Advertisement

Production of Primary and Secondary Metabolites Using Algae

  • Milagros Rico
  • Aridane G. González
  • Magdalena Santana-Casiano
  • Melchor González-Dávila
  • Norma Pérez-Almeida
  • Miguel Suarez de Tangil
Chapter

Abstract

Over the past few decades, there has been an increase in the number of research studies focused on all aspects of the ecology, physiology, biochemistry, cell biology, molecular biology, systematics and uses of algae. This chapter will provide an overview of the potential human health advantages associated with the use of algae as a source of high-value products, especially focused on those metabolites with biological activities and potential therapeutic applications in the pharmaceutical and food industries. Moreover, the production of polyphenols by marine microalgae will be also considered, as well their impact on the biogeochemical cycles of trace metals and the phytoplankton implications. These data will support as a baseline for future research in wastewater and marine environments.

Notes

Acknowledgements

Authors thank the Project CTM2014-52342-P given by the Ministerio de Economia y Competitividad from Spain. Aridane G. Gonzalez thanks the French “Agence Nationale de la Recherche” through the “Laboratoire d’Excellence” LabexMER (ANR-10-LABX-19-01) program, and co-funded by a grant from the French government through the “Investissements d’Avenir” and the Brittany Region.

References

  1. Abd El Baky HH, El Baz FK, El-Barouty GS (2003) Spirulina species as a source of carotenoids and α-tocopherol and its anticarcinoma factors. Biotechnol 3:222–240Google Scholar
  2. Abd El Baky HH, Hanaa El Baz KF, EL-Latife SA (2013) Induction of sulfated polysaccharides in Spirulina platensis as response to nitrogen concentration and its biological evaluation. J Aquac Res Development 5:206, 8 pagesGoogle Scholar
  3. Abd El Baky HH, El-Baroty GS, Ibrahim AE, El Baz FK (2014) Cytotoxicity, antioxidants and antimicrobial activities of lipids extracted from some marine algae. J Aquac Res Dev 5:284, 5 pagesGoogle Scholar
  4. Abd El Baky HH, El Baz FK, El Baroty GS, Asker MMS, Ibrahim EA (2014b) Phospholipids of some marine macroalgae: identification, antivirus, anticancer and antimicrobial bioactivities. Der Pharma Chemica 6:370–382Google Scholar
  5. Abreu MH, Pereira R, Sassi JF (2014) Marine algae and the global food industry. In: Pereira L, Neto JM (eds) Marine algae: biodiversity, taxonomy. Environmental assessment and biotechnology. CRC Press, pp 300–319Google Scholar
  6. Ahn JH, Yang YI, Lee KT, Choi JH (2015) Dieckol, isolated from the edible brown algae Ecklonia cava, induces apoptosis of ovarian cancer cells and inhibits tumor xenograft growth. J Cancer Res Clin Oncol 141:255–268CrossRefPubMedGoogle Scholar
  7. Ahmadi A, Moghadamtousi SZ, Abubakar S, Zandi K (2015) Antiviral potential of algae polysaccharides isolated from marine sources: a review. In: BioMed research international. Article ID 825203, 10 pagesGoogle Scholar
  8. Andersen G, Harnack K, Erbersdobler HF, Somoza V (2008) Dietary eicosapentaenoic acid and docosahexaenoic acid are more effective than alpha-linolenic acid in improving insulin sensitivity in rats. Ann Nutr Metab 52:250–256CrossRefPubMedGoogle Scholar
  9. Aprioku JS (2013) Pharmacology of free radicals and the impact of reactive oxygen species on the testis. J Reprod Infertil 14:158–172PubMedPubMedCentralGoogle Scholar
  10. Barahona T, Encinas MV, Imarai M, Mansilla A, Matsuhiro B, Torres R, Valenzuela B (2014) Bioactive polysaccharides from marine algae. Bioactive Carbohydr Diet Fibre 4:125–138CrossRefGoogle Scholar
  11. Beardal J, Raven, JA (2012) Algal metabolism. In: eLS Chichester. WileyGoogle Scholar
  12. Becker W (2004) 18 Microalgae in human and animal nutrition. Handbook of microalgal culture: biotechnology and applied phycology, p 312Google Scholar
  13. Becker EW (2007) Micro-algae as a source of protein. Biotech Adv 25(2):207–210Google Scholar
  14. Boopathy NS, Kathiresan K (2010) Anticancer drugs from marine flora: an overview. J Oncol Article ID 214186, 18 pagesGoogle Scholar
  15. Borowitzka MA (1995) Microalgae as sources of pharmaceuticals and other biologically active compounds. J Appl Phycol 7:3–15CrossRefGoogle Scholar
  16. Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756CrossRefGoogle Scholar
  17. Bourgaud F, Gravot A, Milesi S, Gontier E (2001) Production of plant secondary metabolites: a historical perspective. Plant Sci 161:839–851CrossRefGoogle Scholar
  18. Brit DF, Hendrich S, Wang W (2001) Dietary agents in cancer prevention: flavonoids and isoflavonoids. Pharmacol Ther 90:157–177CrossRefGoogle Scholar
  19. Castro LFC, Tocher DR, Monroig O (2016) Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire. Prog Lipid Res 62:25–40CrossRefPubMedGoogle Scholar
  20. Chu WL, Phang SM, Goh SH (1994) Studies on the production of useful chemicals, especially fatty acids in the marine diatom Nitzschia conspicua Grunow. In: Ecology and conservation of southeast Asian marine and freshwater environments including wetlands. Springer, Netherlands, pp 3–40Google Scholar
  21. Clifford MN Appendix 1. A nomenclature for phenols with special reference to tea. Washington, DC, 11/1999, CRC Press LLC: Boca Raton, Florida, vol 41, Supplement 5, pp 393–397Google Scholar
  22. Cornish ML, Garbary DJ (2010) Antioxidants from macroalgae: potential applications in human health and nutrition. Algae 25:155–171CrossRefGoogle Scholar
  23. Dai J, Mumper RJ (2010) Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15:7313–7352CrossRefPubMedGoogle Scholar
  24. Damonte E, Neyts J, Pujol CA, Snoeck R, Andrei G, Ikeda S, Witvrouw M, Reymen D, Haines H, Matulewicz MC, Cerezo A, Coto CE, de Clercq E (1994) Antiviral activity of a sulphated polysaccharide from the red seaweed Nothogenia fastigiata. Biochem Pharmacol 47:2187–2192CrossRefPubMedGoogle Scholar
  25. De Clercq E (1996) Chemotherapy of human immunodeficiency virus (HIV) infection: anti-HIV agents targeted at early stages in the virus replicative cycle. Biomed Pharmacother 50:207–215CrossRefPubMedGoogle Scholar
  26. Del Campo JA, Moreno J, Rodrı́guez H, Vargas MA, Rivas J, Guerrero MG (2000) Carotenoid content of chlorophycean microalgae: factors determining lutein accumulation in Muriellopsis sp. (Chlorophyta). J Biotech 76:51–59Google Scholar
  27. Ehresmann DW, Deig EF, Hatch MT (1979) Antiviral properties of algal polysaccharides and related compounds. In: Hoppe HA et al (eds) Marine algae in pharmaceutical science. W de Gruyter, NY, pp 293–302Google Scholar
  28. El Baz FK, Aboul-Enein AM, El-Baroty GS, Youssef AM, Abdel-Baky HH (2002) Accumulation of antioxidant vitamins in Dunaliella salina. J Biol Sci 2:220–223CrossRefGoogle Scholar
  29. Fan X, Bai L, Zhu L, Yang L, Zhang X (2014) Marine algae-derived bioactive peptides for human nutrition and health. J Agric Food Chem 62:9211–9222CrossRefPubMedGoogle Scholar
  30. Farvin KHS, Jacobsen C (2013) Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem 138:1670–1681CrossRefGoogle Scholar
  31. Fassett RG, Coombes JS (2011) Astaxanthin: a potential therapeutic agent in cardiovascular disease. Mar Drugs 9:447–465CrossRefPubMedPubMedCentralGoogle Scholar
  32. Flora SJ (2009) Structural, chemical and biological aspects of antioxidants for strategies against metal and metalloid exposure. Oxid Med Cell Longev 2:191–206CrossRefPubMedPubMedCentralGoogle Scholar
  33. Foley TL, Simeonov A (2012) Targeting iron assimilation to develop new antibacterials. Expert Opin Drug Discov 7:831–847CrossRefPubMedPubMedCentralGoogle Scholar
  34. Ghazala B, Nailaand B, Shameel M (2010) Fatty acids and biological activities of crude extracts of freshwater algae from sindh. Pak J Bot 42:1201–1212Google Scholar
  35. Graf BA, Milbury PE, Blumberg JB (2005) Flavonols, flavonones, flavanones and human health: epidemological evidence. J Med Food 8:281–290CrossRefPubMedGoogle Scholar
  36. Guedes AC, Amaro HM, Malcata FX (2011) Microalgae as sources of carotenoids. Mar Drugs 9:625–644CrossRefPubMedPubMedCentralGoogle Scholar
  37. Grima EM, Belarbi EH, Fernández FA, Medina AR, Chisti Y (2003) Recovery of microalgal biomass and metabolites: process options and economics. Biotech Adv 20:491–515CrossRefGoogle Scholar
  38. Gupta S, Abu-Ghannam N (2011) Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci Technol 22:315–326CrossRefGoogle Scholar
  39. Gylling H, Plat J, Turley S, Ginsberg HN, Ellegård L, Jessup W, Jones PJ, Lütjohann D, Maerz W, Masana L, Silbernagel G, Staels B, Borén J, Catapano AL, De Backer G, Deanfield J, Descamps OS, Kovanen PT, Riccardi G, Tokgözoglu L, Chapman MJ (2014) Plant sterols and plant stanols in the management of dyslipidaemia and prevention of cardiovascular disease. Atherosclerosis 232:346–360CrossRefPubMedGoogle Scholar
  40. Han D, Li Y, Hu Q (2013) Astaxanthin in microalgae: pathways, functions and biotechnological implications. Algae 28:131–147CrossRefGoogle Scholar
  41. Hartmann A, Albert A, Ganzera M (2015) Effects of elevated ultraviolet radiation on primary metabolites in selected alpine algae and cyanobacteria. J Photochem Photobiol B 149:149–155CrossRefPubMedPubMedCentralGoogle Scholar
  42. Harwood JL, Guschina IA (2009) The versatility of algae and their lipid metabolism. Biochimie 91:679–684CrossRefPubMedGoogle Scholar
  43. Hejazi MA, Wijffels RH (2004) Milking of microalgae. Trends Biotechnol 22:189–194CrossRefPubMedGoogle Scholar
  44. Hertog MGL, Feskens EJM, Hollman PCH, Katan MB, Kromhout D (1993) Dietary antioxidant flavonoids and risk of coronary heart disease. Zutphen Elder Study Lancet 342:1007–1011Google Scholar
  45. Hossain Z, Kurihara H, Hosokavca M, Takahashp K (2005) Growth inhibition and induction of differentiation and apoptosis mediated by sodium butyrate in caco-2 cells with algal glycolipids. In Vitro Cell Dev Biol Animal 41:154–159CrossRefGoogle Scholar
  46. Hussain MdS, Fareed S, Ansari S, Rahman MdA, Ahmad IZ, Saeed M (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 4:10–20CrossRefPubMedPubMedCentralGoogle Scholar
  47. Jin ES, Melis A (2003) Microalgal biotechnology: carotenoid production by the green algae Dunaliella salina. Biotech Bioprocess Eng 8:331CrossRefGoogle Scholar
  48. Jomova K, Valkoa M (2011) Importance of iron chelation in free radical-induced oxidative stress and human disease. Curr Pharm Des 17:3460–3473CrossRefPubMedGoogle Scholar
  49. Kang HS, Chung HY, Kim JY, Son BW, Jung HA, Choi JS (2004) Inhibitory phlorotannins from the edible brown alga Ecklonia stolonifera on total reactive oxygen species (ROS) generation. Arch Pharm Res 27:194–198CrossRefPubMedGoogle Scholar
  50. Kang HK, Seo CH, Park Y (2015a) Marine peptides and their anti-infective activities. Mar Drugs 13:618–645CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kang HK, Seo CH, Park Y (2015b) The effects of marine carbohydrates and glycosylated compounds on human health. Int J Mol Sci 16:6018–6056CrossRefPubMedPubMedCentralGoogle Scholar
  52. Kellogg J, Grace MH, Lila MA (2014) Phlorotannins from Alaskan seaweed inhibit carbolytic enzyme activity. Mar Drugs 12:5277–5294CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kim MM, Ta QV, Mendis E, Rajapakse N, Jung WK, Byun HG, Jeon YJ, Kim SK (2006) Phlorotannins in Ecklonia cava extract inhibit matrix metalloproteinase activity. Life Sci 79:1436–1443Google Scholar
  54. Kim SK, Kang KH (2011) Medicinal effects of peptides from marine microalgae. Adv Food Nutr Res 64:313–323CrossRefPubMedGoogle Scholar
  55. Kim TH, Ku SK, Bae JS (2012) Antithrombotic and profibrinolytic activities of eckol and dieckol. J Cell Biochem 113:2877–2883CrossRefPubMedGoogle Scholar
  56. Kiriyama S, Okazaki Y, Yoshida A (1969) Hypocholesterolemic effect of polysaceharides and polysaccharide-rich foodstuffs in cholesterol-fed rats. J Nutr 97:382–388PubMedGoogle Scholar
  57. Klaunig JE, Kamendulis LM (2004) The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 44:239–267CrossRefPubMedGoogle Scholar
  58. Koivikko R, Loponen J, Pihlaja K, Jormalainen V (2007) High-performance liquid chromatographic analysis of phlorotannins from the brown alga Fucus vesiculosus. Phytochem Anal 18:326–332CrossRefPubMedGoogle Scholar
  59. Kotake-Nara E, Terasaki M, Nagao A (2005) Characterization of apoptosis induced by fucoxanthin in human promyelocytic leukemia cells. Biosci Biotechnol Biochem 69:224–227CrossRefPubMedGoogle Scholar
  60. Kumar SR, Hosokawa M, Miyashita K (2013) Fucoxanthin: a marine carotenoid exerting anti-cancer effects by affecting multiple mechanisms. Mar Drugs 11:5130–5147CrossRefPubMedPubMedCentralGoogle Scholar
  61. Kumari P, Kumar M, Reddy CRK, Jha, B (2013) Algal lipids, fatty acids and sterols. In Dominguez H (ed) Functional ingredients from algae for foods and nutraceuticals. Woodhead Publishing, pp 87–134Google Scholar
  62. Lambert JD, Yang CS (2003) Mechanisms of cancer prevention by tea constituents. J Nutr 133(Suppl):3262S–3267SPubMedGoogle Scholar
  63. Lamela M, Anca J, Villar R, Otero J, Calleja JM (1989) Hypoglycemic activity op several seaweed extracts. J Ethnopharmacol 27:35–43CrossRefPubMedGoogle Scholar
  64. Lee SH, Jeon YJ (2015) Efficacy and safety of a dieckol-rich extract (AG-dieckol) of brown algae, ecklonia cava, in pre-diabetic individuals: a double-blind, randomized, placebo-controlled clinical trial. Food Funct 6:853–858CrossRefPubMedGoogle Scholar
  65. Lee TK, Kottuparambil S, Kim YJ, Rhee JS, Choi EM, Brown MT, Häder DP, Taejun H (2014) Ultraviolet radiation and cyanobacteria. J Photochem Photobiol B 141:154–169CrossRefPubMedGoogle Scholar
  66. Leopoldini M, Russo N, Toscano M (2011) The molecular basis of working mechanism of natural polyphenolic antioxidants. Food Chem 125:288–306CrossRefGoogle Scholar
  67. Leu S, Boussiba S (2014) Advances in the production of high-value products by microalgae. Ind Biotechnol 10:169–183CrossRefGoogle Scholar
  68. Li Y-X, Wijesekara I, Li Y, Kim S-K (2011) Phlorotannins as bioactive agents from brown algae. Process Biochem 46:2219–2224CrossRefGoogle Scholar
  69. Li A-N, Li S, Zhang Y-J, Xu X-R, Chen Y-M, Li H-B (2014) Resources and biological activities of natural polyphenols. Nutrients 6:6020–6047CrossRefPubMedPubMedCentralGoogle Scholar
  70. López A, Rico M, Santana-Casiano JM, Gonzaléz AG, González-Dávila M (2015) Phenolic profile of Dunaliella tertiolecta growing under high levels of copper and iron. Environ Sci Pollut Res 22:14820–14828CrossRefGoogle Scholar
  71. Luo X, Su P, Zhang W (2015) Advances in microalgae-derived phytosterols for functional food and pharmaceutical applications. Mar Drugs 13:4231–4254CrossRefPubMedPubMedCentralGoogle Scholar
  72. Machu L, Misurcova L, Ambrozova JV, Orsavova J, Mlcek J, Sochor J, Jurikova T (2015) Phenolic content and antioxidant capacity in algal food products. Molecules 20:1118–1133CrossRefPubMedGoogle Scholar
  73. Mandel SA, Amit T, Zheng H, Weinreb O, Youdim MBH (2006) The essentiality of iron chelation in neuroprotection: a potential role of green tea catechins. In: Luo Y, Packer L (eds) Oxidative stress and disease. CRC Press, pp 277–299Google Scholar
  74. Mata TM, Antonio A, Martins N, Caetano S (2010) Microalgae for biodiesel production and other applications: a review. Renew Sustain Energy Rev 14:217–232CrossRefGoogle Scholar
  75. Metting FB Jr (1996) Biodiversity and application of microalgae. J Ind Microbiol 17:477–289Google Scholar
  76. Mezzomo N, Ferreira SRS (2016) Carotenoids functionality, sources, and processing by supercritical technology: A review. J Chem vol. 2016, Article ID 3164312, 16 pagesGoogle Scholar
  77. Michalak I, Chojnacka K (2015) Algae as production systems of bioactive compounds. Eng Life Sci 15:160–176CrossRefGoogle Scholar
  78. Mikami K, Hosokawa M (2013) Biosynthetic pathway and health benefits of fucoxanthin, an algae-specific xanthophyll in brown seaweeds. Int J Mol Sci 14:13763–13781CrossRefPubMedPubMedCentralGoogle Scholar
  79. Norton TA, Melkonian M, Andersen RA (1996) Algal biodiversity. Phycologia 35:308–326CrossRefGoogle Scholar
  80. Nunomura A, Castellani RJ, Zhu X, Moreira PI, Perry G, Smith MA (2006) Involvement of oxidative stress in Alzheimer disease. J Neuropathol Exp Neurol 65:631–641CrossRefPubMedGoogle Scholar
  81. Panlasigui LN PhD, Baello OQ, Dimatangal JM BSc, Dumelod BD MSc (2003) Blood cholesterol and lipid-lowering effects of carrageenan on human volunteers. Asia Pacific J Clin Nut 12:209–214Google Scholar
  82. Pandey KB, Rizvi SI (2009) Plant polyphenols as dietary antioxidants in human health and disease. Oxid Med Cell Longev 2:270–278CrossRefPubMedPubMedCentralGoogle Scholar
  83. Pangestuti R, Kim SK (2011) Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Foods 3:255–266CrossRefGoogle Scholar
  84. Perron NR, Brumaghim JL (2009) A review of the antioxidant mechanisms of polyphenol compounds related to iron binding. Cell Biochem Biophys 53:75–100CrossRefPubMedGoogle Scholar
  85. Pratt R, Fong J (1940) Studies on Chlorella vulgaris II. Further evidence that Chlorella cells form a growth-inhibiting substance. Am J Bot 27:431–436CrossRefGoogle Scholar
  86. Priyadarshani I, Rath B (2012) Commercial and industrial applications of micro algae—a review. J Algal Biomass Utilization 3:89–100Google Scholar
  87. Quideau S, Deffieux D, Douat-Casassus C, Pouységu L (2011) Plant polyphenols: chemical properties, biological activities, and synthesis. Angew Chem 50:586–621CrossRefGoogle Scholar
  88. Radmer RJ (1996) Algal diversity and commercial algal products. Bioscience 46:263–270CrossRefGoogle Scholar
  89. Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. Prog Phycol Res 4:129–241Google Scholar
  90. Ranga Rao A, Dayananda C, Sarada R, Shamala TR, Ravishankar GA (2007a) Effect of salinity on growth of green alga Botryococcus braunii and its constituents. Bioresour Technol 98:560–564CrossRefPubMedGoogle Scholar
  91. Ranga Rao A, Sarada TR, Ravishankar GA (2007b) Influence of CO2 on growth and hydrocarbon production in Botryococcus braunii. J Microbiol Biotechnol 17:414–419PubMedGoogle Scholar
  92. Ras RT, Hiemstra H, Lin Y, Vermeer MA, Duchateau GSMJE, Trautwein EA (2013) Consumption of plant sterol-enriched foods and effects on plasma plant sterol concentrations—a meta-analysis of randomized controlled studies. Atherosclerosis 230:336–346CrossRefPubMedGoogle Scholar
  93. Rico M, López A, Santana-Casiano JM, González AG, González-Dávila M (2013) Variability of the phenolic profile in the diatom Phaeodactylum tricornutum growing under copper and iron stress. Limnol Oceanogr 58:144–152CrossRefGoogle Scholar
  94. Román RB, Alvarez-Pez JM, Fernández FA, Grima EM (2002) Recovery of pure B-phycoerythrin from the microalga Porphyridium cruentum. J Biotechnol 93:73–85CrossRefGoogle Scholar
  95. Santana-Casiano JM, González-Dávila M, González AG, Rico M, López A, Martel A (2014) Characterization of polyphenol exudates from Phaeodactylum tricornutum and their effects on the chemistry of Fe(II)-Fe(III). Mar Chem 158:10–16CrossRefGoogle Scholar
  96. Satomi Y (2012) Fucoxanthin induces GADD45A expression and G1 arrest with SAPK/JNK activation in LNCap human prostate cancer cells. Anticancer Res 32:807–813PubMedGoogle Scholar
  97. Scala S, Bowler C (2001) Molecular insights into the novel aspects of diatom biology. Cell Mol Life Sci 58:1666–1673CrossRefPubMedGoogle Scholar
  98. Shalaby EA (2011) Algae as promising organisms for environment and health. Plant Signal Behav 6:1338–1350CrossRefPubMedPubMedCentralGoogle Scholar
  99. Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel poduction. Energies 5:1532–1553CrossRefGoogle Scholar
  100. Shimizu Y (1996) Microalgal metabolites: a new perspective. Ann Rev Microbiol 50:431–465CrossRefGoogle Scholar
  101. Shimizu Y (2000) In: Fusetani N (ed) Drugs from the sea. Karger, Basel, pp 30–45CrossRefGoogle Scholar
  102. Shin T, Ahn M, Hyun JW, Kim SH, Moon C (2014) Antioxidant marine algae phlorotannins and radioprotection: a review of experimental evidence. Acta Histochem 116:669–674CrossRefPubMedGoogle Scholar
  103. Siti HN, Kamisah Y, Kamsiah J (2015) The role of oxidative stress, antioxidants and vascular inflammation in cardiovascular disease (a review). Vascul Pharmacol 71:40–56CrossRefPubMedGoogle Scholar
  104. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96CrossRefPubMedGoogle Scholar
  105. Takaichi S (2011) Carotenoids in algae: distributions, biosyntheses and functions. Mar Drugs 9:1101–1118CrossRefPubMedPubMedCentralGoogle Scholar
  106. Yoo C, Jun SY, Lee JY, Ahn CY, Oh HM (2010) Selection of microalgae for lipid production under high levels carbon dioxide. Bioresource Technol 101:S71–S74CrossRefGoogle Scholar
  107. Viskari PJ, Colyer CL (2003) Rapid extraction of phycobiliproteins from cultured cyanobacteria samples. Anal Biochem 319:263–271CrossRefPubMedGoogle Scholar
  108. Wang T, Jónsdóttir R, Ólafsdóttir G (2009) Total phenolic compounds, radical scavenging and metal chelation of extracts from icelandic seaweeds. Food Chem 116:240–248CrossRefGoogle Scholar
  109. Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific Publications, Oxford, Great BritainGoogle Scholar
  110. Wen W, Li K, Alseekh S, Omranian N, Zhao L, Zhou Y, Xiao Y, Jin M, Yang N, Liu H, Florian A, Li W, Pan Q, Nikoloski Z, Yan J, Fernie AR (2015) Genetic determinants of the network of primary metabolism and their relationships to plant performance in a maize recombinant inbred line population. Plant Cell 27:1839–1856CrossRefPubMedPubMedCentralGoogle Scholar
  111. Wijesinghe WAJP, Ko S-C, Jeon Y-J (2011) Effect of phlorotannins isolated from Ecklonia cava on angiotensin I-converting enzyme (ACE) inhibitory activity. Nutr Res Practice 5:93–100CrossRefGoogle Scholar
  112. Witvrouw M, Este JA, Mateu MQ, Reymen D, Andrei G, Snoeck R, Ikeda S, Pauwels R, Bianchini NV, Desmyter J, de Clercq E (1994) Activity of a sulfated polysaccharide extracted from the red seaweed Aghardhiella tenera against human immunodeficiency virus and other enveloped viruses. Antiviral Chem Chemother 5:297–303CrossRefGoogle Scholar
  113. Wood-Kaczmar A, Gandhi S, Wood NW (2006) Understanding the molecular causes of Parkinson’s disease. Trends Mol Med 12:521–528CrossRefPubMedGoogle Scholar
  114. Xue L, Zhang Y, Zhang T, An L, Wang X (2005) Effects of enhanced ultraviolet-B radiation on algae and cyanobacteria. Crit Rev Microbiol 31:79–89CrossRefPubMedGoogle Scholar
  115. Yu X, Chen L, Zhang W (2015) Chemicals to enhance microalgal growth and accumulation of high-value bioproducts. Front Microbiol 6:56, 10 pagesGoogle Scholar
  116. Zhaoa C, Dodina G, Yuanc C, Chena H, Zheng R, Jiac Z, Fana B-T (2005) In vitro protection of DNA from Fenton reaction by plant polyphenol verbascoside. Biochim Biophys Acta 1723:114–123CrossRefGoogle Scholar
  117. Zubia M, Payri C, Deslandes E (2008) Alginate, mannitol, phenolic compounds and biological activities of two range-extending brown algae, Sargassum mangarevense and Turbinaria ornata (Phaeophyta: Fucales), from Tahiti (French Polynesia). J Appl Phycol 20:1033–1043CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Milagros Rico
    • 1
  • Aridane G. González
    • 1
  • Magdalena Santana-Casiano
    • 1
  • Melchor González-Dávila
    • 1
  • Norma Pérez-Almeida
    • 1
  • Miguel Suarez de Tangil
    • 1
  1. 1.Grupo QUIMA, Instituto de Oceanografía y Cambio Global (IOCAG)Universidad de Las Palmas de Gran CanariaLas Palmas de Gran CanariaSpain

Personalised recommendations