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Effects of Ascophyllum nodosum extract on growth and antioxidant defense systems of two freshwater microalgae

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Abstract

Microalgae in genus Chlorella and Scenedesmus are common in aquatic ecosystems and are widely used for various studies on algal growth and applications. Macroalgae may play an important role for control of microalgal growth, attributable to their rich content of bioactive compounds. In this study, the brown seaweed Ascophyllum nodosum was extracted with 70% acetone and the extract was used to treat the green microalgae, Chlorella vulgaris and Scenedesmus sp. Cell density and chlorophyll a concentration were used as growth indexes to evaluate the effects of A. nodosum extract (ANE) on the microalgae. The ANE with concentrations > 1% exhibited significant capability of inhibition of the growth of microalgae by over 80%. On the contrary, 1% ANE caused varying degrees of acceleration of cell proliferation and chlorophyll a synthesis in C. vulgaris and Scenedesmus sp., respectively. Analysis of antioxidant activities of the enzymes superoxide dismutase (SOD) and catalase (CAT) revealed the impact of ANE on the antioxidant defense system of the microalgae. The SOD and CAT activities were significantly depressed by high concentrations (> 2%) ANE, while a slight increase of the enzyme activities was observed with 1% ANE at the early period, which could be correlated to the growth response. Therefore, the mechanism of microalgae control could be related to the interaction between the ANE and the antioxidant defense systems. Phlorotannins are proposed as the principal algistatic components in the ANE which could be utilized in controlling microalgae growth.

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References

  • Abu R, Jiang ZD, Ueno M, Okimura T, Yamaguchi K, Oda T (2013) In vitro antioxidant activities of sulfated polysaccharide ascophyllan isolated from Ascophyllum nodosum. Int J Biol Macromol 59:305–312

    Article  CAS  PubMed  Google Scholar 

  • Aebi H (1974) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 673–684

    Chapter  Google Scholar 

  • Ahn MJ, Yoon KD, Min SY, Lee JS, Kim JH, Kim TG, Kim SH, Kim NG, Huh H, Kim J (2004) Inhibition of HIV-1 reverse transcriptase and protease by phlorotannins from the brown alga Ecklonia cava. Biol Pharm Bull 27:544–547

    Article  CAS  PubMed  Google Scholar 

  • Alam MA, Wan C, Zhao XQ, Chen LJ, Chang JS, Bai FW (2015) Enhanced removal of Zn2+ or Cd2+ by the flocculating Chlorella vulgaris JSC-7. J Hazard Mater 289:38–45

    Article  CAS  PubMed  Google Scholar 

  • Alamsjah MA, Hirao S, Ishibashi F, Oda T, Fujita Y (2008) Algicidal activity of polyunsaturated fatty acids derived from Ulva fasciata and U. pertusa (Ulvaceae, Chlorophyta) on phytoplankton. J Appl Phycol 20:713–720

    Article  CAS  Google Scholar 

  • Anderson DM (2004) Prevention, control and mitigation of harmful algal blooms: multiple approaches to HAB management. Harmful algae management and mitigation Asia-Pacific economic cooperation (Singapore): APEC Publication #204-MR-042, pp 123–130

  • Anderson DM (2009) Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast Manage 52:342–347

  • Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726

    Article  Google Scholar 

  • Audibert L, Fauchon M, Blanc N, Hauchard D, Gall EA (2010) Phenolic compounds in the brown seaweed Ascophyllum nodosum: distribution and radical-scavenging activities. Phytochem Anal 21:399–405

    Article  CAS  PubMed  Google Scholar 

  • Auer MT, Effler SW, Storey ML, Connors SD, Sze P, Siegfried CA, Auer NA, Madsen JD, Smart RM, Eichler LW, Boylen CW, Sutherland JW, Bloomfield JA, Wagner BA, Danehey R, Ringler NA, Gandino C, Hirethota P, Tango P, Arrigo MA, Morgan C, Millard C, Murphy M, Sloan RJ, Niehaus SL, Whitehead KA (1996) Biology. In: Effler SW (ed) Limnological and engineering analysis of polluted urban lake: prelude to environmental management of Onondaga Lake, New York. Springer, NY, pp 384–534

    Chapter  Google Scholar 

  • Ballesteros ML, Wunderlin DA, Bistoni MA (2009) Oxidative stress responses in different organs of Jenynsia multidentata exposed to endosulfan. Ecotox Environ Safe 72:199–205

    Article  CAS  Google Scholar 

  • Borowitzka MA (2016) Chemically-mediated interactions in microalgae. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer International Publishing, Cham, pp 321–357

    Chapter  Google Scholar 

  • Breton F, Cerantola S, Gall EA (2011) Distribution and radical scavenging activity of phenols in Ascophyllum nodosum (Phaeophyceae). J Exp Mar Biol Ecol 399:167–172

    Article  CAS  Google Scholar 

  • Cheng X, Deng G, Su Y, Liu JJ, Yang Y, Du GH CZY, Liu FH (2016) Protein mechanisms in response to NaCl-stress of salt-tolerant and salt-sensitive industrial hemp based on iTRAQ technology. Ind Crop Prod 83:444–452

    Article  CAS  Google Scholar 

  • Chiang IZ, Huang WY, Wu JT (2004) Allelochemicals of Botryococcus braunii (Chlorophyceae). J Phycol 40:474–480

    Article  CAS  Google Scholar 

  • Crawford SA (1979) Farm pond restoration using Chara vulgaris vegetation. Hydrobiologia 62:17–31

    Article  CAS  Google Scholar 

  • Davidson K, Gowen RJ, Tett P, Bresnan E, Harrison PJ, McKinney A, Milligan S, Mills DK, Silke J, Crooks AM (2012) Harmful algal blooms: how strong is the evidence that nutrient ratios and forms influence their occurrence? Estuar Coast Shelf Sci 115:399–413

    Article  CAS  Google Scholar 

  • Della Greca M, Ferrara M, Fiorentino A, Monaco P, Previtera L (1998) Antialgal compounds from Zantedeschia aethiopica. Phytochemistry 49:1299–1304

    Article  CAS  Google Scholar 

  • Dubey RS (1999) Protein synthesis by plants under stressful conditions. In: Handbook of plant and crop stress, second edition. CRC Press, Boca Raton pp 365–397

  • Eustance E, Wray JT, Badvipour S, Sommerfeld MR (2015) The effects of limiting nighttime aeration on productivity and lipid accumulation in Scenedesmus dimorphous. Algal Res 10:33–40

    Article  Google Scholar 

  • Fletcher RL (1975) Heteroantagonism observed in mixed algal cultures. Nature 253:534–535

    Article  CAS  PubMed  Google Scholar 

  • Fong P, Donohoe RM, Zedler JB (1993) Competition with macroalgae and benthic cyanobacterial mats limits phytoplankton abundance in experimental microcosms. Mar Ecol Prog Ser 100:97–102

    Article  Google Scholar 

  • Gall EA, Lelchat F, Hupel M, Jegou C, Stiger-Pouvreau V (2015) Extraction and purification of phlorotannins from brown algae. Methods Mol Biol 1308:131–143

    Article  PubMed  Google Scholar 

  • Gao QT, Wong YS, Tam NFY (2017) Antioxidant responses of different microalgal species to nonylphenol-induced oxidative stress. J Appl Phycol 29:1317–1329

    Article  CAS  Google Scholar 

  • Gross EM (2003) Allelopathy of aquatic autotrophs. Crit Rev Plant Sci 22:313–339

    Article  Google Scholar 

  • He F, Deng P, Wu XH, Cheng SP, Gao YN, Wu ZB (2008) Allelopathic effects on Scenedesmus obliquus by two submerged macrophytes Najas minor and Potamogeton malaianus. Fresen Environ Bull 17:92–97

    CAS  Google Scholar 

  • Hong Y, Hu HY, Li FM (2008a) Physiological and biochemical effects of allelochemical ethyl 2-methyl acetoacetate (EMA) on cyanobacterium Microcystis aeruginosa. Ecotox Environ Safe 71:527–534

    Article  CAS  Google Scholar 

  • Hong Y, Hu HY, Xie X, Li FM (2008b) Responses of enzymatic antioxidants and non-enzymatic antioxidants in the cyanobacterium Microcystis aeruginosa to the allelochemical ethyl 2-methyl acetoacetate (EMA) isolated from reed (Phragmites communis). J Plant Physiol 165:1264–1273

    Article  CAS  PubMed  Google Scholar 

  • Huang LD, Lu DH, Zhang P, Diao JL, Zhou ZQ (2012) Enantioselective toxic effects of hexaconazole enantiomers against Scenedesmus obliquus. Chirality 24:610–614

    Article  CAS  PubMed  Google Scholar 

  • Jeong DH, Jeong MH, Jeong SK, Yang K, Jo WS (2017) Effect of continuous exposure to low-dose-rate gamma irradiation on cell growth and lipid accumulation of marine microalgae. Aquacult Int 25:589–601

    Article  CAS  Google Scholar 

  • Jespersen AM, Christoffersen K (1987) Measurements of chlorophyll-a from phytoplankton using ethanol as extraction solvent. Arch Hydrobiol 109:445–454

    CAS  Google Scholar 

  • Jia Q, Xiang W, Yang F, Hu Q, Tang M, Chen C, Wang G, Dai S, Wu H, Wu H (2016) Low-cost cultivation of Scenedesmus sp. with filtered anaerobically digested piggery wastewater: biofuel production and pollutant remediation. J Appl Phycol 28:727–736

    Article  CAS  Google Scholar 

  • Ken CF, Hsiung TM, Huang ZX, Juang RH, Lin CT (2005) Characterization of Fe/Mn—superoxide dismutase from diatom Thallassiosira weissflogii: Cloning, expression, and property. J Agr Food Chem 53:1470–1474

    Article  CAS  Google Scholar 

  • Koivikko R, Loponen J, Honkanen T, Jormalainen V (2005) Contents of soluble, cell-wall-bound and exuded phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological functions. J Chem Ecol 31:195–212

    Article  CAS  PubMed  Google Scholar 

  • Konig GM, Wright AD, Linden A (1999) Plocamium hamatum and its monoterpenes: chemical and biological investigations of the tropical marine red alga. Phytochemistry 52:1047–1053

    Article  CAS  PubMed  Google Scholar 

  • Lee V, Olsen S (1985) Eutrophication and management initiatives for the control of nutrient inputs to Rhode Island coastal lagoons. Estuaries 8:191–202

    Article  Google Scholar 

  • Lopes G, Sousa C, Silva LR, Pinto E, Andrade PB, Bernardo J, Mouga T, Valentao P (2012) Can phlorotannins purified extracts constitute a novel pharmacological alternative for microbial infections with associated inflammatory conditions? PLoS One 7:e31145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mager WH, Dekruijff AJJ (1995) Stress-induced transcriptional activation. Microbiol Rev 59:506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahdy A, Mendez L, Tomas-Pejo E, del Mar MM, Ballesteros M, Gonzalez-Fernandez C (2016) Influence of enzymatic hydrolysis on the biochemical methane potential of Chlorella vulgaris and Scenedesmus sp. J Chem Technol Biotechnol 91:1299–1305

    Article  CAS  Google Scholar 

  • Marshall SM, Orr AP (1948) Further experiments on the fertilization of a sea loch (Loch Craiglin)—the effect of different plant nutrients on the phytoplankton. J Mar Biol Assoc UK 27:360–379

    Article  CAS  Google Scholar 

  • Mirghaffari N, Moeini E, Farhadian O (2015) Biosorption of Cd and Pb ions from aqueous solutions by biomass of the green microalga, Scenedesmus quadricauda. J Appl Phycol 27:311–320

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Nagayama K, Shibata T, Fujimoto K, Honjo T, Nakamura T (2003) Algicidal effect of phlorotannins from the brown alga Ecklonia kurome on red tide microalgae. Aquaculture 218:601–611

    Article  CAS  Google Scholar 

  • Nguyen TD, Frappart M, Jaouen P, Pruvost J, Bourseau P (2014) Harvesting Chlorella vulgaris by natural increase in pH: effect of medium composition. Environ Technol 35:1378–1388

    Article  CAS  PubMed  Google Scholar 

  • Nicholson P, Howe CJ (1989) Stress-induced protein synthesis in Chlamydomonas reinhardtii. FEMS Microbiol Lett 51:283–287

    Article  CAS  PubMed  Google Scholar 

  • Oh MY, Lee SB, Jin DH, Hong YK, Jin HJ (2010) Isolation of algicidal compounds from the red alga Corallina pilulifera against red tide microalgae. J Appl Phycol 22:453–458

    Article  CAS  Google Scholar 

  • Ohsawa N, Ogata Y, Okada N, Itoh N (2001) Physiological function of bromoperoxidase in the red marine alga, Corallina pilulifera: production of bromoform as an allelochemical and the simultaneous elimination of hydrogen peroxide. Phytochemistry 58:683–692

    Article  CAS  PubMed  Google Scholar 

  • Paerl H (2008) Chapter 10: Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum. Adv Exp Med Biol 619:217–237

    Article  CAS  PubMed  Google Scholar 

  • Parys S, Kehraus S, Krick A, Glombitza KW, Carmeli S, Klimo K, Gerhauser C, Konig GM (2010) In vitro chemopreventive potential of fucophlorethols from the brown alga Fucus vesiculosus L. by anti-oxidant activity and inhibition of selected cytochrome P450 enzymes. Phytochemistry 71:221–229

    Article  CAS  PubMed  Google Scholar 

  • Pereira MM, Mouton L, Yepremian C, Coute A, Lo J, Marconcini JM, Ladeira LO, Raposo NRB, Brandao HM, Brayner R (2014) Ecotoxicological effects of carbon nanotubes and cellulose nanofibers in Chlorella vulgaris. J Nanobiotech 12:15. https://doi.org/10.1186/1477-3155-12-15

    Article  Google Scholar 

  • Qian HF, Chen W, Sheng GD, Xu XY, Liu WP, Fu ZW (2008) Effects of glufosinate on antioxidant enzymes, subcellular structure, and gene expression in the unicellular green alga Chlorella vulgaris. Aquat Toxicol 88:301–307

    Article  CAS  PubMed  Google Scholar 

  • Queguineur B, Goya L, Ramos S, Martin MA, Mateos R, Guiry MD, Bravo L (2013) Effect of phlorotannin-rich extracts of Ascophyllum nodosum and Himanthalia elongata (Phaeophyceae) on cellular oxidative markers in human HepG2 cells. J Appl Phycol 25:1–11

    Article  CAS  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Rosenberg JN, Kobayashi N, Barnes A, Noel EA, Betenbaugh MJ, Oyler GA (2014) Comparative analyses of three Chlorella species in response to light and sugar reveal distinctive lipid accumulation patterns in the microalga C. sorokiniana. PLoS One 9:e92460

    Article  PubMed  PubMed Central  Google Scholar 

  • Rym BD (2012) Photosynthetic behavior of microalgae in response to environmental factors. In: Najafpour MM (ed) Applied photosynthesis. InTech, Riejeka, pp 22–46

    Google Scholar 

  • Salomon PS, Imai I (2006) Pathogens of harmful microalgae. In: Granéli E, Turner JT (eds) Ecology of harmful algae. Springer, Berlin, pp 271–282

    Chapter  Google Scholar 

  • Senturk T, Yildiz S (2016) Adsorbent effect of Chlorella vulgaris and Scenedesmus sp (Chlorophyta) for the removal of some heavy metals and nutrients. Turk J Biochem 41:87–95

    CAS  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Zhong Y, Huang Z, Yang YF (2014) Selenium accumulation in unicellular green alga Chlorella vulgaris and its effects on antioxidant enzymes and content of photosynthetic pigments. PLoS One 9:e112270

    Article  PubMed  PubMed Central  Google Scholar 

  • Tzvetkova-Chevolleau T, Franck F, Alawady AE, Dall'Osto L, Carriere F, Bassi R, Grimm B, Nussaume L, Havaux M (2007) The light stress-induced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. Plant J 50:795–809

    Article  CAS  PubMed  Google Scholar 

  • Vandamme D, Foubert I, Fraeye I, Meesschaert B, Muylaert K (2012) Flocculation of Chlorella vulgaris induced by high pH: role of magnesium and calcium and practical implications. Bioresour Technol 105:114–119

    Article  CAS  PubMed  Google Scholar 

  • Wang L, He F, Sun J, Hu Y, Huang T, Zhang Y, Wu Z (2017) Effects of three biological control approaches and their combination on the restoration of eutrophicated waterbodies. Limnology 18:301–313

    Article  CAS  Google Scholar 

  • Westman JO, Mapelli V, Taherzadeh MJ, Franzen CJ (2014) Flocculation causes inhibitor tolerance in Saccharomyces cerevisiae for second-generation bioethanol production. Appl Environ Microbiol 80:6908–6918

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Sun Q, Zhou J, Masunaga S, Ma F (2015) Reduction in toxicity of wastewater from three wastewater treatment plants to alga (Scenedesmus obliquus) in northeast China. Ecotoxicol Environ Saf 119:132–139

    Article  CAS  PubMed  Google Scholar 

  • Zubia M, Fabre MS, Kerjean V, Le Lann K, Stiger-Pouvreau V, Fauchon M, Deslandes E (2009) Antioxidant and antitumoural activities of some Phaeophyta from Brittany coasts. Food Chem 116:693–701

    Article  CAS  Google Scholar 

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Acknowledgements

The authors appreciate the invaluable discussion of Professor Li Fong Yau Sam from the National University of Singapore and the assistance on extraction work by Yushui Li and Tingting Li.

Funding

This work is financially supported by the Natural Science Foundation of China (No. 21405008), Shenzhen Research Grant (No. JCYJ20140903101648708 and KC2015ZDYF0014A), and by Shenzhen Municipal Government subsidies for postdoctoral research.

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Authors and Affiliations

  1. Shenzhen Engineering Laboratory for Eco-efficient Polysilicate Materials, School of Environment and Energy, Shenzhen Graduate School, Peking University, Shenzhen, 518055, People’s Republic of China

    Ping Shi, Shu Geng, Ting Feng & Huanan Wu

  2. Northwest Agriculture and Forestry University, Yangling, Shaanxi, 712100, People’s Republic of China

    Shu Geng

  3. University of California, Davis, CA, 95616, USA

    Shu Geng

  4. E-112, Peking University, Xili University Town, Shenzhen, 518055, China

    Huanan Wu

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  1. Ping Shi
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Correspondence to Huanan Wu.

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Shi, P., Geng, S., Feng, T. et al. Effects of Ascophyllum nodosum extract on growth and antioxidant defense systems of two freshwater microalgae. J Appl Phycol 30, 851–859 (2018). https://doi.org/10.1007/s10811-017-1287-z

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  • DOI: https://doi.org/10.1007/s10811-017-1287-z

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