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Journal of Applied Phycology

, Volume 31, Issue 5, pp 2933–2940 | Cite as

Diets containing residual microalgae biomass protect fishes against oxidative stress and DNA damage

  • Antonio Ernesto Meister Luz Marques
  • Rafael Ernesto Balen
  • Letícia da Silva Pereira Fernandes
  • Cintya Marques Motta
  • Helena Cristina Silva de Assis
  • Dhyogo Miléo Taher
  • Fábio Meurer
  • José Viriato Coelho Vargas
  • André Bellin MarianoEmail author
  • Marta Margarete Cestari
Article

Abstract

Microalgae are major antioxidant producers and feed containing these substances is known to be beneficial. Microalgae cultivation is an alternative way to produce biodiesel and, after oil extraction, residual algal biomass (RAB) is obtained. The RAB was tested as an ingredient in fish feed production and its safety evaluation is important to prevent risks to fish health. This study aim was to evaluate, through biochemical and genetic biomarkers, the safety of RAB in catfish, Rhamdia quelen, feed. Acutodesmus obliquus microalgae RAB, cultivated in Chu medium, was used in feed formulation. A standard feed without RAB (0%) was produced, and three other feeds were enriched with RAB in 1, 2, and 3% proportion. Each feed kind was given to a 15 R. quelen fingerling group for 60 days. The evaluated biochemical biomarkers were superoxide dismutase (SOD) and catalase (CAT) activities, lipid peroxidation (LPO) in the liver, and acetilcolinesterase (AChE) activity in the brain and muscles. The genetic biomarkers analyzed were halo assay in erythrocytes, comet assay in erythrocytes, liver and brain, and piscine micronucleus. The SOD activity was increased in the 3% group; CAT activity and LPO levels were not different among the groups. In the comet assay, a significant decrease in DNA damage in erythrocytes (2 and 3%) and liver tissue (3%) was observed. In the brain, DNA damage was not observed. These results corroborate that as the RAB amount increased, the organisms showed a potential antioxidant effect, as the 3% RAB feed had the best results.

Keywords

Antioxidant feed Carotenoids Chlorophyll Acutodesmus Residual algal biomass Supplementation 

Notes

Acknowledgements

The authors would like to thank MSc. Camila da Costa Senkiv and Lúcia Gil for providing language and writing support, and the assistance of the following laboratories from Federal University of Paraná (UFPR): Animal Cytogenetics and Environmental Mutagenesis Lab., Aquaculture Technology Lab., Environmental Toxicology Lab. and NPDEAS.

Funding information

This work was financially supported by CNPq and CAPES under the grant [grant numbers 40001016006P1].

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abdel-Daim M, El-Bialy BE, Rahman HGA, Radi AM, Hefny HA, Hassan AM (2016) Antagonistic effects of Spirulina platensis against sub-acute deltamethrin toxicity in mice: biochemical and histopathological studies. Biomed Pharmacother 77:79–85PubMedGoogle Scholar
  2. Abdelkhalek NKM, Ghazy EW, Abdel-Daim MM (2015) Pharmacodynamic interaction of Spirulina platensis and deltamethrin in freshwater fish Nile tilapia, Oreochromis niloticus: impact on lipid peroxidation and oxidative stress. Environ Sci Pollut Res 22:3023–3031Google Scholar
  3. Abdelkhalek NKM, Eissa IAM, Ahmed E, Kilany OE, El-Adl M, Dawood MAO, Hassan AM, Abdel-Daim MM (2017) Protective role of dietary Spirulina platensis against diazinon-induced oxidative damage in Nile tilapia; Oreochromis niloticus. Environ Toxicol Pharmacol 54:99–104PubMedGoogle Scholar
  4. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126Google Scholar
  5. Andrade VM, de Freitas TRO, da Silva J (2004) Comet assay using mullet (Mugil sp.) and sea catfish (Netuma sp.) erythrocytes for the detection of genotoxic pollutants in aquatic environment. Mutat Res 560:57–67PubMedGoogle Scholar
  6. Azqueta A, Collins AR (2012) Carotenoids and DNA damage. Mutation Research, Fundamental and Molecular Mechanisms of Mutagenesis 733:4–13PubMedGoogle Scholar
  7. Azqueta A, Shaposhnikov S, Collins AR (2009) DNA oxidation: investigating its key role in environmental mutagenesis with the comet assay. Mutation Research, Genetic Toxicology and Environmental Mutagenesis 674:101–108Google Scholar
  8. Balen RE, Geraldo E, Marques AEML, Cestari MM, Vargas JVC, Corrêa DDO, Bellin MA, Meurer F (2015) Effect of defatted microalgae (Scenedesmus obliquus) biomass inclusion on growth performance of Rhamdia quelen (Quoy & Gaimard, 1824). J Appl Ichthyol 31:98–101Google Scholar
  9. Barreto A, Luis LG, Soares AMVM, Paíga P, Santos LHMLM, Delerue-Matos C, Hylland K, Loureiro S, Oliveira M (2017) Genotoxicity of gemfibrozil in the gilthead seabream (Sparus aurata). Mutation Research, Genetic Toxicology and Environmental Mutagenesis 821:36–42Google Scholar
  10. Becker AG, Parodi TV, Gonçalves JF, Bagatini MD, Spanevello RM, Morsch VM, Chitolina Schetinger MR, Baldisserotto B (2013) Ectonucleotidase and acetylcholinesterase activities in silver catfish (Rhamdia quelen) exposed to different salinities. Biochem Syst Ecol 46:44–49Google Scholar
  11. Bishop NI, Urbig T, Senger H (1995) Complete separation of the β,ε- and β,β-carotenoid biosynthetic pathways by a unique mutation of the lycopene cyclase in the green alga, Scenedesmus obliquus. FEBS Lett 367:158–162PubMedGoogle Scholar
  12. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedPubMedCentralGoogle Scholar
  13. Bretaud S, Toutant J-P, Saglio P (2000) Effects of carbofuran, diuron, and nicosulfuron on acetylcholinesterase activity in goldfish (Carassius auratus). Ecotoxicol Environ Saf 47:117–124PubMedGoogle Scholar
  14. Canton R, Weingartner M, Fracalossi DM, Zaniboni Filho E (2007) Influência da freqüência alimentar no desempenho de juvenis de jundiá. Rev Bras Zootec 36:749–753Google Scholar
  15. Carrasco KR, Tilbury KL, Myers MS (1990) Assessment of the piscine micronucleus test as an in situ biological indicator of chemical contaminant effects. Can J Fish Aquat Sci 47:2123–2136Google Scholar
  16. Cattaneo R, Clasen B, Loro VL, De Menezes CC, Pretto A, Baldisserotto B, Santi A, De Avila LA (2011) Toxicological responses of Cyprinus carpio exposed to a commercial formulation containing glyphosate. Bull Environ Contam Toxicol 87:597–602PubMedGoogle Scholar
  17. Cemeli E, Baumgartner A, Anderson D (2009) Antioxidants and the comet assay. Mutat Res 681:51–67PubMedGoogle Scholar
  18. Cestari MM, Lemos PMM, Ribeiro CADO, Costa JRMA, Pelletier E, Ferraro MVM, Mantovani MS, Fenocchio AS (2004) Genetic damage induced by trophic doses of lead in the neotropical fish Hoplias malabaricus (Characiformes, Erythrinidae) as revealed by the comet assay and chromosomal aberrations. Genet Mol Biol 27:270–274Google Scholar
  19. Chu SP (1942) The influence of the mineral composition of the medium on the growth of planktonic algae: part I. methods and culture media. J Ecol 30:284–325Google Scholar
  20. Collins AR (2001) Carotenoids and genomic stability. Mutation Research, Fundamental and Molecular Mechanisms of Mutagenesis 475:21–28PubMedGoogle Scholar
  21. Collins AR, Ai-guo M, Duthie SJ (1995) The kinetics of repair of oxidative DNA damage (strand breaks and oxidised pyrimidines) in human cells. Mutation Research, DNA Repair 336:69–77Google Scholar
  22. Damergi E, Schwitzguébel JP, Refardt D, Sharma S, Holliger C, Ludwig C (2017) Extraction of carotenoids from Chlorella vulgaris using green solvents and syngas production from residual biomass. Algal Res 25:488–495Google Scholar
  23. Del Campo JA, García-González M, Guerrero MG (2007) Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biotechnol 74:1163–1174PubMedGoogle Scholar
  24. Ellman GL, Courtney KD, Andres V, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95PubMedPubMedCentralGoogle Scholar
  25. Escorsim AM, da Rocha G, Vargas JVC, Mariano AB, Ramos LP, Corazza ML, Cordeiro CS (2018) Extraction of Acutodesmus obliquus lipids using a mixture of ethanol and hexane as solvent. Biomass Bioenergy 108:470–478Google Scholar
  26. Ferraro MVM, Fenocchio AS, Mantovani MS, Ribeiro CADO, Cestari MM (2004) Mutagenic effects of tributyltin and inorganic lead (Pb II) on the fish H. malabaricus as evaluated using the comet assay and the piscine micronucleus and chromosome aberration tests. Genet Mol Biol 27:103–107Google Scholar
  27. Frenzilli G, Nigro M, Lyons BP (2009) The comet assay for the evaluation of genotoxic impact in aquatic environments. Mutat Res 681:80–92PubMedGoogle Scholar
  28. Gao R, Yuan Z, Zhao Z, Gao X (1998) Mechanism of pyrogallol autoxidation and determination of superoxide dismutase enzyme activity. Bioelectrochem Bioenerg 45:41–45Google Scholar
  29. Ghelfi A, Ribas JLC, Guiloski IC, Bettim FL, Piancini LDS, Cestari MM, Pereira AJ, Sassaki GL, Silva de Assis HC (2016) Evaluation of biochemical, genetic and hematological biomarkers in a commercial catfish Rhamdia quelen exposed to diclofenac. Bull Environ Contam Toxicol 96:49–54PubMedGoogle Scholar
  30. Ghisi NDC, Ramsdorf WA, Ferraro MVM, Almeida MIMD, Ribeiro CADO, Cestari MM (2011) Evaluation of genotoxicity in Rhamdia quelen (Pisces, Siluriformes) after sub-chronic contamination with Fipronil. Environ Monit Assess 180:589–599Google Scholar
  31. Gomes L d C, Golombieski JI, Gomes ARC, Baldisserotto B (2000) Biologia do jundiá Rhamdia quelen (Teleostei, Pimelodidae). Ciência Rural 30:179–185Google Scholar
  32. Gontijo ÁM d MC, Barreto RE, Speit G, Valenzuela Reyes VA, Volpato GL, Favero Salvadori DM (2003) Anesthesia of fish with benzocaine does not interfere with comet assay results. Mutation Research, Genetic Toxicology and Environmental Mutagenesis 534:165–172Google Scholar
  33. Guedes AC, Amaro HM, Pereira RD, Malcata FX (2011) Effects of temperature and pH on growth and antioxidant content of the microalga Scenedesmus obliquus. Biotechnol Prog 27:1218–1224PubMedGoogle Scholar
  34. Guiloski IC, Stein Piancini LD, Dagostim AC, de Morais Calado SL, Fávaro LF, Boschen SL, Cestari MM, da Cunha C, Silva de Assis HC (2017) Effects of environmentally relevant concentrations of the anti-inflammatory drug diclofenac in freshwater fish Rhamdia quelen. Ecotoxicol Environ Saf 139:291–300PubMedGoogle Scholar
  35. He Q, Yang H, Wu L, Hu C (2015) Effect of light intensity on physiological changes, carbon allocation and neutral lipid accumulation in oleaginous microalgae. Bioresour Technol 191:219–228PubMedGoogle Scholar
  36. Heddle JA (1973) A rapid in vivo test for chromosomal damage. Mutat Res 18:187–190PubMedGoogle Scholar
  37. Jiang Z-Y, Hunt JV, Wolff SP (1992) Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Anal Biochem 202:384–389PubMedGoogle Scholar
  38. Kaizer RR, Loro VL, Schetinger MRC, Morsch VM, Tabaldi LA, da Rosa CS, Garcia LDO, Becker AG, Baldisserotto B (2009) NTPDase and acetylcholinesterase activities in silver catfish, Rhamdia quelen (Quoy & Gaimard, 1824) (Heptapteridae) exposed to interaction of oxygen and ammonia levels. Neotropical Ichthyology 7:635–640Google Scholar
  39. Kochhann D, Pavanato MA, Llesuy SF, Correa LM, Konzen Riffel AP, Loro VL, Mesko MF, Flores ÉMM, Dressler VL, Baldisserotto B (2009) Bioaccumulation and oxidative stress parameters in silver catfish (Rhamdia quelen) exposed to different thorium concentrations. Chemosphere 77:384–391PubMedGoogle Scholar
  40. Krinsky NI, Johnson EJ (2005) Carotenoid actions and their relation to health and disease. Mol Asp Med 26:459–516Google Scholar
  41. Löf M, Sundelin B, Liewenborg B, Bandh C, Broeg K, Schatz S, Gorokhova E (2016) Biomarker-enhanced assessment of reproductive disorders in Monoporeia affinis exposed to contaminated sediment in the Baltic Sea. Ecol Indic 63:187–195Google Scholar
  42. Miron DS, Crestani M, Rosa Shettinger M, Maria Morsch V, Baldisserotto B, Angel Tierno M, Moraes G, Vieira VLP (2005) Effects of the herbicides clomazone, quinclorac, and metsulfuron methyl on acetylcholinesterase activity in the silver catfish (Rhamdia quelen) (Heptapteridae). Ecotoxicol Environ Saf 61:398–403Google Scholar
  43. Norambuena F, Hermon K, Skrzypczyk V, Emery JA, Sharon Y, Beard A, Turchini GM (2015) Algae in fish feed: performances and fatty acid metabolism in juvenile Atlantic Salmon. PLoS One 10:e0124042PubMedPubMedCentralGoogle Scholar
  44. Pamplona JH, Oba ET, da Silva TA, Ramos LP, Ramsdorf WA, Cestari MM, Ribeiro CAO, Zampronio AR, Silva de Assis HC (2011) Subchronic effects of dipyrone on the fish species Rhamdia quelen. Ecotoxicol Environ Saf 74:342–349PubMedGoogle Scholar
  45. Patias LD, Fernandes AS, Petry FC, Mercadante AZ, Jacob-Lopes E, Zepka LQ (2017) Carotenoid profile of three microalgae/cyanobacteria species with peroxyl radical scavenger capacity. Food Res Int 100:260–266PubMedGoogle Scholar
  46. Piancini LDS, Santos GS, Tincani FH, Cestari M (2015) Piscine micronucleus test and the comet assay reveal genotoxic effects of atrazine herbicide in the neotropical fish Rhamdia quelen. Ecotoxicology and Environmental Contamination 10:55–60Google Scholar
  47. Quoy JRC, Gaimard P (1824) Description des Poissons. In: Freycinet LCD de (ed) Voyage autour du Monde, Entrepris par Ordre du Roi, ... Exécuté sur les corvettes de S. M. l’Uranie et la Physicienne, pendant les années 1817, 1818, 1819 et 1820. Chez Pillet Aîné, Paris, pp 192–401. https://biodiversitylibrary.org/page/40871183
  48. Ramsdorf WA, Guimarães F de SF, Ferraro MVM, Gabardo J, Trindade ES, Cestari MM (2009) Establishment of experimental conditions for preserving samples of fish blood for analysis with both comet assay and flow cytometry. Mutation Research, Genetic Toxicology and Environmental Mutagenesis 673:78–81Google Scholar
  49. Rao A, Rao L (2007) Carotenoids and human health. Pharmacol Res 55:207–216PubMedGoogle Scholar
  50. Reis LCR, de Oliveira VR, Hagen MEK, Jablonski A, Flôres SH, de Oliveira Rios A (2015) Carotenoids, flavonoids, chlorophylls, phenolic compounds and antioxidant activity in fresh and cooked broccoli (Brassica oleracea var. avenger) and cauliflower (Brassica oleracea var. Alphina F1). Food Science and Technology 63:177–183Google Scholar
  51. Roca M, Chen K, Pérez-Gálvez A (2016) Chlorophylls. In: Carle R, Schweiggert R (eds) Handbook on natural pigments in food and beverages. Elsevier, NY pp 125–158. Google Scholar
  52. Romani R, Antognelli C, Baldracchini F, De Santis A, Isani G, Giovannini E, Rosi G (2003) Increased acetylcholinesterase activities in specimens of Sparus auratus exposed to sublethal copper concentrations. Chem Biol Interact 145:321–329PubMedGoogle Scholar
  53. Sayed AEDH, El-Sayed YS, El-Far AH (2017) Hepatoprotective efficacy of Spirulina platensis against lead-induced oxidative stress and genotoxicity in catfish; Clarias gariepinus. Ecotoxicol Environ Saf 143:344–350PubMedGoogle Scholar
  54. Schetinger MR, Bonan CD, Morsch VM, Bohrer D, Valentim LM, Rodrigues SR (1999) Effects of aluminum sulfate on delta-aminolevulinate dehydratase from kidney, brain, and liver of adult mice. Braz J Med Biol Res 32:761–766PubMedGoogle Scholar
  55. Schmid W (1975) The micronucleus test. Mutat Res 31:9–15PubMedGoogle Scholar
  56. Singh NP (2000) A simple method for accurate estimation of apoptotic cells. Exp Cell Res 256:328–337PubMedGoogle Scholar
  57. Speit G, Hartmann A (1999) The comet assay (single-cell gel test): a sensitive genotoxicity test for the detection of DNA damage and repair. Methods Mol Biol 113:203–212PubMedGoogle Scholar
  58. Stankevičiūtė M, Butrimavičienė L, Valskienė R, Greiciūnaitė J, Baršienė J, Vosylienė MZ, Svecevičius G (2016) Analysis of nuclear abnormalities in erythrocytes of rainbow trout (Oncorhynchus mykiss) treated with cu and Zn and after 4-, 8-, and 12-day depuration (post-treatment recovery). Mutation Research, Genetic Toxicology and Environmental Mutagenesis 797:26–35PubMedGoogle Scholar
  59. Sturm A, da Silva de Assis H, Hansen P-D (1999) Cholinesterases of marine teleost fish: enzymological characterization and potential use in the monitoring of neurotoxic contamination. Mar Environ Res 47:389–398Google Scholar
  60. van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149Google Scholar
  61. Ventura L, Giovannini A, Savio M, Donà M, Macovei A, Buttafava A, Carbonera D, Balestrazzi A (2013) Single cell gel electrophoresis (comet) assay with plants: research on DNA repair and ecogenotoxicity testing. Chemosphere 92:1–9PubMedGoogle Scholar
  62. Villela IV, de Oliveira IM, Silveira JC, Dias JF, Henriques JAP, da Silva J (2007) Assessment of environmental stress by the micronucleus and comet assays on Limnoperna fortunei exposed to Guaíba hydrographic region samples (Brazil) under laboratory conditions. Mutation Research, Genetic Toxicology and Environmental Mutagenesis 628:76–86Google Scholar
  63. Zeppenfeld CC, Toni C, Becker AG, Miron DDS, Parodi TV, Heinzmann BM, Barcellos LJG, Koakoski G, Rosa JGSD, Loro VL, Cunha MAD, Baldisserotto B (2014) Physiological and biochemical responses of silver catfish, Rhamdia quelen, after transport in water with essential oil of Aloysia triphylla (L’Herit) Britton. Aquaculture 418–419:101–107Google Scholar
  64. Zmora O, Grosse DJ, Zou N, Samocha TM (2013) Microalga for aquaculture: Practical implications. In: Richmond A, Hu Q (eds) Handbook of microalgal Culture.2nd Edn. John Wiley & Sons, Oxford, pp 628–652Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Antonio Ernesto Meister Luz Marques
    • 1
    • 2
  • Rafael Ernesto Balen
    • 3
  • Letícia da Silva Pereira Fernandes
    • 4
  • Cintya Marques Motta
    • 2
  • Helena Cristina Silva de Assis
    • 4
  • Dhyogo Miléo Taher
    • 1
  • Fábio Meurer
    • 3
  • José Viriato Coelho Vargas
    • 1
    • 5
  • André Bellin Mariano
    • 1
    • 6
    Email author
  • Marta Margarete Cestari
    • 1
    • 2
  1. 1.Centre for Research and Development of Sustainable Energy (NPDEAS)Federal University of Paraná (UFPRCuritibaBrazil
  2. 2.Department of Genetics/UFPR, Animal Cytogenetics and Environmental Mutagenesis LaboratoryCuritibaBrazil
  3. 3.Department of Zoology/UFPR, Aquaculture Technology LaboratoryCuritibaBrazil
  4. 4.Department of Pharmacology/UFPR, Environmental Toxicology LaboratoryCuritibaBrazil
  5. 5.Department of Mechanical Engineering/UFPRCuritibaBrazil
  6. 6.Departamento de Engenharia Elétrica, Centro Politécnico, Setor de Tecnologia, Avenida Coronel Francisco H. dos Santos S/N, CP 19011, CEP 81531-980CuritibaBrazil

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