5 MIC of ECEE (weight basis) were highly inhibited compared with the untreated sample. Furthermore, treatment of crude HDCinoculated mackerel muscle with 0.5% ECEE and 0.5% EBEE (weight basis), which exhibited excellent inhibitory activities against crude HDC, reduced the overall histamine production by 46.29% and 56.89%, respectively, compared with the untreated sample. Thus, these inhibitory effects of ECEE and EBEE should be helpful in enhancing the safety of mackerel by suppressing histamine production in this fish species.

Keywords

Brown algae, Histamine, Histidine decarboxylase, Mackerel muscle, Morganella morganii

References

  1. Borchardt SA, Allain EJ, Michels JJ, Stearns GW, Kelly RF, Mccoy WF. 2001. Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl. Environ. Microbiol. 67: 3174-3179.
    CrossRef
  2. El Gamal AA. 2010. Biological importance of marine algae. Saudi Pharm. J. 18: 1-25.
    CrossRef
  3. FDA. 2011. Scombrotoxin (histamine) formation. In: Fish and Fishery Products Hazards and Controls Guidance. FDA Center for Food Safety and Applied Nutrition, Office of Seafood. Available at http://www.fda.gov/FoodGuidances.
  4. Gale EF. 1940. The production of amines by bacteria: the decarboxylation of amino-acids by strains of bacterium coli. Biochem. J. 34: 392-413.
  5. Gale EF. 1943. Factors influencing the enzymatic activities of bacteria. Bacteriol. Rev. 7: 139-173.
  6. Gupta S, Abu-Ghannam N. 2011. Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci. Technol. 22: 315-326.
    CrossRef
  7. Hungerford JM. 2010. Scombroid poisoning: a review. Toxicon 56: 231-243.
    CrossRef
  8. Joe MJ, Kim SN, Choi HY, Shin WS, Park GM, Kang DW, Kim YK. 2006. The inhibitory effects of eckol and dieckol from Ecklonia stolonifera on the expression of matrix metalloproteinase-1 in human dermal fibroblasts. Biol. Pharm. Bull. 29: 11735-11739.
    CrossRef
  9. Kang HS, Kim HR, Byun DS, Son BW, Nam TJ, Choi JS. 2004. Tyrosinase inhibitors isolated from the edible brown alga Ecklonia stolonifera. Arch. Pharm. Res. 27: 1226-1232.
    CrossRef
  10. Kanki M, Yoda T, Tsukamoto T, Baba E. 2007. Histidine decarboxylases and their role in accumulation of histamine in tuna and dried saury. Appl. Environ. Microbiol. 73: 14671473.
    CrossRef
  11. Kim SH, Ben-Gigirey B, Barros-Velázquez J, Price RJ, An H. 2000. Histamine and biogenic amine production by Morganella morganii isolated from temperature-abused albacore. J. Food Prot. 63: 244-251.
  12. Küpper FC, Gaquerel E, Boneberg EM, Morath S, Salaün JP, Potin P. 2006. Early events in the perception of lipopolysaccharides in the brown alga Laminaria digitata include an o xidative b urst and a ctivation of fatty a cid oxidation cascades. J. Exp. Bot. 57: 1991-1999.
    CrossRef
  13. Lee SH, Park NH, Heo SJ, Kang SM, Ko SC, Han JS, Jeon YJ. 2010. Dieckol isolated from Ecklonia cava inhibits αglucosidase and α-amylase in vitro and alleviates postprandial hyperglycemia in streptozotocin-induced diabetic mice. Food Chem. Toxicol. 48: 2633-2637.
    CrossRef
  14. Lee SH, Li Y, Karadeniz F, Kim MM, Kim SK. 2009. αGlucosidase and α-amylase inhibitory activities of phloroglucinal derivatives from edible marine alga, Ecklonia cava. J. Sci. Food Agric. 89: 1552-1558.
    CrossRef
  15. Lee SY, Song EJ, Kim KBWR, Lim SI, Hong YK, Ahn DH. 2011. Antimicrobial activity of Myagropsis myagroides and interaction with food composition. Food Sci. Biotechnol. 20:85-92.
    CrossRef
  16. Lee SY, Kim JH, Song EJ, Kim KBWR, Hong YK, Lim SM, Ahn DH. 2009. Investigation of antimicrobial activity of brown algae extracts and the thermal and pH effects on their activity. Food Sci. Biotechnol. 18: 506-512.
  17. Lehane L, Olley J. 2000. Histamine fish poisoning revisited. Int. J. Food Microbiol. 58: 1-37.
    CrossRef
  18. Li YX, Wijesekara I, Li Y, Kim SK. 2011. Phlorotannins as bioactive agents from brown algae. Process Biochem. 46:2219-2224.
    CrossRef
  19. López-Sabater EI, Rodríguez-Jerez JJ, Hernández-Herrero M, Mora-Ventura MT. 1996. Incidence of histamine-forming bacteria and histamine content in scombroid fish species from retail markets in the Barcelona area. Int. J. Food Microbiol. 28: 411-418.
    CrossRef
  20. Mah JH, Kim YJ, Hwang HJ. 2009. Inhibitory effects of garlic and other spices on biogenic amine production in Myeolchi-jeot, Korean salted and fermented anchovy product. Food Control 20: 449-454.
    CrossRef
  21. Morii H, Kasama, K. 2004. Activity of two histidine decarboxylases from Photobacterium phosphoreum at different temperatures, pHs, and NaCl concentrations. J. Food Prot. 67: 1736-1742.
  22. Murray CK, Hobbs G, Gilbert RJ. 1982. Scombrotoxin and scombrotoxin-like poisoning from canned fish. J. Hyg. Cambridge 88: 215-220.
    CrossRef
  23. Myung CS, Shin HC, Bao HY, Yeo SJ, Lee BH, Kang JS. 2005. Improvement of memory by dieckol and phlorofucofuroeckol in ethanol-treated mice: possible involvement of the inhibition of acetylcholinesterase. Arch. Pharm. Res. 28: 691698.
    CrossRef
  24. Rawles DD, Flick GJ, Martin RE. 1996. Biogenic amines in fish and shellfish. Adv. Food Nutr. Res. 39: 329-364.
    CrossRef
  25. Shakila RJ, Vasundhara TS, Rao DV. 1996. Inhibitory effect of spices o n in vitro histamine production and histidine decarboxylase activity of Morganella morganii and on the biogenic amine formation in mackerel stored at 30oC. Z. Lebensm. Unters. Forsch. 203: 71-76.
    CrossRef
  26. Shibata T, Yamaguchi K, Nagayama K, Kawaguchi S, Nakamura T. 2002. Inhibitory activity of brown algal phlorotannins against glycosidases from the viscera of the turban shell Turbo cornutus. Eur. J. Phycol. 37: 493-500.
    CrossRef
  27. Siamopoulou P, Bimplakis A, Iliopoulou D, Vagias C, Cos P, Berghe DV, Roussis V. 2004. Diterpenes from the brown algae Dictyota dichotoma and Dictyota linearis. Phytochemistry 65: 2025-2030.
    CrossRef
  28. Silla Santos MH. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29: 213-231.
    CrossRef
  29. Stern JL, Hagerman AE, Steinberg PD, Mason PK. 1996. Phlorotannin-protein interactions. J. Chem. Ecol. 22: 18771899.
    CrossRef
  30. Tanase S, Guirard BM, Snell EE. 1985. Purification and properties of a pyridoxal 5’-phosphate-dependent histidine decarboxylase from Morganella morganii AM-15. J. Biol. Chem. 260: 6738-6746.
  31. Wendakoon CN, Sakaguchi M. 1992. Non-volatile amine production in mackerel muscle during growth of different bacterial species. J. Food Hyg. Soc. Jpn. 33: 39-45.
    CrossRef
  32. Wendakoon CN, Sakaguchi M. 1993. Combined effect of sodium chloride and clove on growth and biogenic amine formation of Enterobacter aerogenes in mackerel muscle extract. J. Food Prot. 56: 410-413.
  33. Wendakoon CN, Sakaguchi M. 1995. Inhibition of amino acid decarboxylase activity of Enterobacter aerogenes by active components in spices. J. Food Prot. 58: 280-283.
  34. Wijesinghe WAJP, Ko SC, Jeon YJ. 2011. Effect of phlorotannins isolated from Ecklonia cava on angiotensin Iconverting enzyme (ACE) inhibitory activity. Nutr. Res. Pract. 5: 93-100.
    CrossRef
  35. Zhu W, Chiu LCM, Ooi VEC, Chan PKS, Ang Jr PO. 2004. Antiviral property and mode of action of a sulphated polysaccharide from Sargassum patens against herpes simplex virus type 2. Int. J. Antimicrob. Agents 24: 279-283.
    CrossRef

Related articles in JMB

More Related Articles

Article

Research article

J. Microbiol. Biotechnol. 2014; 24(4): 465-474

Published online April 28, 2014 https://doi.org/10.4014/jmb.1309.09071

Copyright © The Korean Society for Microbiology and Biotechnology.

Inhibitory Effects of Brown Algae Extracts on Histamine Production in Mackerel Muscle via Inhibition of Growth and Histidine Decarboxylase Activity of Morganella morganii

Dong Hyun Kim 1, Koth Bong Woo Ri Kim 2, Ji Young Cho 3 and Dong Hyun Ahn 4*

1Hydro colloid Div., MSC Co., Ltd, Yangsan, Kyeongnam 626-280, Republic of Korea, 2Institute of Fisheries Sciences, Pukyong National University, Busan 619-911, Republic of Korea, 3Department of Marine Biotechnology, Soonchunhyang University, Asan 336-900, Republic of Korea, 4Department of Food Science & Technology/Institute of Food Science, Pukyong National University, Busan 608-737, Republic of Korea

Received: September 26, 2013; Accepted: January 5, 2014

Abstract

This study was performed to investigate the inhibitory effects of brown algae extracts on
histamine production in mackerel muscle. First, antimicrobial activities of brown algae
extracts against Morganella morganii were investigated using a disk diffusion method. An
ethanol extract of Ecklonia cava (ECEE) exhibited strong antimicrobial activity. The minimum
inhibitory concentration (MIC) of ECEE was 2 mg/ml. Furthermore, the brown algae extracts
were examined for their ability to inhibit crude histidine decarboxylase (HDC) of M. morganii.
The ethanol extract of Eisenia bicyclis (EBEE) and ECEE exhibited significant inhibitory
activities (19.82% and 33.79%, respectively) at a concentration of 1 mg/ml. To obtain the
phlorotannin dieckol, ECEE and EBEE were subjected to liquid-liquid extraction, silica gel
column chromatography, and HPLC. Dieckol exhibited substantial inhibitory activity with an
IC50 value of 0.61 mg/ml, and exhibited competitive inhibition. These extracts were also tested
on mackerel muscle. The viable cell counts and histamine production in mackerel muscle
inoculated with M. morganii treated with ≥2.5 MIC of ECEE (weight basis) were highly
inhibited compared with the untreated sample. Furthermore, treatment of crude HDCinoculated
mackerel muscle with 0.5% ECEE and 0.5% EBEE (weight basis), which exhibited
excellent inhibitory activities against crude HDC, reduced the overall histamine production by
46.29% and 56.89%, respectively, compared with the untreated sample. Thus, these inhibitory
effects of ECEE and EBEE should be helpful in enhancing the safety of mackerel by
suppressing histamine production in this fish species.

Keywords: Brown algae, Histamine, Histidine decarboxylase, Mackerel muscle, Morganella morganii

References

  1. Borchardt SA, Allain EJ, Michels JJ, Stearns GW, Kelly RF, Mccoy WF. 2001. Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl. Environ. Microbiol. 67: 3174-3179.
    CrossRef
  2. El Gamal AA. 2010. Biological importance of marine algae. Saudi Pharm. J. 18: 1-25.
    CrossRef
  3. FDA. 2011. Scombrotoxin (histamine) formation. In: Fish and Fishery Products Hazards and Controls Guidance. FDA Center for Food Safety and Applied Nutrition, Office of Seafood. Available at http://www.fda.gov/FoodGuidances.
  4. Gale EF. 1940. The production of amines by bacteria: the decarboxylation of amino-acids by strains of bacterium coli. Biochem. J. 34: 392-413.
  5. Gale EF. 1943. Factors influencing the enzymatic activities of bacteria. Bacteriol. Rev. 7: 139-173.
  6. Gupta S, Abu-Ghannam N. 2011. Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci. Technol. 22: 315-326.
    CrossRef
  7. Hungerford JM. 2010. Scombroid poisoning: a review. Toxicon 56: 231-243.
    CrossRef
  8. Joe MJ, Kim SN, Choi HY, Shin WS, Park GM, Kang DW, Kim YK. 2006. The inhibitory effects of eckol and dieckol from Ecklonia stolonifera on the expression of matrix metalloproteinase-1 in human dermal fibroblasts. Biol. Pharm. Bull. 29: 11735-11739.
    CrossRef
  9. Kang HS, Kim HR, Byun DS, Son BW, Nam TJ, Choi JS. 2004. Tyrosinase inhibitors isolated from the edible brown alga Ecklonia stolonifera. Arch. Pharm. Res. 27: 1226-1232.
    CrossRef
  10. Kanki M, Yoda T, Tsukamoto T, Baba E. 2007. Histidine decarboxylases and their role in accumulation of histamine in tuna and dried saury. Appl. Environ. Microbiol. 73: 14671473.
    CrossRef
  11. Kim SH, Ben-Gigirey B, Barros-Velázquez J, Price RJ, An H. 2000. Histamine and biogenic amine production by Morganella morganii isolated from temperature-abused albacore. J. Food Prot. 63: 244-251.
  12. Küpper FC, Gaquerel E, Boneberg EM, Morath S, Salaün JP, Potin P. 2006. Early events in the perception of lipopolysaccharides in the brown alga Laminaria digitata include an o xidative b urst and a ctivation of fatty a cid oxidation cascades. J. Exp. Bot. 57: 1991-1999.
    CrossRef
  13. Lee SH, Park NH, Heo SJ, Kang SM, Ko SC, Han JS, Jeon YJ. 2010. Dieckol isolated from Ecklonia cava inhibits αglucosidase and α-amylase in vitro and alleviates postprandial hyperglycemia in streptozotocin-induced diabetic mice. Food Chem. Toxicol. 48: 2633-2637.
    CrossRef
  14. Lee SH, Li Y, Karadeniz F, Kim MM, Kim SK. 2009. αGlucosidase and α-amylase inhibitory activities of phloroglucinal derivatives from edible marine alga, Ecklonia cava. J. Sci. Food Agric. 89: 1552-1558.
    CrossRef
  15. Lee SY, Song EJ, Kim KBWR, Lim SI, Hong YK, Ahn DH. 2011. Antimicrobial activity of Myagropsis myagroides and interaction with food composition. Food Sci. Biotechnol. 20:85-92.
    CrossRef
  16. Lee SY, Kim JH, Song EJ, Kim KBWR, Hong YK, Lim SM, Ahn DH. 2009. Investigation of antimicrobial activity of brown algae extracts and the thermal and pH effects on their activity. Food Sci. Biotechnol. 18: 506-512.
  17. Lehane L, Olley J. 2000. Histamine fish poisoning revisited. Int. J. Food Microbiol. 58: 1-37.
    CrossRef
  18. Li YX, Wijesekara I, Li Y, Kim SK. 2011. Phlorotannins as bioactive agents from brown algae. Process Biochem. 46:2219-2224.
    CrossRef
  19. López-Sabater EI, Rodríguez-Jerez JJ, Hernández-Herrero M, Mora-Ventura MT. 1996. Incidence of histamine-forming bacteria and histamine content in scombroid fish species from retail markets in the Barcelona area. Int. J. Food Microbiol. 28: 411-418.
    CrossRef
  20. Mah JH, Kim YJ, Hwang HJ. 2009. Inhibitory effects of garlic and other spices on biogenic amine production in Myeolchi-jeot, Korean salted and fermented anchovy product. Food Control 20: 449-454.
    CrossRef
  21. Morii H, Kasama, K. 2004. Activity of two histidine decarboxylases from Photobacterium phosphoreum at different temperatures, pHs, and NaCl concentrations. J. Food Prot. 67: 1736-1742.
  22. Murray CK, Hobbs G, Gilbert RJ. 1982. Scombrotoxin and scombrotoxin-like poisoning from canned fish. J. Hyg. Cambridge 88: 215-220.
    CrossRef
  23. Myung CS, Shin HC, Bao HY, Yeo SJ, Lee BH, Kang JS. 2005. Improvement of memory by dieckol and phlorofucofuroeckol in ethanol-treated mice: possible involvement of the inhibition of acetylcholinesterase. Arch. Pharm. Res. 28: 691698.
    CrossRef
  24. Rawles DD, Flick GJ, Martin RE. 1996. Biogenic amines in fish and shellfish. Adv. Food Nutr. Res. 39: 329-364.
    CrossRef
  25. Shakila RJ, Vasundhara TS, Rao DV. 1996. Inhibitory effect of spices o n in vitro histamine production and histidine decarboxylase activity of Morganella morganii and on the biogenic amine formation in mackerel stored at 30oC. Z. Lebensm. Unters. Forsch. 203: 71-76.
    CrossRef
  26. Shibata T, Yamaguchi K, Nagayama K, Kawaguchi S, Nakamura T. 2002. Inhibitory activity of brown algal phlorotannins against glycosidases from the viscera of the turban shell Turbo cornutus. Eur. J. Phycol. 37: 493-500.
    CrossRef
  27. Siamopoulou P, Bimplakis A, Iliopoulou D, Vagias C, Cos P, Berghe DV, Roussis V. 2004. Diterpenes from the brown algae Dictyota dichotoma and Dictyota linearis. Phytochemistry 65: 2025-2030.
    CrossRef
  28. Silla Santos MH. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29: 213-231.
    CrossRef
  29. Stern JL, Hagerman AE, Steinberg PD, Mason PK. 1996. Phlorotannin-protein interactions. J. Chem. Ecol. 22: 18771899.
    CrossRef
  30. Tanase S, Guirard BM, Snell EE. 1985. Purification and properties of a pyridoxal 5’-phosphate-dependent histidine decarboxylase from Morganella morganii AM-15. J. Biol. Chem. 260: 6738-6746.
  31. Wendakoon CN, Sakaguchi M. 1992. Non-volatile amine production in mackerel muscle during growth of different bacterial species. J. Food Hyg. Soc. Jpn. 33: 39-45.
    CrossRef
  32. Wendakoon CN, Sakaguchi M. 1993. Combined effect of sodium chloride and clove on growth and biogenic amine formation of Enterobacter aerogenes in mackerel muscle extract. J. Food Prot. 56: 410-413.
  33. Wendakoon CN, Sakaguchi M. 1995. Inhibition of amino acid decarboxylase activity of Enterobacter aerogenes by active components in spices. J. Food Prot. 58: 280-283.
  34. Wijesinghe WAJP, Ko SC, Jeon YJ. 2011. Effect of phlorotannins isolated from Ecklonia cava on angiotensin Iconverting enzyme (ACE) inhibitory activity. Nutr. Res. Pract. 5: 93-100.
    CrossRef
  35. Zhu W, Chiu LCM, Ooi VEC, Chan PKS, Ang Jr PO. 2004. Antiviral property and mode of action of a sulphated polysaccharide from Sargassum patens against herpes simplex virus type 2. Int. J. Antimicrob. Agents 24: 279-283.
    CrossRef