Advertisement

In vivo prebiotic properties of Ascophyllum nodosum polysaccharide hydrolysates from lactic acid fermentation

  • Waraporn Kaewmanee
  • Prisana SuwannapornEmail author
  • Tzou Chi Huang
  • Farage Al-Ghazzewi
  • Richard Frank Tester
Article

Abstract

Crude polysaccharide from seaweed Ascophyllum nodosum (SCP) was digested enzymatically using cellulase and pectinase followed by lactic acid fermentation by Lactobacillus plantarum or Enterococcus faecalis to obtain crude polysaccharide hydrolysate (SCPH). The total carbohydrates of SCPH (26.76%) were higher than SCP (22.68%). The sulphate content (which indicated sulphate ester groups of sulphated polysaccharides such as fucoidan) was higher relatively after enzymatic and lactic fermentation (from 17.14 to 25.36%). Fourier transform infrared spectroscopy-attenuated total reflection (FTIR-ATR) spectroscopy established a peak between 1228 and 1226 cm-1—which indicated sulphate ester groups, a component of fucoidan—was observed in all A. nodosum polysaccharides but not with purified alginate. Peaks at 814–817 cm-1 indicated also monosaccharide-linked sulphate groups—located at C-2 and C-3—which again highlighted the presence of fucoidan. The capacity of these fragments and other seaweed carbohydrates (alginates) to lower blood glucose was ranked in the order ‘hydrolysed’ alginate, native alginate, SCPH and SCP. Hydrolysed alginate fed to rats produced the greatest quantity of acetic acid followed by native alginate, SCPH (by L. plantarum), SCPH (by E. faecalis) and SCP (23.62, 18.02, 14.95, 14.04 and 12.10 mM respectively). Hydrolysed alginate and native alginate showed better potential gut health benefits (prebiotic properties) in terms of either gastrointestinal (GI) transit resistance or SCFAs production compared with crude seaweed polysaccharide due to the higher percentage of polysaccharides. A novel process to produce seaweed polysaccharides with beneficial bioactivities was proposed.

Keywords

Ascophyllum nodosum Crude polysaccharide hydrolysates Lactic fermentation Prebiotic Sulphate 

Notes

Acknowledgements

The authors are grateful to Ms. Hong Guo (Edinburgh, UK) for collecting the seaweed.

Funding information

This study was partially supported by a grant from the International Affairs Division and Kasetsart University Research and Development Institute, Kasetsart University, Thailand.

References

  1. Akiyama H, Endo T, Nakakita R, Murata K, Yonemoto Y, Okayama K (1992) Effect of depolymerized alginates on the growth of bifidobacteria. Biosci Biotechnol Biochem 56:355–356CrossRefGoogle Scholar
  2. Ale MT, Mikkelsen JD, Meyer AS (2011) Important determinants for fucoidan bioactivity: a critical review of structure-function relations and extraction methods for fucose-containing sulphated polysaccharides from brown seaweeds. Mar Drugs 9:2106–2130CrossRefGoogle Scholar
  3. Amorim RNS, Rodrigues JAG, Holanda ML, Quindere ALG, Paula RCMP, Melo VMM, Benevides NMB (2012) Antimicrobial effect of a crude sulfated polysaccharide from the red seaweed Gracilaria ornata. Braz Arch Biol Technol 55:171–181CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  5. Chale-Dzul J, Moo-Puc R, Robledo D, Freile-Pelegrin Y (2015) Hepatoprotective effect of the fucoidan from the brown seaweed Turbinaria tricostata. J Appl Phycol 27:2123–2135CrossRefGoogle Scholar
  6. Debon S, Tester RF (2001) In vitro binding of calcium, iron and zinc by non-starch polysaccharides. Food Chem 73:401–410CrossRefGoogle Scholar
  7. Deville C, Damas J, Forget J, Dandrifosse G, Peulen O (2004) Laminarin in the dietary fiber concept. J Sci Food Agric 84:1030–1038CrossRefGoogle Scholar
  8. Dierick N, Ovyn A, De Smet S (2009) Effect of feeding intact brown seaweed Ascophyllum nodosum on some digestive parameters and on iodine content inedible tissues in pigs. J Sci Food Agric 89:584–594CrossRefGoogle Scholar
  9. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  10. Dumas P, Miller L (2003) The use of synchrotron infrared microspectroscopy in biological and biomedical investigations. Vib Spectrosc 32:3–21CrossRefGoogle Scholar
  11. Gomez-Ordonez E, Ruperez P (2011) FTIR-ATR spectroscopy as a tool for polysaccharide identification in edible brown and red seaweeds. Food Hydrocoll 25:1514–1520CrossRefGoogle Scholar
  12. Gupta S, Abu-Ghannam N, Scannell AGM (2011) Growth and kinetics of Lactobacillus plantarum in the fermentation of edible Irish brown seaweeds. Food Bioprod Process 89:346–355CrossRefGoogle Scholar
  13. Hu B, Gong Q, Wang Y, Ma Y, Li J, Yu W (2006) Prebiotic effects of neoagaro oligosaccharides prepared by enzymatic hydrolysis of agarose. Anaerobe 12:260–266CrossRefGoogle Scholar
  14. Hughes SA, Shewry PR, Li L, Gibson GR, Sanz ML, Rastall RA (2007) In vitro fermentation by human faecal microflora of wheat arabinoxylans. J Agric Food Chem 55:4589–4595CrossRefGoogle Scholar
  15. Hwang PA, Phan NN, Lu WJ, Ngoc Hieu BT, Lin YC (2016) Low-molecular-weight fucoidan and high-stability fucoxanthin from brown seaweed exert prebiotics and anti-inflammatory activities in Caco-2 cells. Food Nutr Res 60:32033CrossRefGoogle Scholar
  16. Jimenez-Escrig A, Sanchez-Muniz FJ (2000) Dietary fiber from edible seaweeds: chemical, structure, physicochemical properties and effects on cholesterol metabolism. Nutr Res 20:585–598CrossRefGoogle Scholar
  17. Katiyar VK (2003) Regulation of blood glucose level in diabetes mellitus using palatable diet composition. Australas Phys Eng Sci Med 26:132–139CrossRefGoogle Scholar
  18. Kazy S, Sar P, Singh SP, Sen AK, D'Souza SF (2002) Extracellular polysaccharides of a copper-sensitive and a copper-resistant Pseudomonas aeruginosa strain: synthesis, chemical nature and copper binding. World J Microbiol Biotechnol 18:583–588CrossRefGoogle Scholar
  19. Kazy SK, Sar P, D'Souza SF (2008) Studies on uranium removal by the extracellular polysaccharide of a Pseudomonas aeruginosa strain. Bioremed J 12:47–57CrossRefGoogle Scholar
  20. Kolmert A, Wikstrom P, Hallberg KB (2000) A fast and simple turbidimetric method for the determination of sulphate in sulphate-reducing bacterial cultures. J Microbiol Methods 41:179–184CrossRefGoogle Scholar
  21. Kong Q, Dong S, Gao J, Jiang C (2016) In vitro fermentation of sulphated polysaccharides from E. prolifera and L. japonica by human faecal microbiota. Int J Biol Macromol 91:867–871CrossRefGoogle Scholar
  22. Lamela M, Anca J, Villar R, Otero J, Calleja JM (1989) Hypoglycemic activity of several seaweed extracts. J Ethnopharmacol 27:35–43CrossRefGoogle Scholar
  23. Lim SJ, Wan Aida MW (2017) Extraction of sulphated polysaccharides (Fucoidan) from brown seaweed. In: Venkatesan J, Anil S, Kim SK (eds) Seaweed polysaccharides: isolation, biological and biomedical applications. Elsevier, Amsterdam, pp 27–43CrossRefGoogle Scholar
  24. Lynch MB, Sweeney T, Callan JJ, O'Sullivan JT, O’Doherty JV (2010) The effect of dietary Laminaria-derived laminarin and fucoidan on nutrient digestibility, nitrogen utilisation, intestinal microflora and volatile fatty acid concentration in pigs. J Sci Food Agric 90:430–437Google Scholar
  25. Mathlouthi M, Koenig JL (1987) Vibrational spectra of carbohydrates. Adv Carbohydr Chem Biochem 44:7–89CrossRefGoogle Scholar
  26. Michel C, Macfarlane GT (1996) Digestive fates of soluble polysaccharides from marine macroalgae: involvement of the colonic microflora and physiological consequences for the host. J Appl Bacteriol 80:349–369CrossRefGoogle Scholar
  27. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428CrossRefGoogle Scholar
  28. Muraoka T, Ishihara K, Oyamada C, Kunitake H, Hirayama I, Kimura T (2008) Fermentation properties of low-quality red alga Susabinori Porphyra yezoensis by intestinal bacteria. Biosci Biotechnol Biochem 72:1731–1739CrossRefGoogle Scholar
  29. Pokusaeva K, Fitzgerald G, Sinderen D (2011) Carbohydrate metabolism in Bifidobacteria. Genes Nutr 6:285–306CrossRefGoogle Scholar
  30. Qi X, Al-Ghazzewi FH, Tester RF (2018) Dietary fibre, gastric emptying, and carbohydrate digestion: a mini-review. Starch-Stärke 70 Article 1700346Google Scholar
  31. Ramnani P, Chitarrari R, Tuohy K, Grant J, Hotchkiss S, Philp K, Campbell R, Gill C, Rowland I (2012) In vitro fermentation and prebiotic potential of novel low molecular weight polysaccharides derived from agar and alginate seaweeds. Anaerobe 18:1–6CrossRefGoogle Scholar
  32. Salyers AA, West SE, Vercellotti JR, Wilkins TD (1977) Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Appl Environ Microbiol 34:529–533Google Scholar
  33. Shobharani P, Halami PM, Sachindra NM (2013) Potential of marine lactic acid bacteria to ferment Sargassum sp. for enhanced anticoagulant and antioxidant properties. J Appl Microbiol 114:96–107CrossRefGoogle Scholar
  34. Silchenko AS, Kusaykin MI, Kurilenko VV, Zakharenko AM, Isakov VV, Zaporozhets TS, Gazha AK, Zvyagintseva TN (2013) Hydrolysis of fucoidan by fucoidanase isolated from the marine bacterium, Formosa algae. Mar Drugs 11:2413–2430CrossRefGoogle Scholar
  35. Terada A, Hara H, Mitsuoka T (1995) Effect of dietary alginate on the faecal microbiota and faecal metabolic activity in humans. Microb Ecol Health Dis 8:259–266CrossRefGoogle Scholar
  36. Wang Y, Han F, Hu B, Li J, Yu W (2006) In vivo prebiotic properties of alginate oligosaccharides prepared through enzymatic hydrolysis of alginate. Nutr Res 26:597–603CrossRefGoogle Scholar
  37. Zaporozhets TS, Besednova NN, Kusnetsova TA, Zvyagintseva TN, Makarenkova ID, Kryzhanovsky SP, Melnikov VG (2014) The prebiotic potential of polysaccharides and extracts of seaweeds. Russ J Mar Biol 40:1–9CrossRefGoogle Scholar
  38. Zhang CY, Wu WH, Wang J, Lan MB (2012) Antioxidant properties of polysaccharide from the brown seaweed Sargassum graminifolium (Turn.) and its effects on calcium oxalate crystallization. Mar Drugs 10:119–130CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Food Science and TechnologyKasetsart UniversityBangkokThailand
  2. 2.Department of Biological Science and TechnologyNational Pingtung University of Science and TechnologyNeipuTaiwan
  3. 3.Glycologic LimitedGlasgowUK

Personalised recommendations