Abstract
Pressurized liquid extraction (PLE), an environmentally friendly technique, has been used to obtain antiviral compounds from microalgae commonly used as carotenoid sources: Haematococcus pluvialis and Dunaliella salina. The antiviral properties of PLE extracts (hexane, ethanol and water) were evaluated against herpes simplex virus type 1 (HSV-1) at different stages during viral infection. Pretreatment of Vero cells with 75 μg mL−1 of H. pluvialis ethanol extract inhibited virus infection by approximately 85%, whereas the same concentration of water and hexane extracts reduced the virus infectivity 75% and 50%, respectively. D. salina extracts were less effective than H. pluvialis extracts and presented a different behaviour since water and ethanol extracts produced a similar virus inhibition (65%). Moreover, H. pluvialis ethanol extract was also the most effective against HSV-1 intracellular replication. The antiviral activity of water PLE extracts was found to correlate with polysaccharides since the polysaccharide-rich fraction isolated from these extracts showed higher antiviral activity than the original water extracts. A gas chromatography-mass spectrometry (GC-MS) characterization of the H. pluvialis ethanol extract showed the antiviral activity of this extract could be partially related with the presence of short-chain fatty acids, although other compounds could be involved in this activity; meanwhile, in the case of D. salina ethanol extract other compounds seemed to be implied, such as: β-ionone, neophytadiene, phytol, palmitic acid and α-linolenic acid. The results demonstrate the use of PLE allows obtaining antiviral compounds from microalgae used as carotenoids sources, which gives the microalgae biomass an added value.
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Abbasi A, Amiri S (2008) Emulsifying behavior of an exopolysaccharide produced by Enterobacter clocae. African J Biotechnol 7:1574–1576
Aranzaldi M, Sottofattori E, Rizetto R, Granello B, Balbi A (1999) Synthesis and antimicrobial activity of heterocyclic ionone-like derivatives. Eur J Med Chem 34:837–842
Borowitzka MA, Huisman JM, Osborn A (1991) Culture of the asthaxanthin-producing green alga Haematococcus pluvialis. I. Effects of nutrients on growth and cell type. J Appl Phycol 3:295–304
Cherrington CA, Hinton M, Mead GC, Chopra I (1991) Organic acids: chemistry, antibacterial activity, and practical applications. Adv Microb Physiol 32:87–95
Dai J, Wu Y, Chen S, Zhu S, Yin H, Wang M, Tang J (2010) Sugar compositional determination of polysaccharides from Dunaliella salina by modified RP-HPLC method of precolumn derivatization with 1-phenyl-3-methyl-5-pyrazolone. Carbohydr Res 82:629–635
Damiani MC, Leonardi PI, Pieroni OI, Cáceres EJ (2006) Ultrastructure of the cyst wall of Haematococcus pluvialis (Chlorophyceae): wall development and behavior during cyst germination. Phycologia 45:616–623
Damonte EB, Matulewicz MC, Cerezo AS (2004) Sulfated seaweed polysaccharides as antiviral agents. Curr Med Chem 11:2399–2419
Denery JR, Dragull K, Tang CS, Li QX (2004) Pressurized fluid extraction of carotenoids from Haematococcus pluvialis and Dunaliella salina and kavalactones form Piper methysticum. Anal Chim Acta 501:175–179
Duarte MER, Noseda DG, Noseda MD, Tulio S, Pujol CA, Damonte EB (2001) Inhibitory effect of sulfathed galactans from marine alga Bostrychia montagnei on herpes simplex virus replication in vitro. Phytomedicine 81:53–58
Dufossé L, Galaup P, Yaron A, Arad SM, Blanc P, Murthy KNC, Ravishankar GA (2005) Microorganisms and microalgae as sources of pigments for food use: a scientific oddity or an industrial reality? Trends Food Sci Technol 16:389–406
Fabregas J, García D, Fernandez-Alonso M, Rocha AI, Gómez-Puertas P, Escribano JM, Otero A, Coll JM (1999) In vitro inhibition of the replication of haemorrhagic septicemia virus (VHSV) and African swine fever virus (ASFV) by extracts from marine microalgae. Antiviral Res 44:67–73
Fox JD, Robyt JF (1991) Miniaturization of three carbohydrate analysis using a microsample plate reader. Anal Biochem 1:93–96
Ghosh P, Adhikari U, Ghosal PK, Pujol CA, Carlucci MJ, Damonte EB, Ray B (2004) In vitro anti-herpetic activity of sulfated polysaccharide fractions from Caulerpa racemosa. Phytochemistry 65:3151–3157
Guang-Zhou L, Tiao-Yin L, John TAH (2004) Anti-HCV activities of selective polyunsaturated fatty acids. Biochem Biophys Res Commun 318:275–280
Hagen C, Siegmund S, Braune W (2002) Ultrastructural and chemical changes in the cell wall of Haematococcus pluvialis (Volvocales, Chlorophyta) during aplanospore formation. Eur J Phycol 37:217–226
Hayashi T, Hayashi K, Maeda M, Kojima I (1996) Calcium spirulan, an inhibitor of enveloped virus replication, from a blue-green alga Spirulina platensis. J Nat Prod 59:83–87
Herrero M, Ibáñez E, Cifuentes A, Reglero G, Santoyo S (2006) Dunaliella salina microalga pressurized liquid extracts as potential antimicrobials. J Food Prot 69:2478–2477
Jeurink PV, Lull-Noguera C, Savelkoul HFJ, Wichers HJ (2008) Immunomodulatory capacity of fungal proteins on the cytokine production of human peripheral blood mononuclear cells. Int Immunopharmacol 8:1124–1133
King JW (2000) Advances in critical fluid technology for food processing. Food Sci Technol Tod 14:186–189
Lee JB, Srisomporn P, Hayashi K, Tanaka T, Sankawa U, Hayashi T (2001) Effects of structural modification of calcium spirulan, a sulfated polysaccharide from Spirulina platensis, on antiviral activity. Chem Pharm Bull 49:108–110
Mahmoud H, Ishanu V, Tal J, Arad S (2002) Activity of Porphyridium sp. polysaccharide against herpes simplex viruses in vitro and in vivo. J Biochem Biophys Methods 50:189–200
Mandal P, Mateu CG, Chattopadhyay K, Pujol CA, Damonte EB, Ray B (2007) Structural features and antiviral activity of sulphated fucans from the brown seaweed Cystoseira indica. Antivir Chem Chemother 18:153–162
Mayer AMS, Hamann MT (2005) Marine pharmacology in 2001–2002: Marine compounds with antihelmintic, antibacterial, anticoagulant, antidiabetic, antifungal, anti-inflammatory, antimalarial, antiplatelet, antiprotozoal, antituberculosis, and antiviral activities; affecting the cardiovascular, immune and nervous systems and other miscellaneous mechanisms of action. Comp Biochem Phycol C 140:265–286
Mayer AMS, Rodriguez AD, Berlinck RBS, Hamann MT (2009) Marine pharmacology in 2005–2006: Marine compounds with antihelmintic, antibacterial, anticoagulant, antidiabetic, antifungal, anti-inflammatory, antimalarial, antiplatelet, antiprotozoal, antituberculosis, and antiviral activities; affecting the cardiovascular, immune and nervous systems and other miscellaneous mechanisms of action. Biochim Biophys Acta 1790:283–308
Mbandi E, Shelef LA (2002) Enhanced antimicrobial effects of combination of lactate and diacetate on Listeria monocytogenes and Salmonella spp. in beef bologna. Int J Food Microbiol 76:191–198
Mendes RL, Nobre BP, Cardoso MT, Pereira AP, Palabra AF (2003) Supercritical carbon dioxide extraction of compounds with pharmaceutical importance from microalgae. Inorg Chim Acta 356:328–334
Mishra A, Jha B (2009) Isolation and characterization of extracellular substances from microalgae Dunaliella salina under salt stress. Bioresour Technol 100:3382–2286
Monsant A, Zarka A, Boussiba S (2001) Presence of a nonhydrolyzable biopolymer in the cell wall of vegetative cells and astaxanthin-rich cysts of Haematococcus pluvialis (Chlorophyceae). Mar Biotechnol 3:515–521
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63
Nakayama T, Watanabe S, Mitsui K, Uchida H, Inouye I (1996) The phylogenetic relationship between the Chlamydomonadales and Chlorococcales inferred from 18S rDNA data. Phycol Res 44:47–55
Nichols HW, Bold HC (1964) Trichsarcina polymorpha gen. et sp. nov. J Phycol 1:34–39
Orhan I, Deliorman-Orhan D, ÖzÇelik B (2009) Antiviral activity and cytotoxicity of the lipophilic extracts of various edible plants and their fatty acids. Food Chem 115:701–705
Rechter S, König T, Auerochs S, Thulke S, Walter H, Dörnenburg H, Walter C, Marschall M (2006) Antiviral activity of Arthrospira-derived spirulan-like substances. Antiviral Res 72:197–206
Rodriguez-Meizoso I, Jaime L, Santoyo S, Cifuentes A, García-Blairsy Reina G, Señorans FJ, Ibañez E (2008) Pressurized fluid extraction of bioactive compounds from Phormidium sp. J Agric Food Chem 56:3517–3523
Santoyo S, Herrero M, Señorans FJ, Cifuentes A, Ibañez E, Jaime L (2006) Functional characterization of pressurized liquid extracts of Spirulina platensis. Eur Food Res Technol 224:75–81
Santoyo S, Rodríguez-Meizoso I, Cifuentes A, Jaime L, García-Blairsy Reina G, Señorans FJ, Ibañez E (2009) Green processes based on the extraction with pressurized fluids to obtain potent antimicrobials from Haematococcus pluvialis microalgae. LWT-Food Sci Tech 42:1213–1218
Santoyo S, Plaza M, Jaime L, Ibañez E, Reglero G, Señorans FJ (2010a) Pressurized liquid extraction as an alternative process to obtain antiviral agents from the edible microalga Chlorella vulgaris. J Agric Food Chem 58(8522–8527):692
Santoyo S, Plaza M, Jaime L, Ibañez E, Reglero G, Señorans FJ (2010b) Pressurized liquids as an alternative green process to extract antiviral agents from the edible seaweed Himanthalia elongata. J Appl Phycol. doi:10.1007/s10811-010-9611-x
Sommer TR, Pott W, Morrissy NM (1991) Utilization of microalgal asthaxanthin by rainbow trout (Oncorhynchus mykiss). Aquaculture 94:79–88
Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96
Yff BTS, Linsey KL, Taylor MB, Erasmus DG, Jäger AK (2002) The pharmacological screening of Pentanisia prunelloides and the isolation of the antibacterial compound palmitic acid. J Etnopharm 79:101–107
Zheng SZ, Wang DY, Zhang Q, Shen XW (1997) Chemical studies on the polysaccharide from Dunaliella salina. J Northwest Normal University 33:93–95
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This work has been financed by the Spanish Ministry of Education and Science (AGL2005-06726-C04), the programme CONSOLIDER-INGENIO 2010 (CDS2007-00063) and the regional programme ALIBIRD-CM S-0505/AGR-0153 from the Comunidad de Madrid, Spain.
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Santoyo, S., Jaime, L., Plaza, M. et al. Antiviral compounds obtained from microalgae commonly used as carotenoid sources. J Appl Phycol 24, 731–741 (2012). https://doi.org/10.1007/s10811-011-9692-1
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DOI: https://doi.org/10.1007/s10811-011-9692-1