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Natalie Heffernan Extraction, characterization and seasonal variation of bioactive compounds (polyphenols, carotenoids and polysaccharides) from Irish origin macroalgae with potential for inclusion in functional food products. By Natalie Heffernan A Thesis Presented in Fulfilment of the Requirement for the Degree of Doctor of Philosophy Supervisors: Prof. Dick FitzGerald, University of Limerick Dr. Nigel Brunton, University College Dublin Dr. Thomas Smyth, Teagasc Food Research Centre, Ashtown Submitted to the University of Limerick June 2015 Declaration of originality “I hereby certify that the work of this thesis is based on my own independent work, except where I have received help as stated in the acknowledgements and text. All quotations and summary of the work of others have been acknowledged where appropriate. Permission is granted for this work to be copied in whole or in a part for the purpose of private study, provided that in each case the user acknowledges the source and his or her indebtedness to the author.” Natalie Heffernan Signed: Date: I Table of Contents Declaration of originality……………………………………………………………………….....I Table of contents……………………………………………………………………………….....II Abstract………………………………………………………………………………………….. X Acknowledgements………………………………………………………………………………XI List of figures……………………………………………………………………………………XII List of tables………………………………………………………………………………...….XVI Chapter 1. Literature Review…………………………………………………….………………1 1.0 Marine Algae (Seaweed)…………………………………………………………………..2 1.1 Utilization of marine algae………………………………………………………………...3 1.1.1 Commercial uses…………………………………………………………………………..3 1.1.2 Human food………………………………………………………………………………...4 1.1.3 Dietary supplementation………………………………………………………………….5 1.1.4 Food supplements for animals…………………………………………………………...5 1.1.5 Organic manure……………………………………………………………………………6 1.1.6 Seaweed as a renewable energy source………………………………………………...6 1.1.7 Cosmetics……………………………………………………………………………………7 1.1.8 Traditional medicinal uses of seaweed………………………………………………….7 1.2 Marine algal components……………………………………………………………….…8 1.2.1 Protein/Nitrogen……………………………………………………………………………8 1.2.2 Lipids…………………………………………………………………………………………9 1.2.3 Minerals……………………………………………………………………………………10 1.2.4 Vitamins……………………………...………………………………….…………………11 1.2.5 Polysaccharides……………………...…………………………………………………...12 1.2.5.1 Polysaccharides in green marine algae……………………………………..….12 1.2.5.1 Polysaccharides in red marine algae…………………………………..……….13 1.2.5.3 Polysaccharides in brown marine algae………………………………..………13 1.2.6 Polyphenols………………………………………………………………………………..17 1.2.7 Carotenoids…………………………………………………………………………….….20 II 1.3 The Health promoting properties of macroalgal derived antioxidants……………………22 1.4 Specific seaweeds investigated in the present study……………………….…………….23 1.4.1 Laminaria digitata…………………………………………………………………………..24 1.4.2 Fucus serratus……………………………………………………………………………….26 1.4.3 Gracilaria gracilis…………………………………………………………………………..27 1.4.4 Codium fragile…………………………………...………………………………………….28 1.4.5 Cystoseira nodicaulis……………………………………………………………………….29 1.4.6 Fucus vesiculosus…………………………………………………………………………...30 1.4.7 Himanthalia elongata……………………………………...……………………………….32 1.5 Extraction of antioxidant compounds from macroalgae………………………..…………33 1.5.1 Solid liquid extraction (SLE)………………………...…………………………………….34 1.5.2 Pressurised liquid extraction (PLE)…………………..………………………………….40 1.5.3 Supercritical fluid extraction (SFE)………………………………………………..…….41 1.6 Fractionation and purification of bioactive compounds……………………………….….45 1.6.1 Dialysis……………………………………………………………………………………….46 1.6.2 Flash chromatography………….……………………………………………...…...47 1.6.3 Solid-phase extraction………………………………………………………...……………47 1.7 Measurement of in-vitro antioxidant activity…………………………………..…………49 1.7.1 2, 2-Diphenyl-1-picryl-hydrazyl (DPPH) assay……………………………...…………51 1.7.2 Ferric reducing antioxidant power (FRAP) assay…...…………………………………52 1.7.3 Food Compositional bioassays………………………………………………………...….53 1.7.3.1 Total phenolic content (TPC)…………………………………………………………..53 1.8 Compositional determination of algal biomass…………………………………………...54 1.8.1 Protein determination………………………………………………………………………54 1.8.2 Carbohydrate determination………………………………………………………………55 1.8.3 Ash and mineral determination……………………………………………………………56 1.8.4 Lipid determination…………………………………………………………………………58 1.8.5 Moisture determination…………………………………………………………………….59 1.9 Structural elucidation and analysis of bioactive compounds from macroalgae…………..60 1.9.1 HPLC analysis of antioxidant compounds from macroalgae…………………………61 1.9.2 UPLC-MS of antioxidant compounds…………………………………………………….62 III 1.9.3 Matrix-assissted-laser desorption/ionization mass spectrometry (MALDI-MS) of algal sugars………………………………………………………………………………………………....63 1.10 Factors affecting the antioxidant content of macroalgae……...……………………...64 1.10.1 Salinity……………………………………………………………………………….……..65 1.10.2 Temperature….…………………………………………………………………………….65 1.10.3 Nutrient availability……………………………………………………………………….66 1.10.4 UV-exposure………………………………………………………………………………..66 1.10.5 Dehydration…………………………………………………………………………………67 .1.10.6 Maturity……………………………………………………………………………………..68 Objective of Thesis…….…………………………………………………………………..69 References……………………….…………………………………………………………72 Chapter 2. Comparison of pressurized liquid extraction and solid-liquid extraction in the recovery of antioxidant compounds from four Irish origin macroalgae…………………………96 Abstract……………………………………………………………………………………..97 2.0 Introduction……………………………………………………………………………..97 2.1 Materials and methods………………………………………...……………………..100 2.1.1 Chemicals………………………...…………………………………………...….100 2.1.2 Macroalgal material…………………...…………………………………………101 2.1.3 Solid-liquid extraction (SLE)………………...………………………………………….101 2.1.4 Pressurized liquid extraction (PLE)………………………………………………….102 2.1.5 Total phenolic content (TPC)………………………………………………………….103 2.1.6 In-vitro antioxidant activity……………………………………………………………103 2.1.6.1 Ferric reducing antioxidant power (FRAP)…………………………………..103 2.1.6.1 2, 2-diphenyl-1-picryl-hydrazyl (DPPH) scavenging activity…………………104 2.1.7 Statistical analysis…………………………………………………………………….…..105 2.2 Results and discussion…………………………………………………………………106 2.2.1 Extraction yield…………………………………………………………………………….106 2.2.2 Total phenolic content……………………………………………………………………..107 2.2.3 In-vitro antioxidant activity……………………………………………………………….112 2.3 Conclusion……………………………………………………………………………..115 IV References…………………………………………………………………………………116 Chapter 3. Antioxidant activities and Phenolic content of enriched fractions from four selected Irish macroalgae species (Laminaria digitata, Fucus serratus, Gracilaria gracilis and Codium fragile)…………………………………………………………………………………………..120 Abstract……………………………………………………………………………………121 3.0 Introduction……………………………………………………………………………121 3.1 Materials and methods…………………………………………………………………124 3.1.1 Chemicals…………………………………………………………………………………..124 3.1.2 Macroalgal materials……………………………………………………………………..124 3.1.3 Preparation of crude seaweed extracts…………………………………………………125 3.1.4 Preparation of molecular weight cut-off and hydrophobic fractions………………126 3.1.5 Reverse-phase (RP) flash chromatography……………………………………………127 .3.1.6 Assays for antioxidant activities…………………………………………………………127 3.1.6.1 Ferric reducing antioxidant power (FRAP) assay………………………………127 3.1.6.2 DPPH (2, 2-Diphenyl-1-picryl-hydrazyl) scavenging activity…………………127 3.1.6.3 Determination of total phenolic content…..……………………………………….128 3.1.7 Quadrupole time-of-flight mass spectrometry………………………………………….128 3.1.8 Statistical analysis…………………………………………………………………………128 3.2 Results…………………………………………………………………………………129 3.2.1 Total phenolic content (TPC) of MWCO fractions…………………………………….129 3.2.2 DPPH activity………………………………………………………………………………129 3.2.3 Ferric reducing antioxidant power (FRAP)…………………………………………….134 3.2.4 Phlorotannin enrichment in low molecular weight fractions if Fucus serratus.…..135 3.2.5 Total phenolic content (TPC) and in vitro antioxidant activity of phlorotannin enriched fractions…………………………………………………………………………………………136 3.2 Discussion……………………………………………………………………………..142 3.4 Conclusion……………………………………………………………………………..147 References…………………………………………………………………………………149 V Chapter 4. Profiling of the molecular weight and structural isomer abundance of macroalgae derived phlorotannins………………………………………………………….………………..152 Abstract……………………………………………………………………………………153 4.0 Introduction……………………………………………………………………………154 4.1 Materials and methods………………………………………………………………...156 4.1.1 Standards and reagents…………………………………………………………………..156 4.1.2 Macroalgal samples………………………………………………………………………156 4.1.3 Solid-liquid extraction (SLE)…………………………………………………………….157 4.1.4 Partitioning and molecular weight cut-off (MWCO) dialysis……………….…...….157 4.1.5 Reversed-phase flash chromatography…………………………………………………157 4.1.6 Total phenolic content (TPC)…………………………………………………………….158 4.1.7 In-vitro antioxidant activity………………………………………………………………158 4.1.7.1 Ferric reducing antioxidant power (FRAP).…………………………………….158 4.1.7.2 DPPH (2, 2- Diphenyl-1-picryl-hydrazyl) scavenging activity……………….158 4.1.8 Statistical analysis………………………………………………………………………...158 4.1.9 UPLC-ESI-MS of phlorotannin enriched fractions…………………………………...159 4.2 Results and discussion…………………………………………………………………159 4.2.1 Total phenolic content (TPC) and in-vitro antioxidant activities…………………...159 4.2.2 UPLC-QQQ-MS profiling of phlorotannin enriched fractions………………………161 4.3 Conclusion……………………………………………………………………………..173 References…………………………………………………………………………………175 Chapter 5. Seasonal and geographical variation of the nutritional
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