Abstract
Reducing fish pathogenic bacteria outbreak is important as it results in economic losses in aquaculture. Antibiotics are an inevitable tool to control the pathogenic bacteria outbreak. However, the authorities are taking more regulations to prevent the emergence of drug-resistant strain development. Alternative materials to be employed for the purpose are needed from natural sources. In this research, we explored the antibacterial activity of natural products derived from hop against fish pathogenic strains Streptococcus iniae and Vibrio vulnificus. Antimicrobial activities of nine separates from hops were tested against S. iniae and V. vulnificus and identified. Xanthohumol (1) showed strongest antibacterial property against S. iniae. In addition, desmethylxanthohumol (4) and 8-prenylnaringenin (5) showed antibacterial against both of the tested pathogen strains. Antibacterial compounds were all prenylated flavonoids, and these might be used as index components for development of feed additives for fish in aquaculture.
Similar content being viewed by others
References
Ben Hamed, S., M. J. Tavares Ranzani-Paiva, L. Tachibana, D. de Carla Dias, C. M. Ishikawa, and M. A. Esteban (2018) Fish pathogen bacteria: adhesion, parameters influencing virulence and interaction with host cells. Fish Shellfish Immunol. 80: 550–562.
Terzi, E., O. Corum, S. Bilen, O. N. Kenanoglu, O. Atik, and K. Uney (2020) Pharmacokinetics of danofloxacin in rainbow trout after different routes of administration. Aquaculture. 520: 734984.
Alexander, C. P., C. J. W. Kirubakaran, and R. D. Michael (2010) Water soluble fraction of Tinospora cordifolia leaves enhanced the non-specific immune mechanisms and disease resistance in Oreochromis mossambicus. Fish Shellfish Immunol. 29: 765–772.
Gabriel, N. N., J. Qiang, J. He, X. Y. Ma, M. D. Kpundeh, and P. Xu (2015) Dietary Aloe vera supplementation on growth performance, some haemato-biochemical parameters and disease resistance against Streptococcus iniae in tilapia (GIFT). Fish Shellfish Immunol. 44: 504–514.
Caruso, D., A. M. Lusiastuti, Taukhid, J. Slembrouck, O. Komarudin, and M. Legendre (2013) Traditional pharmacopeia in small scale freshwater fish farms in West Java, Indonesia: an ethnoveterinary approach. Aquaculture. 416–417: 334–345.
Acar, Ü., O. S. Kesbiç, S. Yılmaz, N. Gültepe, and A. Türker (2015) Evaluation of the effects of essential oil extracted from sweet orange peel (Citrus sinensis) on growth rate of tilapia (Oreochromis mossambicus) and possible disease resistance against Streptococcus iniae. Aquaculture. 437: 282–286.
Van Hai, N. (2015) The use of medicinal plants as immunostimulants in aquaculture: a review. Aquaculture. 446: 88–96.
U-taynapun, K., N. Mueangkan, and N. Chirapongsatonkul (2018) Efficacy of herbal extracts to control multi-antibiotics resistant (MAR) Aeromonas veronii isolated from motile Aeromonas septicemia (MAS)-exhibiting Nile tilapia (Oreochromis niloticus). Int. J. Agric. Technol. 14: 2191–2206.
Simpson, M. G. (2010) Plant Systematics. 2nd ed. Academic Press, Amsterdam, Netherlands.
Bocquet, L., S. Sahpaz, and C. Rivière (2018) An overview of the antimicrobial properties of hop. pp. 31–54. In: J.-M. Mérillon and C. Riviere (eds.). Natural Antimicrobial Agents. Springer, Cham, Switzerland.
Alworth, J. (2015) The Beer Bible. Workman Publishing, New York, NY, USA.
Faivre, C., K. Ghedira, P. Goetz, R. Lejeune, and H. Staub (2007) Humulus lupulus L. Phytotherapie (Paris). 5: 86–89.
Kramer, B., J. Thielmann, A. Hickisch, P. Muranyi, J. Wunderlich, and C. Hauser (2015) Antimicrobial activity of hop extracts against foodborne pathogens for meat applications. J. Appl. Microbiol. 118: 648–657.
Bhattacharya, S., S. Virani, M. Zavro, and G. J. Haas (2003) Inhibition of Streptococcus mutans and other oral streptococci by hop (Humulus lupulus L.) constituents. Econ. Bot. 57: 118–125.
Yamaguchi, N., K. Satoh-Yamaguchi, and M. Ono (2009) In vitro evaluation of antibacterial, anticollagenase, and antioxidant activities of hop components (Humulus lupulus) addressing acne vulgaris. Phytomedicine. 16: 369–376.
Zanoli, P. and M. Zavatti (2008) Pharmacognostic and pharmacological profile of Humulus lupulus L. J. Ethnopharmacol. 116: 383–396.
Pier, G. B. and S. H. Madin (1976) Streptococcus iniae sp. nov., a beta-hemolytic streptococcus isolated from an Amazon freshwater dolphin, Inia geoffrensis. Int. J. Syst. Evol. Microbiol. 26: 545–553.
Pier, G. B., S. H. Madin, and S. Al-Nakeeb (1978) Isolation and characterization of a second isolate of Streptococcus iniae. Int. J. Syst. Evol. Microbiol. 28: 311–314.
Robinson, J. A. and F. P. Meyer (1966) Streptococcal fish pathogen. J. Bacteriol. 92: 512.
Kitao, T., T. Aoki, and R. Sakoh (1981) Epizootic caused by β-haemoltytic Streptococcus species in cultured freshwater fish. Fish Pathol. 15: 301–307.
Kaige, N., T. Mjyazaki, and S. S. Kubota (1984) The pathogen and the histopathology of vertebral deformity in cultured yellowtail. Fish Pathol. 19: 173–179.
Eldar, A., Y. Bejerano, and H. Bercovier (1994) Streptococcus shiloi and Streptococcus difficile: two new streptococcal species causing a meningoencephalitis in fish. Curr. Microbiol. 28: 139–143.
Perera, R. P., S. K. Johnson, M. D. Collins, and D. H. Lewis (1994) Streptococcus iniae associated with mortality of Tilapia nilotica × T. aurea hybrids. J. Aquat. Anim. Health. 6: 335–340.
Eldar, A., Y. Bejerano, A. Livoff, A. Horovitcz, and H. Bercovier (1995) Experimental streptococcal meningo-encephalitis in cultured fish. Vet. Microbiol. 43: 33–40.
Feldhusen, F. (2000) The role of seafood in bacterial foodborne diseases. Microbes Infect. 2: 1651–1660.
Tamplin, M., G. E. Rodrick, N. J. Blake, and T. Cuba (1982) Isolation and characterization of Vibrio vulnificus from two Florida estuaries. Appl. Environ. Microbiol. 44: 1466–1470.
O’Neill, K. R., S. H. Jones, and D. J. Grimes (1992) Seasonal incidence of Vibrio vulnificus in the Great Bay estuary of New Hampshire and Maine. Appl. Environ. Microbiol. 58: 3257–3262.
DePaola, A., G. M. Capers, and D. Alexander (1994) Densities of Vibrio vulnificus in the intestines of fish from the U.S. Gulf Coast. Appl. Environ. Microbiol. 60: 984–988.
Wright, A. C., R. T. Hill, J. A. Johnson, M.-C. Roghman, R. R. Colwell, and J. G. Morris Jr. (1996) Distribution of Vibrio vulnificus in the Chesapeake Bay. Appl. Environ. Microbiol. 62: 717–724.
Hai, L., J. L. Larsen, I. Dalsgaard, and A. Dalsgaard (1998) Occurrence of Vibrio vulnificus biotypes in Danish marine environments. Appl. Environ. Microbiol. 64: 7–13.
Bisharat, N., V. Agmon, R. Finkelstein, R. Raz, G. Ben-Dror, L. Lerner, S. Soboh, R. Colodner, D. N. Cameron, D. L. Wykstra, D. L. Swerdlow, and J. J. Farmer 3rd (1999) Clinical, epidemiological, and microbiological features of Vibrio vulnificus biogroup 3 causing outbreaks of wound infection and bacteraemia in Israel. Lancet. 354: 1421–1424.
do Nascimento, S. M. M., R. H. dos Fernandes Vieira, G. N. D. Theophilo, D. Dos Prazeres Rodrigues, and G. H. F. Vieira (2001) Vibrio vulnificus as a health hazard for shrimp consumers. Rev. Inst. Med. Trop. Sao Paulo. 43: 263–266.
Baffone, W., R. Tarsi, L. Pane, R. Campana, B. Repetto, G. L. Mariottini, and C. Pruzzo (2006) Detection of free-living and plankton-bound vibrios in coastal waters of the Adriatic Sea (Italy) and study of their pathogenicity-associated properties. Environ. Microbiol. 8: 1299–1305.
Oliver, J. D. (2006) Vibrio vulnificus. pp. 253–276. In: S. Belkin and R. R. Colwell (eds.). Oceans and Health: Pathogens in the Marine Environment. Springer, Boston, MA, USA.
Mahmud, Z. H., S. B. Neogi, A. Kassu, B. T. Mai Huong, I. K. Jahid, M. S. Islam, and F. Ota (2008) Occurrence, seasonality and genetic diversity of Vibrio vulnificus in coastal seaweeds and water along the Kii Channel, Japan. FEMS Microbiol. Ecol. 64: 209–218.
Wiegand, I., K. Hilpert, and R. E. Hancock (2008) Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3: 163–175.
Chen, Q.-H., M.-L. Fu, M.-M. Chen, J. Liu, X.-J. Liu, G.-Q. He, and S.-C. Pu (2012) Preparative isolation and purification of xanthohumol from hops (Humulus lupulus L.) by high-speed counter-current chromatography. Food Chem. 132: 619–623.
Stevens, J. F., A. W. Taylor, G. B. Nickerson, M. Ivancic, J. Henning, A. Haunold, and M. L. Deinzer (2000) Prenylflavonoid variation in Humulus lupulus: distribution and taxonomic significance of xanthogalenol and 4′-O-methylxanthohumol. Phytochemistry. 53: 759–775.
Sukito, A. and S. Tachibana (2014) Isolation of hyperoside and isoquercitrin from Camellia sasanqua as antioxidant agents. Pak. J. Biol. Sci. 17: 999–1006.
Wei, Y., Q. **e, D. Fisher, and I. A. Sutherland (2011) Separation of patuletin-3-O-glucoside, astragalin, quercetin, kaempferol and isorhamnetin from Flaveria bidentis (L.) Kuntze by elution-pump-out high-performance counter-current chromatography. J. Chromatogr. A. 1218: 6206–6211.
Chen, S.-N., D. C. Lankin, L. R. Chadwick, B. U. Jaki, and G. F. Pauli (2009) Dynamic residual complexity of natural products by qHNMR: solution stability of desmethylxanthohumol. Planta Med. 75: 757–762.
Kim, H. J., S.-H. Kim, B. Y. Kang, and I.-S. Lee (2008) Microbial metabolites of 8-prenylnaringenin, an estrogenic prenylflavanone. Arch. Pharm. Res. 31: 1241–1246.
Stevens, J. F., M. Ivancic, V. L. Hsu, and M. L. Deinzer (1997) Prenylflavonoids from Humulus lupulus. Phytochemistry 44: 1575–1585.
Zhao, F., Y. Watanabe, H. Nozawa, A. Daikonnya, K. Kondo, and S. Kitanaka (2005) Prenylflavonoids and phloroglucinol derivatives from hops (Humulus lupulus). J. Nat. Prod. 68: 43–49.
Intelmann, D., G. Haseleu, and T. Hofmann (2009) LC-MS/MS quantitation of hop-derived bitter compounds in beer using the ECHO technique. J. Agric. Food Chem. 57: 1172–1182.
Moir, M. (2000) Hops—a millennium review. J. Am. Soc. Brew. Chem. 58: 131–146.
Bocquet, L., S. Sahpaz, J. L. Hilbert, C. Rambaud, and C. Rivière (2018) Humulus lupulus L., a very popular beer ingredient and medicinal plant: overview of its phytochemistry, its bioactivity, and its biotechnology. Phytochem. Rev. 17: 1047–1090.
Simpson, W. J. and A. R. Smith (1992) Factors affecting antibacterial activity of hop compounds and their derivatives. J. Appl. Bacteriol. 72: 327–334.
Ohsugi, M., P. Basnet, S. Kadota, E. Ishii, T. Tamura, Y. Okumura, and T. Namba (1997) Antibacterial activity of traditional medicines and an active constituent lupulone from Humulus lupulus against Helicobacter pylori. J. Tradit. Med. 14: 186–191.
Verzele, M. and D. De Keukeleire (2013) Chemistry and Analysis of Hop and Beer Bitter Acids. Elsevier, Amsterdam, Netherlands.
Stevens, J. F., A. W. Taylor, and M. L. Deinzer (1999) Quantitative analysis of xanthohumol and related prenylflavonoids in hops and beer by liquid chromatography-tandem mass spectrometry. J. Chromatogr. A. 832: 97–107.
Gerhäuser, C. (2005) Broad spectrum anti-infective potential of xanthohumol from hop (Humulus lupulus L.) in comparison with activities of other hop constituents and xanthohumol metabolites. Mol. Nutr. Food Res. 49: 827–831.
Nagel, J., L. K. Culley, Y. Lu, E. Liu, P. D. Matthews, J. F. Stevens, and J. E. Page (2008) EST analysis of hop glandular trichomes identifies an O-methyltransferase that catalyzes the biosynthesis of xanthohumol. Plant Cell. 20: 186–200.
Chen, X., E. Mukwaya, M.-S. Wong, and Y. Zhang (2014) A systematic review on biological activities of prenylated flavonoids. Pharm. Biol. 52: 655–660.
Hatano, T., Y. Shintani, Y. Aga, S. Shiota, T. Tsuchiya, and T. Yoshida (2000) Phenolic constituents of licorice. VIII. Structures of glicophenone and glicoisoflavanone, and effects of licorice phenolics on methicillin-resistant Staphylococcus aureus. Chem. Pharm. Bull. (Tokyo). 48: 1286–1292.
De Smet, P. A. G. M., K. Keller, R. Hänsel, and R. F. Chandler (1992) Adverse Effects of Herbal Drugs. Springer, Berlin, Germany.
Acknowledgements
This research was supported by the grants from the National Research Foundation of Korea (NRF-2019R1I1A1A01044151 & NRF-2021R1F1A1061707) and a project to train professional personnel in biological materials by the Ministry of Environment
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
The authors declare they have no conflict of interest. Neither ethical approval nor informed consent was required for this study.
Additional information
Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Lee, M., Lee, J., Kim, J.M. et al. Antibacterial Activity of Prenylated Flavonoids Isolated from Hop against Fish Pathogens Streptococcus iniae and Vibrio vulnificus. Biotechnol Bioproc E 27, 361–369 (2022). https://doi.org/10.1007/s12257-021-0247-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12257-021-0247-2