Abstract
Fucoxanthin is a xanthophyll-type carotenoid that provides many benefits to human health. However, the mechanism by which fucoxanthin interacts with microbes and inhibits pathogenic bacteria is unknown. In this study, we investigated the effects of fucoxanthin isolated from the edible seaweed Undaria pinnatifida on pathogenic bacteria Escherichia coli and lactobacilli both in vitro and in vivo. Fucoxanthin strongly inhibited the growth of Gram-positive pathogenic bacteria but was less effective against Gram-negative bacteria. Fucoxanthin extracted from the crude mixture had a recovery rate of 93.38% and a purity of 82.70%, which were higher than those of fucoxanthin extracted using a previous method. Fucoxanthin also promoted the growth of intestinal microbes in mice. Fucoxanthinol, a metabolite of fucoxanthin, was generated in the culture media. Fucoxanthin can be deacetylated into fucoxanthinol not only by conventional digestive enzymes in the digestive tract, but also by E. coli and lactobacilli in the intestine. These results indicate that fucoxanthin interacts with and influences E. coli and lactobacilli in the intestine. Therefore, fucoxanthin isolated from Undaria pinnatifida possibly can be applied in human health maintenance.
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Airanthi, M. K., Sasaki, N., Iwasaki, S., Baba, N., Abe, M., Hosokawa, M., Baba, N., Abe, M., Hosokawa, M., and Miyashita, K., 2011. Effect of brown seaweed lipids on fatty acid composition and lipid hydroperoxide levels of mouse liver. Journal of Agricultural and Food Chemistry, 59 (8): 4156–4163, DOI: https://doi.org/10.1021/jf104643b.
Asai, A., Sugawara, T., Ono, H., and Nagao, A., 2004. Biotransformation of fucoxanthinol into amarouciaxanthin a in mice and hepg2 cells: Formation and cytotoxicity of fucoxanthin metabolites. Drug Metabolism & Disposition, 32 (2): 205–211, DOI: https://doi.org/10.1124/dmd.32.2.205.
Asai, A., Yonekura, L., and Nagao, A., 2008. Low bioavailability of dietary epoxyxanthophylls in humans. British Journal of Nutrition, 100 (02): 273–277, DOI: https://doi.org/10.1017/s0007114507895468.
Breemen, R. B. V., Dong, L., and Pajkovic, N. D., 2012. Atmospheric pressure chemical ionization tandem mass spectrometry of carotenoids. International Journal of Mass Spectrometry, 312 (2): 163–172, DOI: https://doi.org/10.1016/j.ijms.2011.07.030.
Burapan, S., Kim, M., and Han, J., 2017. Curcuminoid demethylation as an alternative metabolism by human intestinal microbiota. Journal of Agricultural and Food Chemistry, 65 (16): 3305–3310, DOI: https://doi.org/10.1021/acs.jafc.7b00943.
Chen, B., Zhou, G., and Liu, Q., 2001. Study on the effect of carotenoid, sodium taurocholate and free fatty acids on carotenoids uptake by intestinal cells in vitro. Acta Zoonutrimenta Sinica, 13 (2): 47–50, DOI: https://doi.org/10.3969/j.issn.1006-267X.2001.02.011.
Cheng, R. Y., Li, M., Li, S. S., He, M., Yu, X. H., Shi, L., and He, F., 2017. Vancomycin and ceftriaxone can damage intestinal microbiota and affect the development of the intestinal tract and immune system to different degrees in neonatal mice. Pathogens & Disease, 75 (8): 1–9, DOI: https://doi.org/10.1093/femspd/ftx104.
Cho, I., and Blaser, M. J., 2012. The human microbiome: At the interface of health and disease. Nature Reviews Genetics, 13 (4): 260–270, DOI: https://doi.org/10.1038/nrg3182.
Colpitts, S. L., Kasper, E. J., Keever, A., Liljenberg, C., Kirby, T., and Magori, K., 2017. A bidirectional association between the gut microbiota and CNS disease in a biphasic murine model of multiple sclerosis. Gut Microbes, 8 (6): 561–573, DOI: https://doi.org/10.1080/19490976.2017.1353843.
Devine, D. A., and Hancock, R. E., 2002. Cationic peptides: Distribution and mechanisms of resistance. Current Pharmaceutical Design, 8 (9): 703–714, DOI: https://doi.org/10.2174/1381612023395501.
Galasso, C., Corinaldesi, C., and Sansone, C., 2017. Carotenoids from marine organisms: Biological functions and industrial applications. Antioxidants, 6 (4): 96–129, DOI: https://doi.org/10.3390/antiox6040096.
Gammone, M. A., Riccioni, G., and D’Orazio, N., 2015. Carotenoids: Potential allies of cardiovascular health? Food and Nutrition Research, 59: 26762, DOI: https://doi.org/10.3402/fnr.v59.26762.
Guarner, F., and Malagelada, J. R., 2003. Gut flora in health and disease. The Lancet, 361 (9356): 512–519, DOI: https://doi.org/10.1016/S0140-6736(03)12489-0.
Gudielurbano, M., and Goñi, I., 2002. Effect of edible seaweeds (Undaria pinnatifida and Porphyra ternera) on the metabolic activities of intestinal microflora in rats. Nutrition Research, 22 (3): 323–331, DOI: https://doi.org/10.1016/S0271-5317(01)00383-9.
Habeebullah, S. F. K., Surendraraj, A., and Jacobsen, C., 2018. Isolation of fucoxanthin from brown algae and its antioxidant activity: In vitro and 5% fish oil-in-water emulsion. Journal of the American Oil Chemists Society, 95 (7): 835–843, DOI: https://doi.org/10.1002/aocs.12092.
Hu, T., Liu, D., Chen, Y., Wu, J., and Wang, S., 2010. Antioxidant activity of sulfated polysaccharide fractions extracted from Undaria pinnitafida in vitro. International Journal of Biological Macromolecules, 46 (2): 193–198, DOI: https://doi.org/10.1016/j.ijbiomac.2009.12.004.
Hu, X., Li, Y., Li, C., Fu, Y., Cai, F., Chen, Q., and Li, D., 2012. Combination of fucoxanthin and conjugated linoleic acid attenuates body weight gain and improves lipid metabolism in high-fat diet-induced obese rats. Archives of Biochemistry & Biophysics, 519 (1): 59–65, DOI: https://doi.org/10.1016/j.abb.2012.01.011.
Jaswir, I., Novirndri, D., Mohd, S. H., and Miyashita, K., 2012. Fucoxanthin extractions of brown seaweeds and analysis of their lipid fraction in methanol. Food Science & Technology International Tokyo, 18 (2): 251–257, DOI: https://doi.org/10.3136/fstr.18.251.
Johansson, M. A., Sjögren, Y. M., Persson, J. O., Nilsson, C., and Sverremark-Ekström, E., 2011. Early colonization with a group of Lactobacilli decreases the risk for allergy at five years of age despite allergic heredity. PLoS One, 6 (8): e23031, DOI: https://doi.org/10.1371/journal.pone.0023031.
Kim, S. M., Jung, Y. J., Kwon, O. N., Cha, K. H., Um, B. H., Chung, D., and Pan, C. H., 2012. A potential commercial source of fucoxanthin extracted from the microalga Phaeodactylum tricornutum. Applied Biochemistry and Biotechnology, 166 (7): 1843–1855, DOI: https://doi.org/10.1007/s12010-012-9602-2.
Komba, S., Kotakenara, E., and Tsuzuki, W., 2018. Degradation of fucoxanthin to elucidate the relationship between the fucoxanthin molecular structure and its antiproliferative effect on caco-2 cells. Marine Drugs, 16 (8): 275–284, DOI: https://doi.org/10.3390/md16080275.
Lievin, V., Peiffer, I., Hudault, S., Rochat, F., Brassart, D., Neeser, J. R., and Servin, A. L., 2000. Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity. Gut, 47 (5): 646–652, DOI: https://doi.org/10.1136/gut.47.5.646.
Mallett, A. K., Bearne, C. A., and Rowland, I. R., 2010. The influence of incubation pH on the activity of rat and human gut flora enzymes. Journal of Applied Microbiology, 66 (5): 433–437, DOI: https://doi.org/10.1111/j.1365-2672.1989.tb05112.x.
Manimala, M. R. A., and Murugesan, R., 2014. In vitro antioxidant and antimicrobial activity of carotenoid pigment extracted from Sporobolomyces sp. isolated from natural source. Journal of Applied and Natural Science, 6 (2): 649–653, DOI: https://doi.org/10.31018/jans.v6i2.511.
Matsumoto, M., Hosokawa, M., Matsukawa, N., Hagio, M., Shinoki, A., Nishimukai, M., and Hara, H., 2010. Suppressive effects of the marine carotenoids, fucoxanthin and fucoxanthinol on triglyceride absorption in lymph duct-cannulated rats. European Journal of Nutrition, 49 (4): 243–249, DOI: https://doi.org/10.1007/s00394-009-0078-y.
Milani, A., Basirnejad, M., Shahbazi, S., and Bolhassani, A., 2016. Carotenoids: Biochemistry, pharmacology and treatment. British Journal of Pharmacology, 174 (11): 1290–1324, DOI: https://doi.org/10.1111/bph.13625.
Miyashita, K., Nishikawa, S., Beppu, F., Tsukui, T., Abe, M., and Hosokawa, M., 2011. The allenic carotenoid fucoxanthin, a novel marine nutraceutical from brown seaweeds. Journal of the Science of Food & Agriculture, 91 (7): 1166–1174, DOI: https://doi.org/10.1002/jsfa.4353.
Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., and Medzhitov, R., 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell, 118 (2): 229–241, DOI: https://doi.org/10.1016/j.cell.2004.07.002.
Sachindra, N. M., Sato, E., Maeda, H., Hosokawa, M., Niwano, Y., Kohno, M., and Miyashita, K., 2007. Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites. Journal of Agricultural and Food Chemistry, 55 (21): 8516–8522, DOI: https://doi.org/10.1021/jf071848a.
Sanjay, K. R., 2009. Characterization of aspergillus carbonarius mutant in relation to xanthin production, toxicity studies and fermentation conditions for pigment production. Karnataka Journal of Agricultural Sciences, 24 (4): 656–659, DOI: https://doi.org/10.1093/jac/18.6.656.
Sarmientorubiano, L. A., Zúñiga, M., Pérezmartínez, G., and Yebra, M. J., 2007. Dietary supplementation with sorbitol results in selective enrichment of lactobacilli in rat intestine. Research in Microbiology, 158 (8): 694–701, DOI: https://doi.org/10.1016/j.resmic.2007.07.007.
Sugawara, T., Baskaran, V., Tsuzuki, W., and Nagao, A., 2002. Brown algae fucoxanthin is hydrolyzed to fucoxanthinol during absorption by caco-2 human intestinal cells and mice. Journal of Nutrition, 132 (5): 946–951, DOI: https://doi.org/10.1093/jn/132.5.946.
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., and Gordon, J. I., 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444 (7122): 1027–1031, DOI: https://doi.org/10.1038/nature05414.
Ushakumari, U. N., and Ramanujan, R., 2013. Isolation of astaxanthin from marine yeast and study of its pharmacological activity. International Current Pharmaceutical Journal, 2 (3): 67–69, DOI: https://doi.org/10.3329/icpj.v2i3.13584.
Velmurugan, G., Ramprasath, T., Gilles, M., Swaminathan, K., and Ramasamy, S., 2017. Gut microbiota, endocrine-disrupting chemicals, and the diabetes epidemic. Trends in Endocrinology & Metabolism, 28 (8): 612–625, DOI: https://doi.org/10.1016/j.tem.2017.05.001.
Wang, Z., Klipfell, E., Bennett, B. J., Koeth, R., Levison, B. S., and DuGar, B., 2011. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature, 472 (7341): 57–63, DOI: https://doi.org/10.1038/nature09922.
Wang, W., Wang, C., and Yue, S., 2017. Effects of lactobacillus on cholesterolemia and gut flora in hyperlipidemia mice. Chinese Journal of Rehabilitation Medicine, 32 (9): 989–993, DOI: https://doi.org/10.3969/j.issn.1001-1242.2017.09.004.
Wingerath, T., Stahl, W., and Sies, H., 1995. β-cryptoxanthin selectively increases in human chylomicrons upon ingestion of tangerine concentrate rich in β-cryptoxanthin esters. Archives of Biochemistry & Biophysics, 324 (2): 385–390, DOI: https://doi.org/10.1006/abbi.1995.0052.
Wu, W. L., 2017. Association among gut microbes, intestinal physiology, and autism. Ebiomedicine, 25: 11–12, DOI: https://doi.org/10.1016/j.ebiom.2017.10.013.
Xia, S., Wang, K., Wan, L., Li, A., Hu, Q., and Zhang, C., 2013. Production, characterization, and antioxidant activity of fucoxanthin from the marine diatom Odontella aurita. Marine Drugs, 11 (7): 2667–2681, DOI: https://doi.org/10.3390/md11072667.
Yissachar, N., Yan, Z., Ung, L., Lai, N. Y., Mohan, J. F., Ehrlicher, A., and Benoist, C., 2017. An intestinal organ culture system uncovers a role for the nervous system in microbeimmune crosstalk. Cell, 168 (6): 1135–1148, DOI: https://doi.org/10.1016/j.cell.2017.02.009.
Zhu, J., Sun, X., Chen, X., Wang, S., and Wang, D., 2016. Chemical cleavage of fucoxanthin from Undaria pinnatifida and formation of apo-fucoxanthinones and apo-fucoxanthinals identified using lc-dad-apci-ms/ms. Food Chemistry, 211 (15): 365–373, DOI: https://doi.org/10.1016/j.foodchem.2016.05.064.
Zorofchian, M. S., Karimian, H., Khanabdali, R., Razavi, M., Firoozinia, M., Zandi, K., and Abdul Kadir, H., 2014. Anticancer and antitumor potential of fucoidan and fucoxanthin, two main metabolites isolated from brown algae. The Scientific World Journal, 2014: 768323, DOI: https://doi.org/10.1155/2014/768323.
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This work was supported by the Independent Innovation Major Project of Huangdao District, Qingdao City (No. 2014-3-11), and the National Natural Science Foundation of China (No. 31371731).
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Liu, Z., Sun, X., Sun, X. et al. Fucoxanthin Isolated from Undaria pinnatifida Can Interact with Escherichia coli and lactobacilli in the Intestine and Inhibit the Growth of Pathogenic Bacteria. J. Ocean Univ. China 18, 926–932 (2019). https://doi.org/10.1007/s11802-019-4019-y
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DOI: https://doi.org/10.1007/s11802-019-4019-y