Skip to main content
SpringerLink
Log in

In vitro antioxidant and anti-glycation properties of Sargassum horneri from golden tides on the South Korean coast and the effect on gut microbiota of mice fed a high-sucrose and low-fibre diet

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Outbreaks of algal blooms for Sargassum horneri and Ulva spp., called golden and green tides on the South Korean coast, severely damage the local coastal environment and marine ecological system. However, these edible algae are natural resources of beneficial bioactive components, such as dietary fibres, phenolic compounds, and minerals. In this study, the antioxidant and anti-glycation properties of 2% aqueous extract solution (AES) in vitro from S. horneri (Sh) and Ulva pertusa (Up), and the effects of dried S. horneri and Up on the caecal microbiota of mice fed a high-sucrose and low-fiber diet were investigated. Total phenolic content, antioxidant activity (DPPH radical scavenging and Fe-reducing power), and anti-glycation activity in the BSA-fructose model were higher in Sh-AES than in Up-AES groups. Male Institute of Cancer Research (ICR) mice fed a 5% (w/w) S. horneri diet for 14 days showed a reduced increase in body weight. 16S rDNA (V4) amplicon sequencing results showed that the ratio of Firmicutes/Bacteroidota was reduced after S. horneri and U. pertusa intake. Faecalibaculum rodentium-, Akkermansia muciniphila-, and Roseburia intestinalis-like bacteria were enriched in the S. horneri group. Phocaeicola vulgatus-like bacteria were abundant in both the S. horneri and U. pertusa groups. In contrast, the prevalence of Clostridium disporicum-like bacteria was low in mice fed the S. horneri diet. Among the bacteria enriched after S. horneri and U. pertusa administration, P. vulgatus was found to be prevalent. From these results, S. horneri from golden tides may be useful as a functional food.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

modified by LEfSe (p < 0.01) for caecal microbiota in mice fed a high sucrose-containing diet with no fibre (n = 5) and 5% (w/w) Sargassum horneri (n = 5)

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Amorati A, Valgimigli L (2018) Methods to measure the antioxidant activity of phytochemicals and plant extracts. J Agric Food Chem 66:3324–3329

    Article  CAS  PubMed  Google Scholar 

  • AOAC Intl (2006) Official methods of analysis, 18th ed. Association of Official Analytical Chemists (AOAC). Washington, DC

  • Chi C, Xue Y, Liu R, Wang Y, Lv N, Zeng H, Buys N, Zhu B, Sun J, Yin C et al (2020) Effects of a formula with a probiotic Bifidobacterium lactis supplement on the gut microbiota of low birth weight infants. Eur J Nutr 59:1493–1503

    Article  PubMed  Google Scholar 

  • Duwaerts CC, Maher JJ (2019) Macronutrients and the adipose-liver axis in obesity and fatty liver. Cell Mol Gastroenterol Hepatol 7:749–761

    Article  PubMed  PubMed Central  Google Scholar 

  • Eda M, Kuda T, Kataoka M, Takahashi H, Kimura B (2016) Anti-glycation properties of the aqueous extract solutions of dried algae products harvested and made in the Miura Peninsula, Japan, and effect of lactic acid fermentation on the properties. J Appl Phycol 28:3617–3624

    Article  Google Scholar 

  • Fernando IPS, Jayawardena TU, Sanjeewa KKA, Wang L, Jeon YJ, Lee WW (2018) Anti-inflammatory potential of alginic acid from Sargassum horneri against urban aerosol-induced inflammatory responses in keratinocytes and macrophages. Ecotoxicol Environ Saf 160:24–31

    Article  CAS  PubMed  Google Scholar 

  • Guo L, Goff HD, Xu F, Liu F, Ma J, Chen M, Zhong F (2020) The effect of sodium alginate on nutrient digestion and metabolic responses during both in vitro and in vivo digestion process. Food Hydrocolloids 107:105304

    Article  CAS  Google Scholar 

  • Harada M, Kuda T, Nakamura S, Lee GY, Hajime T, Kimura B (2021) In vitro antioxidant and immunomodulation capacities of low-molecular weight-alginate- and laminaran-responsible gut indigenous bacteria. LWT Food Sci Technol 151:112127

    Article  CAS  Google Scholar 

  • Hirota K, Inagaki S, Hamada R, Ishihara K, Miyake Y (2014) Evaluation of a rapid oral bacteria quantification system using dielectrophoresis and the impedance measurement. Biocontrol Sci 19:45–49

    Article  PubMed  Google Scholar 

  • Jesumani V, Du H, Pei O, Zheng C, Cheong KL, Huang N (2019) Unravelling property of polysaccharides from Sargassum sp. as an anti-wrinkle and skin whitening property. Int J Biol Macromol 140:216–224

    Article  CAS  PubMed  Google Scholar 

  • Kasubuchi M, Hasegawa S, Hiramatsu T, Ichimura A, Kimura I (2015) Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients 7:2839–2849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim HS, Sanjeewa KKA, Fernando IPS, Ryu BM, Yang HW, Ahn G, Kang MC, Heo SJ, Je JG, Jeon YJ (2018) A comparative study of Sargassum horneri Korea and China strains collected along the coast of Jeju island South Korea: Its components and bioactive properties. Algae 33:341–349

    Article  CAS  Google Scholar 

  • Kim BR, Shin J, Guevarra RB, Lee JH, Kim DW, Seol JH, Lee JH, Kim HB, Isaacson R (2017) Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol 27:2089–2093

    Article  PubMed  Google Scholar 

  • Knapp BK, Bauer LL, Swanson KS, Swanson KS, Tappenden KA, Fahey JRGC, Godoy MRC (2013) Soluble fiber dextrin and soluble corn fiber supplementation modify indices of health in cecum and colon of Sprague-Dawley rats. Nutrients 5:396–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong C, Gao R, Yan X, Huang L, Qin H (2019) Probiotics improve gut microbiota dysbiosis in obese mice fed a high-fat or high-sucrose diet. Nutrition 60:175–184

    Article  CAS  PubMed  Google Scholar 

  • Kuda T, Nishizawa M, Toshima D, Matsushima K, Yoshida S, Takahashi H, Kimura B, Yamagishi T (2021) Antioxidant and anti-norovirus properties of aqueous acetic acid macromolecular extracts of edible brown macroalgae. LWT Food Sci Technol 141:110942

    Article  CAS  Google Scholar 

  • Kuda T, Taniguchi E, Nishizawa M, Araki Y (2002) Fate of water-soluble polysaccharides in dried Chorda filum a brown alga during water washing. J Food Compos Anal 15:3–9

    Article  CAS  Google Scholar 

  • Laurens LML, Wolfrum EJ (2011) Feasibility of spectroscopic characterization of algal lipids: Chemometric correlation of NIR and FTIR spectra with exogenous lipids in algal biomass. Bioenergy Res 4:22–35

    Article  Google Scholar 

  • Lv L, Cheng Y, Zheng T, Li X, Zhai R (2014) Purification, antioxidant activity and antiglycation of polysaccharides from Polygonum multiflorum Thunb. Carbohyd Polym 99:765–773

    Article  CAS  Google Scholar 

  • Mohammed A, Bissoon R, Bajnath E, Mohammaed K, Lee T, Bissram M, John N, Kjalsa N, Lee KY, Ward K (2018) Multistage extraction and purification of waste Sargassum natans to produce sodium alginate: An optimization approach. Carbohyd Polym 198:109–118

    Article  CAS  Google Scholar 

  • Morrison DJ, Preston T (2016) Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7:189–200

    Article  PubMed  PubMed Central  Google Scholar 

  • Mizutani K, Ikeda K, Yamori Y (2000) Resveratrol inhibits AGEs-induced proliferation and collagen synthesis activity in vascular smooth muscle cells from stroke-prone spontaneously hypertensive rats. Biochem Biophys Res Commun 274:61–67

    Article  CAS  PubMed  Google Scholar 

  • Murakami K, Yamaguchi Y, Noda K, Fujii T, Shinohara N, Ushirokawa T et al (2011) Seasonal variation in the chemical composition of a marine brown alga, Sargassum horneri (Turner) C. Agardh. J Food Compos Anal 24:231–236

    Article  CAS  Google Scholar 

  • Nunes N, Rosa GP, Ferraz S, Barreto MC, Pinheiro de Carvalho MAA (2019) Fatty acid composition, TLC screening, ATR-FTIR analysis, anti-cholinesterase activity, and in vitro cytotoxicity to A549 tumor cell line of extracts of 3 macroalgae collected in Madeira. J Appl Phycol 32:759–771

    Article  CAS  Google Scholar 

  • Ottman N, Geerlings SY, Aalvink S, Vos WM, Belzer C et al (2017) Action and function of Akkermansia muciniphila in microbiome ecology, health and disease. Best Pract Res Clin Gastroenterol 31:637–642

    Article  PubMed  Google Scholar 

  • Park JJ, Lee WY (2021) Anti-glycation effect of Ecklonia cava polysaccharides extracted by combined ultrasound and enzyme-assisted extraction. Int J Biol Macromol 180:684–691

    Article  CAS  PubMed  Google Scholar 

  • Peasura N, Laohakunjit N, Kerdchoechuen O, Wanlapa S (2015) Characteristics and antioxidant of Ulva intestinalis sulphated polysaccharides extracted with different solvents. Int J Biol Macromol 81:912–919

    Article  CAS  PubMed  Google Scholar 

  • Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V et al (2017) Oxidative stress: Harms and benefits for human health. Oxid Med Cell Longev 2017:841676313

    Google Scholar 

  • Poncheewin W, Hermes GDA, van Dam JCJ, Koehorst JJ, Smidt H, Schaap PJ (2020) NG-Tax 2.0: A Semantic framework for high-throughput amplicon analysis. Front Genet 10:1366

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Quigley EMM (2013) Gut bacteria in health and disease. Gastroenterol Hepatol 9:560–569

    Google Scholar 

  • Sanjeewa KKA, Jayawardena TU, Kim SY, Lee HG, Je JG, Jee Y, Jeon YJ (2020) Sargassum horneri (Turner) inhibit urban particulate matter-induced inflammation in MH-S lung macrophages via blocking TLRs mediated NF-κB and MAPK activation. J Ethnopharmacol 249:112363

    Article  CAS  PubMed  Google Scholar 

  • Schalkwijk CG, Stehouwer CDA, van Hinsbergh VWM (2004) Fructose-mediated non-enzymatic glycation: sweet coupling or bad modification. Diabetes Metab Res Rev 20:369–382

    Article  CAS  PubMed  Google Scholar 

  • Seong H, Bae JH, Seo JS, Seo JS, Kim SA, Kim TJ, Han NS (2019) Comparative analysis of prebiotic effects of seaweed polysaccharides laminaran, porphyran, and ulvan using in vitro human fecal fermentation. J Funct Foods 57:408–416

    Article  CAS  Google Scholar 

  • Shahidi F, Ambigaipalan P (2015) Phenolics and polyphenolics in foods, beverages and spices: Antioxidant activity and health effects – A review. J Funct Foods 18:820–897

    Article  CAS  Google Scholar 

  • Shao P, Chen X, Sun P (2013) In vitro antioxidant and antitumor activities of different sulfated polysaccharides isolated from three algae. Int J Biol Macromol 62:155–161

    Article  CAS  PubMed  Google Scholar 

  • Shao P, Chen X, Sun P, Sun P (2014) Chemical characterization, antioxidant and antitumor activity of sulfated polysaccharide from Sargassum horneri. Carbohyd Polym 105:260–269

    Article  CAS  Google Scholar 

  • Shen Z, Zhu C, Quan Y, Yang J, Yuan W, Yang Z, Wu S, Luo W, Tan B, Wang X (2018) Insights into Roseburia intestinalis which alleviates experimental colitis pathology by inducing anti-inflammatory responses. J Gastroenterol Hepatol 33:1751–1760

    Article  CAS  PubMed  Google Scholar 

  • Sinclair L, Osman OA, Bertilsson S, Eiler A (2015) Microbial community composition and diversity via 16S rRNA gene amplicons: Evaluating the illumina platform. PLoS ONE 10:e0116955

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504:84–88

    Article  CAS  PubMed  Google Scholar 

  • Song W, Wang Z, Zhang X, Li Y (2018) Ethanol extract from Ulva prolifera prevents high-fat diet-induced insulin resistance, oxidative stress, and inflammation response in mice. Biomed Res Int 9:1374565

    Google Scholar 

  • Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SH, Wingreen NS, Sonnenburg JL (2016) Diet-induced extinctions in the gut microbiota compound over generations. Nature 529:212–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takei M, Kuda T, Eda M, Shikano A, Takahashi H, Kimura B (2017) Antioxidant and fermentation properties of aqueous solutions of dried algal products from the Boso Peninsula, Japan. Food Biosci 19:85–91

    Article  CAS  Google Scholar 

  • Takei M, Kuda T, Fukunaga M, Toyama A, Goto M, Takahashi H et al (2019) Effects of edible algae on caecal microbiomes of ICR mice fed a high-sucrose and low–dietary fibre diet. JAppl Phycol 31:3696–3978

    Google Scholar 

  • Takei MN, Kuda T, Taniguchi M, Nakamura S, Takahashi T, Kimura B (2020) Detection and isolation of low molecular weight alginate- and laminaransusceptible gut indigenous bacteria from ICR mice. Carbohyd Polymers 238:116205

  • Tako M, Tamanaha M, Tamashiro Y, Uechi S (2015) Structure of ulvan isolated from the edible green seaweed, Ulva pertusa. Adv Biosci Biotechnol 6:60824

    Google Scholar 

  • Taniguchi M, Kuda T, Takei M, Takahashi H, Kimura B (2021) Effects of fermented Aphanizomenon flos-aquae on the caecal microbiome of mice fed a high-sucrose and low-dietary fibre diet. J Appl Phycol 33:397–407

    Article  CAS  Google Scholar 

  • van Tussenbroek BI, Hernández AHA, Rodríguez-Martínez RE, Julio Espinoza-Avalosb HM, Canizales-Floresa CE, González-Godoy CE (2017) Severe impacts of brown tides caused by Sargassum spp. on near-shore Caribbean seagrass communities. Mar Pollut Bull 122:272–281

    Article  PubMed  CAS  Google Scholar 

  • Vlassara H (2005) Advanced glycation in health and disease: Role of the modern environment. Ann N Y Acad Sci 1043:452–460

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Yagiz Y, Buran TJ, Nunes CdN, Gu L (2011) Phytochemicals from berries and grapes inhibited the formation of advanced glycation end-products by scavenging reactive carbonyls. Food Res Int 44:2666–2673

    Article  CAS  Google Scholar 

  • Wei Q, Liu T, Sun DW, Sun DS (2018) Advanced glycation end-products (AGEs) in foods and their detecting techniques and methods: A review. Trends Food Sci Technol 82:32–45

    Article  CAS  Google Scholar 

  • Wu TR, Lin CS, Chang CJ, Lin TL, Martel J, Ko YF, Ojcius DM, Lu CC, Young JD, Lai HC (2019) Gut commensal Parabacteroides goldsteinii plays a predominant role in the anti-obesity effects of polysaccharides isolated from Hirsutella sinensis. Gut 68:248–262

    Article  CAS  PubMed  Google Scholar 

  • Yan SF, Ramasamy R, Naka Y, Schmidt AM (2003) Glycation, inflammation, and RAGE: a scaffold for the macrovascular complications of diabetes and beyond. Circulation Res 93:1159–11

    Article  CAS  PubMed  Google Scholar 

  • Yang JY, Lee YS, Kim Y, Lee SH, Ryu S, Fukuda S, et al. (2017) Gut commensal Bacteroides acidifaciens prevents obesity and improves insulin sensitivity in mice. Mucosal Immunol 10:104–116

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Cong Y (2021) Gut microbiota-derived metabolites in the regulation of host immune responses and immune-related inflammatory diseases. Cell Mol Immunol 18:866–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Zhu X, Yu Y, He L, Li Y, Liu R (2021) Comprehensive analysis of the anti-glycation effect of peanut skin extract. Food Chem 362:130169

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Wang F, Wang X, Liu X, Hou Y, Zhang Q (2010) Extraction of the polysaccharides from five algae and their potential antioxidant activity in vitro. Carbohyd Polym 82:118–121

    Article  CAS  Google Scholar 

  • Zheng LX, Chen XQ, Cheong KL (2020) Current trends in marine algae polysaccharides: The digestive tract, microbial catabolism, and prebiotic potential. Int J Biol Macromol 151:344–354

    Article  CAS  PubMed  Google Scholar 

  • Zou Y, Xue W, Luo G, Deong Z, Qin P, Guo R et al (2019) 1,520 reference genomes from cultivated human gut bacteria enable functional microbiome analyses. Nat Biotechnol 37:179–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was partially supported by the Yanmar Resource Recycling Support Organization, Tokyo, Japan and the Toyo Suisan Foundation, Tokyo, Japan. The authors thank Editage (www.editage.com) for their assistance with English language editing.

Author information

Authors and Affiliations

  1. Department of Food Science and Technology, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo, 108-8477, Japan

    Gayang Lee, Yuko Midorikawa, Takashi Kuda, Mika Harada, Sae Fujita, Hajime Takahashi & Bon Kimura

Authors
  1. Gayang Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuko Midorikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takashi Kuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mika Harada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sae Fujita
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hajime Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bon Kimura
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Gayang Lee: conceptualisation, methodology, validation, formal analysis, investigation, resources, data curation, writing – original draft, visualisation. Yuko Midorikawa: conceptualisation, methodology, validation, formal analysis, investigation. Takashi Kuda: Conceptualisation, methodology, validation, formal analysis, resources, data curation, writing – review and editing, visualisation, supervision, project administration. Mika Harada and Sae Fujita: formal analysis and investigation. Hajime Takahashi: Conceptualisation, Methodology, Supervision. Bon Kimura: Conceptualisation and supervision.

Corresponding author

Correspondence to Takashi Kuda.

Ethics declarations

Competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 190 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, G., Midorikawa, Y., Kuda, T. et al. In vitro antioxidant and anti-glycation properties of Sargassum horneri from golden tides on the South Korean coast and the effect on gut microbiota of mice fed a high-sucrose and low-fibre diet. J Appl Phycol 34, 2211–2222 (2022). https://doi.org/10.1007/s10811-022-02756-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-022-02756-5

Keywords

Search

Navigation