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Drying and extraction effects on three edible brown seaweeds for metabolomics

  • 8th Asian Pacific Phycological Forum
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Abstract

Metabolomics is often used to comprehensively elucidate the metabolites in organisms like seaweed. Amino acids hydrolysed from proteins and certain targeted metabolites in seaweed have been investigated. However, water-soluble metabolites like free amino acids, organic acids, and sugars have seldom been comprehensively analysed. Metabolomics are valuable tools for these studies, but they require optimisation of pre-treatment methodology. Here, we evaluated various pre-treatment drying and extraction methods for brown seaweed metabolomics. Three edible brown seaweeds (Cladosiphon okamuranus [Mozuku], Saccharina japonica [Kombu], and Undaria pinnatifida [Wakame]) were used. Freeze-drying and oven-drying at both 40 and 80 °C were investigated. Methanol-water extracts with and without chloroform were compared. Metabolites were evaluated and quantified using liquid chromatography-mass spectrometry and capillary electrophoresis-mass spectrometry. The results showed that metabolite profiling was determined mainly by seaweed species identity rather than pre-treatment method. Freeze-drying yielded higher metabolite concentrations than oven-drying at either 40 or 80 °C. The effects of extraction with and without chloroform on metabolite concentration varied with seaweed species.

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References

  • Ale MT, Meyer AS (2013) Fucoidans from brown seaweeds: an update on structures, extraction techniques and use of enzymes as tools for structural elucidation. RSC Adv 3:8131–8141

    Article  CAS  Google Scholar 

  • Amorim K, Lage-Yusty M-A, López-Hernández J (2012) Changes in bioactive compounds content and antioxidant activity of seaweed after cooking processing. CyTA - J Food 10:321–324

    Article  CAS  Google Scholar 

  • Angelina LM, Yasir S, Matanjun P, Abu Bakar MF (2015) Effect of different drying techniques on the phytochemical content and antioxidant activity of Kappaphycus alvarezii. J Appl Phycol 27:1717–1723

    Article  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  Google Scholar 

  • Buschmann AH, Camus C, Infante J, Neori A, Israel A, Hernandez-Gonzalez MC (2017) Seaweed production: overview of the global state of exploitation, farming and emerging research activity. Eur J Phycol 52:391–406

    Article  Google Scholar 

  • Chan JC-C, Cheung PC-K, Ang PO (1997) Comparative studies on the effect of three drying methods on the nutritional composition of seaweed Sargassum hemiphyllum (Turn.) C. Ag. J Agric Food Chem 45:3056–3059

    Article  CAS  Google Scholar 

  • Date Y, Sakata K, Kikuchi J (2012) Chemical profiling of complex biochemical mixtures from various seaweeds. Polym J 44:888–894

    Article  CAS  Google Scholar 

  • Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899

    Article  CAS  Google Scholar 

  • Ernst M, Silva DB, Silva RR, Vêncio RZ, Lopes NP (2014) Mass spectrometry in plant metabolomics strategies: from analytical platforms to data acquisition and processing. Nat Prod Rep 31:784–806

    Article  CAS  Google Scholar 

  • Fleurence J (2010) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Technol 10:25–28

    Article  Google Scholar 

  • Gerasimenko N, Logvinov S (2016) Seasonal composition of lipids, fatty acids pigments in the brown alga Sargassum pallidum: the potential for health. Open J Mar Sci 06:498–523

    Article  Google Scholar 

  • Goulitquer S, Potin P, Tonon T (2012) Mass spectrometry-based metabolomics to elucidate functions in marine organisms and ecosystems. Mar Drugs 10:849–880

    Article  CAS  Google Scholar 

  • Guiry MD, Guiry GM (2017) Algaebase: listing the world’s algae. In: World-Wide Electron. Publ. Natl. Univ. Ireland, Galway. http://www.algaebase.org/. Accessed 24 Nov 2017

  • Gupta S, Abu-Ghannam N (2011) Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci Technol 22:315–326

    Article  CAS  Google Scholar 

  • Gupta S, Cox S, Abu-Ghannam N (2011) Effect of different drying temperatures on the moisture and phytochemical constituents of edible Irish brown seaweed. LWT Food Sci Technol 44:1266–1272

    Article  CAS  Google Scholar 

  • Gupta V, Thakur RS, Reddy CRK, Jha B (2013) Central metabolic processes of marine macrophytic algae revealed from NMR based metabolome analysis. RSC Adv 3:7037

    Article  CAS  Google Scholar 

  • Gupta V, Thakur RS, Baghel RS, Reddy CRK, Jha B (2014) Seaweed metabolomics. A new facet of functional genomics. Adv Bot Res 71:31–52

    Article  Google Scholar 

  • Harnedy PA, FitzGerald RJ (2011) Bioactive proteins, peptides and amino acids from macrolagae. J Phycol 47:218–232

    Article  CAS  Google Scholar 

  • Heyman HM, Dubery IA (2016) The potential of mass spectrometry imaging in plant metabolomics: a review. Phytochem Rev 15:297–316

    Article  CAS  Google Scholar 

  • Hirayama A, Wakayama M, Soga T (2014) Metabolome analysis based on capillary electrophoresis-mass spectrometry. Trends Anal Chem 61:215–222

    Article  CAS  Google Scholar 

  • Jian Q, Zhu X, Chen J, Zhu Z, Yang R, Luo Q, Chen H, Yan X (2017) Analysis of global metabolome by gas chromatography-mass spectrometry of Pyropia haitanensis stimulated with 1-octen-3-ol. J Appl Phycol 29:2049–2059

    Article  CAS  Google Scholar 

  • Kaehler S, Kennish R (1996) Summer and winter comparisons in the nutritional value of marine macroalgae from Hong Kong. Bot Mar 39:11–17

    Article  Google Scholar 

  • Kim HK, Verpoorte R (2010) Sample preparation for plant metabolomics. Phytochem Anal 21:4–13

    Article  CAS  Google Scholar 

  • Lin M, Shapiro MJ (1997) Mixture analysis by NMR spectroscopy. Anal Chem 69:4731–4733

    Article  CAS  Google Scholar 

  • Malyarenko OS, Usoltseva RV, Shevchenko NM, Isakov VV, Zvyagintseva TN, Ermakova SP (2017) In vitro anticancer activity of the laminarans from Far Eastern brown seaweeds and their sulfated derivatives. J Appl Phycol 29:543–553

    Article  CAS  Google Scholar 

  • Mohamed S, Hashim SN, Rahman HA (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Technol 23:83–96

    Article  CAS  Google Scholar 

  • Murphy C, Hotchkiss S, Worthington J, McKeown SR (2014) The potential of seaweed as a source of drugs for use in cancer chemotherapy. J Appl Phycol 26:2211–2264

    Article  CAS  Google Scholar 

  • Murtagh F, Legendre P (2014) Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion? J Classif 31:274–295

    Article  Google Scholar 

  • Naylor J (1976) Production, trade and utilization of seaweed and seaweed products. FAO Fish Tech Pap 159:73

    Google Scholar 

  • Nielsen SS (2010) Determination of moisture content. In: Nielsen SS (ed) Food analysis laboratory manual, 2nd edn. Springer US, Boston, MA, pp 17–27

    Chapter  Google Scholar 

  • Ninomiya K (2002) Umami: a universal taste. Food Rev Int 18:23–38

    Article  CAS  Google Scholar 

  • Nylund GM, Weinberger F, Rempt M, Pohnert G (2011) Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla. PLoS One 6:e29359

    Article  CAS  Google Scholar 

  • Qasim R (1991) Amino acid composition of some common seaweeds. Pak J Pharm Sci 4:49–54

    CAS  PubMed  Google Scholar 

  • De Raad M, Fischer CR, Northen TR (2016) High-throughput platforms for metabolomics. Curr Opin Chem Biol 30:7–13

    Article  Google Scholar 

  • Robledo D, Freile Pelegrín Y (1997) Chemical and mineral composition of six potentially edible seaweed species of Yucatan. Bot Mar 40:301–306

    Article  CAS  Google Scholar 

  • Rousseau F, Draisma S, de Reviers B (2007) Classification of the Phaeophyceae from past to present and current challenges. In: Brodie J, Lewis J (eds) Unravelling the algae – the past, present and future of algal molecular systematics. Systematics Association, London, pp 267–284

    Chapter  Google Scholar 

  • Sánchez-Machado DI, López-Cervantes J, López-Hernández J, Paseiro-Losada P (2004) Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chem 85:439–444

    Article  Google Scholar 

  • Sanina NM, Goncharova SN, Kostetsky EY (2004) Fatty acid composition of individual polar lipid classes from marine macrophytes. Phytochemistry 65:721–730

    Article  CAS  Google Scholar 

  • Sappati PK, Nayak B, VanWalsum GP, Mulrey OT (2018) Combined effects of seasonal variation and drying methods on the physicochemical properties and antioxidant activity of sugar kelp (Saccharina latissima). J Appl Phycol 1–22

  • Soga T, Heiger DN (1998) Simultaneous determination of monosaccharides in glycoproteins by capillary electrophoresis. Anal Biochem 261:73–78

    Article  CAS  Google Scholar 

  • Soga T, Igarashi K, Ito C, Mizobuchi K, Zimmermann HP, Tomita M (2009) Metabolomic profiling of anionic metabolites by capillary electrophoresis mass spectrometry. Anal Chem 81:6165–6174

    Article  CAS  Google Scholar 

  • Stévant P, Indergård E, Ólafsdóttir A, Marfaing H, Larssen WE, Fleurence J, Roleda MY, Rustad T, Slizyte R, Nordtvedt TS (2018) Effects of drying on the nutrient content and physico-chemical and sensory characteristics of the edible kelp Saccharina latissima. J Appl Phycol 30:2587–2599

    Article  Google Scholar 

  • Sugimoto M, Kawakami M, Robert M, Soga T, Tomita M (2012) Bioinformatics tools for mass spectroscopy-based metabolomic data processing and analysis. Curr Bioinforma 7:96–108

    Article  CAS  Google Scholar 

  • Terasaki M, Itabashi Y (2003) Glycerolipid acyl hydrolase activity in the brown alga Cladosiphon okamuranus Tokida. Biosci Biotechnol Biochem 67:1986–1989

    Article  CAS  Google Scholar 

  • Van Hal JW, Huijgen WJJ, López-Contreras AM (2014) Opportunities and challenges for seaweed in the biobased economy. Trends Biotechnol 32:231–233

    Article  Google Scholar 

  • Wakayama M, Aoki N, Sasaki H, Ohsugi R (2010) Simultaneous analysis of amino acids and carboxylic acids by capillary electrophoresis−mass spectrometry using an acidic electrolyte and uncoated fused-silica capillary. Anal Chem 82:9967–9976

    Article  CAS  Google Scholar 

  • Wakayama M, Hirayama A, Soga T (2015) Capillary electrophoresis-mass spectrometry. In: Methods in molecular biology. Humana Press, New York, pp 113–122

    Google Scholar 

  • Wijesekara I, Pangestuti R, Kim S-K (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84:14–21

    Article  CAS  Google Scholar 

  • Wong K, Cheung PC (2001) Influence of drying treatment on three Sargassum species 1. Proximate composition, amino acid profile and some physico-chemical properties. J Appl Phycol 13:43–50

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Tatsuki Ogura and Mr. Yujin Ashio (Institute for Advanced Biosciences, Keio University, Japan) for their helpful suggestions.

Funding

This study was funded by the Yamagata prefectural government and by the city of Tsuruoka. It was also supported by a scholarship from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT), Japan, for an international student (Hamid, S.S).

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Authors and Affiliations

  1. Keio University, Institute for Advanced Biosciences, Tsuruoka, Yamagata, 997-0052, Japan

    Shahlizah Sahul Hamid, Masataka Wakayama, Tomoyoshi Soga & Masaru Tomita

  2. Systems Biology Program, Graduate School of Media and Governance, Keio University, Fujisawa, 252-8520, Japan

    Shahlizah Sahul Hamid, Masataka Wakayama, Tomoyoshi Soga & Masaru Tomita

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  1. Shahlizah Sahul Hamid
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  2. Masataka Wakayama
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  3. Tomoyoshi Soga
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Correspondence to Masataka Wakayama.

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Electronic supplementary material

ESM 1

Fig. S1 PCA a) score plots and b) loading plots of metabolites concentrations in three brown seaweed after all drying and extractions methods. The horizontal axis value indicates PC1-PC4 separation variance and the vertical axis value indicates PC2-5 separation variance. The blue colour box indicate the metabolites which contributed to PC1. The green colour box indicate the metabolites which contributed to PC2. All legends and abbreviations are as same as Fig.1. The abbreviations for metabolites as same as Fig. 2. Fig. S2 PCA a) score plots and b) loading plots of metabolites concentrations in freeze-dry methods. All other legends and abbreviations are as same as Fig. S1. Fig. S3 PCA a) score plots and b) loading plots of metabolites concentrations in oven-dry at 40 °C. All other legends and abbreviations are as same as Fig. S1. Fig. S4 PCA a) score plots and b) loading plots of metabolites concentrations in oven-dry at 80 °C. All other legends and abbreviations are as same as Fig. S1. Fig. S5 PCA a) score plots and b) loading plots of metabolites concentrations in methanol: chloroform: water extraction methods. All other legends and abbreviations are as same as Fig. S1. Fig. S6 PCA a) score plots and b) loading plots of metabolites concentrations in methanol: water extraction methods. All other legends and abbreviations are as same as Fig. S1. Fig. S7 PCA a) score plots and b) loading plots of metabolites concentrations in Mozuku samples. All other legends and abbreviations are as same as Fig. S1. Fig. S8 PCA a) score plots and b) loading plots of metabolites concentrations in Kombu. All other legends and abbreviations are as same as Fig. S1. Fig. S9 PCA a) score plots and b) loading plots of metabolites concentrations in Wakame. All other legends and abbreviations are as same as Fig. S1. (PDF 5908 kb)

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Hamid, S.S., Wakayama, M., Soga, T. et al. Drying and extraction effects on three edible brown seaweeds for metabolomics. J Appl Phycol 30, 3335–3350 (2018). https://doi.org/10.1007/s10811-018-1614-z

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  • DOI: https://doi.org/10.1007/s10811-018-1614-z

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