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Investigation on the effects of nitrate and salinity stress on the antioxidant properties of green algae with special reference to the use of processed biomass as potent fish feed ingredient

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Abstract

Antioxidant properties of four common green algal genera viz. Cladophora glomerata, Chaetomorpha aerea, Rhizoclonium crassipellitum, and Pithophora cleveana collected from Sunderban areas of Eastern India were tested in controlled and nutrient stress conditions. Experimental algae were exposed to growth media with variations in nitrate and NaCl salt concentrations from 0 to 1500 ppm level for a period of 21 days. A dose-dependent upregulation in total phenols, flavonoids, pigment, and antioxidant property in relation to % DPPH activity and % ferrous ion chelating activity was observed. Maximum phenol content was observed for algal biomass exposed to 1500 ppm nitrate stress conditions (52.55 ± 0.01 mg GAE/g DW-16.48 ± 0.041 mg GAE/g DW) with Rhizoclonium showing the maximum contents. In the case of total flavonoid content, maximum upregulation was noted in the hypersaline conditions and Pithophora showed the highest contents amongst all (71.8 ± 0.21 mg QE/g DW). The highest carotenoid contents were observed in 750 ppm stress condition. Optimally stressed algal biomass having maximum carotenoid levels and high antioxidant levels were selected as fish feed ingredients, based on dose- and time-dependent two-way Anova and Tukeys test (750 ppm nitrate, 7 days). The processed biomass was included as fish feed ingredient to study the nutritive effects on goldfish (Carassius auratus). Algal feed (AF) was prepared from algal biomass only, which was further mixed with the commercial feed (CF) in varying proportions to formulate three different types of value-added feed (VAF). The experimental feed (25% VAF, 50% VAF, 75%VAF and AF) were tested against commercial feed (control) for 30 days in artificially aerated static aquaria system. The feed type formulated as 50% VAF was found to be most effective in terms of skin pigmentation, growth, and antioxidant activities of experimental fishes showing almost (1.44–4-folds increase) compared to the control setup. Statistically significant results were obtained regarding nutritive properties of experimental feed and fishes using PCA and Tukeys test respectively. Body weight gain and specific growth rate also changed significantly in experimental fishes.

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Abbreviations

TPC:

Total phenol content

TFC:

Total flavonoid content

TCC:

Total carotenoid content

TAC:

Total antioxidant capacity

LPX:

Lipid peroxidation

MDA:

Malondialdehyde

SOD:

Superoxide dismutase activity

CAT:

Catalase activity

GAE:

Gallic acid

QE:

Quercetin

CF:

Commercial feed

AF:

Total algal feed

VAF:

Value-added feed

HPTLC:

High-performance liquid chromatography, nitrate salt

NaCl:

Sodium chloride salt

References

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    PubMed  PubMed Central  CAS  Google Scholar 

  • Athukorala Y, Lee KW, Song C, Ahn CB, Shin TS, Cha YJ, Shahidi F, Jeon YJ (2003) Potential antioxidant activity of marine red alga Grateloupia filicina extracts. J Food Lipids 10:251–265

    CAS  Google Scholar 

  • Barufi JB, Korbee N, Mariana C, Felix O, Figueroa L (2011) Effects of N supply on the accumulation of photosynthetic pigments and photoprotectors in Gracilariatenuistipitata (Rhodophyta) cultured under UV radiation. J Appl Phycol 23:457–466

    CAS  Google Scholar 

  • Beauchamp CO, Fridovich I (1971) Superoxide dismutase improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    PubMed  CAS  Google Scholar 

  • Becker K, Schreiber S, Angoni C, Blum R (1999) Growth performance and feed utilization response of Oreochromis niloticus x Oreochromis aureus hybrids to L carnitine measured over a full fattening cycle under commercial conditions. Aquaculture 174:313–322

    CAS  Google Scholar 

  • Boonyaratpalin M, Supamattaya K, Britton G, Schlipalius LE (2001) Effects of b-carotene source, Dunaliella salina, and astaxanthin on pigmentation, growth, survival and health of Penaeus mondon. Aquac Research 32:182S–190S

    Google Scholar 

  • Borowitzka MA, Borowitzka LJ (1988) Micro-algal biotechnology. Cambridge University Press, Cambridge, pp 96–100

    Google Scholar 

  • Borowitzka MA, Huisman JM, Osborn A (1991) Culture of theastaxanthin-producing green alga Haematococcus pluvialis. Effects of nutrients on growth and cell type. J Appl Phycol 3:295–304

    CAS  Google Scholar 

  • Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB J 9:1551–1558

    PubMed  CAS  Google Scholar 

  • Chandini SK, Ganesan P, Bhaska N (2008) In-vitro antioxidant activities of three selected brown seaweeds of India. Food Chem 107:707–713

    CAS  Google Scholar 

  • Choo K, Snoeijs P, Pedersén M (2004) Oxidative stress tolerance in the filamentous green algae Cladophora glomerata and Enteromorpha ahlneriana. J Exp Mar Biol Ecol 298:111–123

    CAS  Google Scholar 

  • Choochote W, Suklampoo L, Ochaikul D (2014) Evaluation of antioxidant capacities of green microalgae. J Appl Phycol 26:43–48

    CAS  Google Scholar 

  • Coesel SN, Cordeiro A, Licia B, Teles M, Ramos AA, Henriques NM, Cancela L, Carlos J, Varela S (2008) Nutrient limitation is the main regulatory factor for carotenoid accumulation and for Psy and Pds steady state transcript levels in Dunaliella salina (Chlorophyta) exposed to high light and salt stress. Mar Biotechnol 10:602–611

    PubMed  CAS  Google Scholar 

  • Colla LM, Furlong EB, Costa JAV (2007) Antioxidant properties of Spirulina (Arthospira) platensis cultivated under different temperatures and nitrogen regimes. 50:161–167

  • Collen J, Davidson I (1999) Stress tolerance and reactive oxygen metabolism in the intertidal red seaweed Mastocarpusstellatus and Chondruscrispus. Plant Cell 22:1143–1151

    CAS  Google Scholar 

  • Decker EA, Welch B (1990) Role of ferritin as a lipid oxidation catalyst in muscle food. J Agric Chem 38:674–677

    CAS  Google Scholar 

  • Del Campo JA, Moreno J, Rodríguez H, Vargas MA, Rivas J, Guerrero MG (2000) Carotenoid content of chlorophycean microalgae: factors determining lutein accumulation in Muriellopsis sp. (Chlorophyta). J Biotechnol 76(1):51–59

    PubMed  Google Scholar 

  • Dixon RA, Paiva N (1995) Stressed induced phenyl propanoid metabolism. Plant Cell 22:1143–1151. https://doi.org/10.1105/tpc.7.7.1085

    Article  Google Scholar 

  • Goiris K, Colen WV, Wilches I, Leon-Tamariz F, Cooman LD, Muylaert K (2015) Impact of nutrient stress on antioxidant production in three species of microalgae. Algal Research 7:51–57

    Google Scholar 

  • Gouveia L, Gomes E, Empis J (1998) Use of Chlorella vulgaris in diets for rainbow trout to enhance pigmentation of muscle. J Appl Aquac 77:61–70

    Google Scholar 

  • Gouveia L, Rema P, Pereira O, Empis J (2003) Colouring ornamental fish (Cyprinus carpio and Carassiusauratus) with microalgal biomass. Aquac. Nutr 9(2):123–129

    CAS  Google Scholar 

  • Guroy BK, Cirik S, Guroy D, Sanver F, Tekinay AA (2007) Effects of Ulva rigida and Cystoseira barbata meals as a feed additive on growth performance, feed utilization and body composition of Nile Tilapia, Oreochromis niloticus. Turk J Vet Anim Sci 31(2):91–97

    Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    PubMed  CAS  Google Scholar 

  • Hodge JE, Hofreiter BT (1962) Determination of reducing sugars and carbohydrates. In: Whistler RL, Wolfrom ML (eds) Methods in carbohydrate chemistry. Acad Press Inc., New York, pp 380–394

    Google Scholar 

  • Iwai K (2008) Antidiabetic and anti oxidant effects of polyphenols in brown alga Ecklonia stolonifera in genetically diabetic KK-A(Y) mice. Plant Foods Hum Nutr 63(4):163–169

    PubMed  CAS  Google Scholar 

  • Kakinuma M, Coury DA, Kuno Y, Itoh S, Kozawa Y, Inagaki E, Yoshiura Y, Amano H (2006) Physiological and biochemical responses to thermal and salinity stresses in a sterile mutant of Ulvapertusa (Ulvales, Chlorophyta). Mar Biol 149:97–106

    CAS  Google Scholar 

  • Khatoon N, Sengupta P, Homechaudhuri S, Pal R (2010) Evaluation of algae based feed in goldfish (Carassius auratus) nutrition. Proc Zool Soc 63(2):109–114

    Google Scholar 

  • Kobayashi M, Kakizono T, Yamaguchi K, Nishio N, Nagai S (1992) Growth and astaxanthin formation of Haematococcus pluvialis in heterotrophic and mixotrophic conditions. J Ferment Bioeng 74:17–20

    CAS  Google Scholar 

  • Koivikko R (2008) Brown algal phlorotannins improving and applying chemical methods. Turun YliopistoTurku

  • Kop A, Durmaz Y (2008) The effect of synthetic and natural pigments on the colour of the cichlids (Cichlasoma severum sp.,heckel 1840). Aquac Int 16:117–122

    Google Scholar 

  • Kumar KS, Ganessan K, Rao PVS (2007) Antioxidant potential of solvent extract of Kappaphycus alverezii (Doty). Doty—edible seaweed. Food Chem 107:289–295

    Google Scholar 

  • Kumar M, Kumari P, Gupta V, Reddy C, Jha B (2010) Biochemical responses of red alga Gracilariacorticata (Gracilariales, Rhodophyta) to salinity induced oxidative stress. J Exp Mar Biol Ecol 391:27–34

    CAS  Google Scholar 

  • Lee TM, Chang YC, Lin YH (1999) Seasonal acclimation in Gracilaria tenuistipitata. Differences in physiological responses between winter and summer Gracilariatenuistipitata (Gigartinales, Rhodophyta). Bot Bull Acad Sin 49:93–100

    Google Scholar 

  • Lemoine Y, Schoef B (2010) Secondary keto carotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177

    PubMed  CAS  Google Scholar 

  • Liu F, Phang SJ (2010) Stress tolerance and antioxidant enzymatic activities in the

  • Lowry OH, Rosebrough NJ, Far AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Markham KR, Porter LJ (1969) Flavonoids in the green algae (chlorophyta). In: Cody V, Middleton E, Harborne JB (eds) Plant flavonoids in biology and medicine. Alan R. Liss, New York, pp 15–24

    Google Scholar 

  • Mayer AMS, Lehmann VKB (2000) Marine pharmacology in 1998: marine compounds with antibacterial, anticoagulant, anti-inflammatory, anthelmintic, antiplatelet, antiprotozoan, and antiviral activities; with actions on the cardiovascular, endocrine, immune, and nervous systems; and other miscellaneous mechanisms of action. The Pharmac 42:62–69

    Google Scholar 

  • Meenakshi S, Manicka Gnanambigai D, Tamil mozhi S, Arumugam M, Balasubramanian T (2009) Total flavanoid and in vitro antioxidant activity of two seaweeds of Rameshwaram coast. Global J Pharm 3(2):59–62

    Google Scholar 

  • Miranda MS, Cintra RG, Barros SBM, Mancini-Filho J (1998) Antioxidant activity of themicroalga Spirulina maxima. Braz J Med Biol Res 31:1075–1079

    PubMed  CAS  Google Scholar 

  • Mukherjee P, Nandi C, Khatoon N, Pal R (2015) Mixed algal diet for skin colour enhancement of ornamental fishes. J Algal Biomass Util 6(4):35–46

    Google Scholar 

  • Nagayama Y, Takahashi M, Fukuyama Y, Kinzyo Z (1989) An antiplasmin inhibitor, eckol, isolated from the brown alga (Ecklonia kurome) OKAMURA. Agric Biol Chem 63:3025–3030

    Google Scholar 

  • Nalewajko C, Thomas PM (2001) Effects of temperature, and availability of nitrogen and phosphorus on the abundance of Anabaena and Microcystis in Lake Biwa, Japan: an experimental approach. Limno 2:45–48

    Google Scholar 

  • Nasraoui AH, Djellouli A, Nasri-Ayachi MB (2013) Study of oxidative stress responses in two Mediterranean green algae (Tunisian Sea). Int J Curr Res 5(02):271–275

    CAS  Google Scholar 

  • O'Connor WA, Heasman MP (1997) Diet and feeding regimens for larval doughboy scallops, Mimachlamys asperrima. Aquac 158:289–303

    Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349. https://doi.org/10.1016/j.ecoenv.2004.06.010

    Article  CAS  Google Scholar 

  • Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269:337–341

    PubMed  CAS  Google Scholar 

  • Radhakrishnan S, Saravana Bhavan P, Seenivasan C, Muralisankar T (2015) Effect of dietary replacement of fishmeal with Chlorella vulgaris on growth performance, energy utilization and digestive enzymes in Macrobrachium rosenbergii postlarvae. Int J Fish Aquac 7(5):62–70

    CAS  Google Scholar 

  • Sachindra NM, Mahendrakar NS (2005) Process optimization for extraction of carotenoids from shrimp waste with vegetable oils. Bioresour Technol 96:1195–1200

    PubMed  CAS  Google Scholar 

  • Sadashivam S, Manickam A (1996) Biochemical methods, 2nd edn. New Age International Pvt. Ltd. 2005

  • Sadati N, Khanavi M, Mahrokh A, Nabavi SMB, Sohrabipour J, Hadjiakhoondi A (2011) Comparison of antioxidant activity and total phenolic antioxidant activities of marine algae 203 contents of some Persian Gulf marine algae. J Med Plants 10(37):73–79

    CAS  Google Scholar 

  • Sathyaa R, Kanagaa N, Sankarb P, Jeeva S (2017) Antioxidant properties of phlorotannins from brown seaweed Cystoseira trinodis(Forsska) C. Agardh. Arab J Chem 10:S2608–S2614

    Google Scholar 

  • Satpati GG, Gorain PC, Paul I, Pal R (2016) An integrated salinity-driven workflow for rapid lipid enhancement in green microalgae for biodiesel application. RSC Adv 6:112340–112355

    CAS  Google Scholar 

  • Seigler DS (1998) Plant secondary metabolism. Chapman and Hall (Kluwer Academic Publishers), Boston 711

    Google Scholar 

  • Shaish A, Avron M, Pick U, Ben-Amotz A (1993) Are active oxygen species involved in induction of b-carotene in Dunaliella bardawil? Planta 190:363–368

    CAS  Google Scholar 

  • Singleton VL, Rossi JA Jr (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungtic acid reagent. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

  • Yamamoto I, Maruyama H, Takahashi M, Komiyama K (1986) The effect of dietary or intraperitoneally injected seaweed preparations on the growth of sarcoma-180 cells subcutaneously implanted into mice. Cancer Lett 30:125–131

    PubMed  CAS  Google Scholar 

  • Yen GC, Chen HY (1995) Antioxidant activity of various tea extracts in relation to their antimutagenecity. Journ Agric Food Chem 43:27–37

    CAS  Google Scholar 

  • Yoshie Y, Wang W, Hsieh YP, Suzuki T (2002) Compositional difference of phenolic compounds between two seaweeds, Halimeda spp. J Tok Univ Fish 88:21–24

    Google Scholar 

  • Zeng LM, Wang CJ, Su JY (2001) Flavonoids from the red alga Acanthophora spicifera. Chin J Chem 19(11):1 097–1100

    Google Scholar 

  • Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the West Bengal State Council of Science and Technology for funding to PM, DST – FIST and CAS phase VII, Department of Botany for providing instrumental facility. University Grants Commission, New Delhi, India, for granting financial support [award no. F. /2014 -15/RGNF – 2014 -15 D – OBC –WES – 61330].

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Correspondence to Ruma Pal.

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Mukherjee, P., Gorain, P.C., Paul, I. et al. Investigation on the effects of nitrate and salinity stress on the antioxidant properties of green algae with special reference to the use of processed biomass as potent fish feed ingredient. Aquacult Int 28, 211–234 (2020). https://doi.org/10.1007/s10499-019-00455-6

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