Abstract
The modulation of antioxidant responses and onset of oxidative stress is due to several factors, including temperature, diets, and hypoxia followed by re-oxygenation in several aerobic organisms including rotifers. In this context, the aims of this study were (1) to establish a protocol for evaluating in vivo ROS (reactive oxygen species) concentration in rotifer Brachionus plicatilis and (2) to determine the effects on population growth and oxidative stress responses in rotifers fed with different diets: commercial baker’s yeast (Saccharomyces cerevisiae) or concentrated microalgae Nannochloropsis oculata. The rotifers were stocked in five densities (200, 400, 660, 800, and 1000 rotifers mL−1) and exposed to four concentrations of dichlorofluorescein diacetate (H2DCF-DA) (4.4, 8.7, 17.5, and 35 nmol L−1) to optimize a protocol for in vivo ROS determination. The methodology was standardized using 8.7 nmol H2DCF-DA L−1 and it is effective when rotifer density lies within 400 and 1000 rotifers mL−1. In the second experiment, rotifers were fed with 55 × 109 microalgae cells or 0.6 g yeast per million rotifers for 4 days in quadruplicate. Rotifers fed with yeast showed poorer oxidative condition as shown by (a) a higher in vivo ROS concentration; (b) a higher GST (glutathione S-transferase) activity; and (3) a reduced total antioxidant capacity. In conclusion, the methodology to measure in vivo ROS concentration using the H2DCF-DA was efficiently standardized for the first time to rotifers B. plicatilis. Although the yeast-fed rotifers showed higher population growth comparing with this concentration of microalgae, the rotifers fed with N. oculata faced a safer pro-oxidant scenario and presented a higher percentage of egg-carrying females throughout the experiment indicating a better physiological condition.
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References
Amado LL, Garcia ML, Ramos PB, Freitas RF, Zafalon B, Ferreira JLR, Yunes JS, Monserrat JM (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci Total Environ 407:2115–2123. https://doi.org/10.1016/j.scitotenv.2008.11.038
Amado LL, Garcia ML, Pereira TC, Yunes JS, Bogo MR, Monserrat JM (2011) Chemoprotection of lipoic acid against microcystin-induced toxicosis in common carp (Cyprinus carpio, Cyprinidae). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 154:146–153. https://doi.org/10.1016/j.cbpc.2011.04.007
Araujo AB, Snell TW, Hagiwara A (2000) Effect of unionized ammonia, viscosity and protozoan contamination on the enzyme activity of the rotifer Brachionus plicatilis. Aquac Res 31(4):359–365. https://doi.org/10.1046/j.1365-2109.2000.00449.x
Bendschneider K, Robinson RJ (1952) A new spectrophotometric method for the determination of nitrite in seawater. J Mar Res 11:87–96
Blanchette B, Feng X, Singh BR (2007) Marine glutathione S-transferases. Mar Biotechnol 9(5):513–542. https://doi.org/10.1007/s10126-007-9034-0
Conceição LEC, Yúfera M, Makridis P, Morais S, Dinis MT (2009) Live feeds for early stages of fish rearing. Aquac Res 41(5):613–640. https://doi.org/10.1111/j.1365-2109.2009.02242.x
Eaton AD, Clesceri LS, Rice EW, Greenberg AE (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, Washington, D.C.
Esparcia A, Miracle MR, Serra M (1989) Brachionus plicatilis tolerance to low oxygen concentrations. Hydrobiologia 186-187(1):331–337. https://doi.org/10.1007/978-94-009-0465-1_40
Fong S, Gruber J, Halliwell B (2010) Measuring reactive oxygen species in C. elegans using DCFDA – a word of caution. The Worm Breeder’s Gazette 18(11).
Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405. https://doi.org/10.1016/S0076-6879(81)77053-8
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Halliwell B, Gutteridge JM (2015) Free radicals in biology and medicine. Oxford University Press, USA
Hirata H, Yamasaki S (1987) Effect of feeding on the respiration rate of the rotifer Brachionus plicatilis. Hydrobiologia 147(1):283–288. https://doi.org/10.1007/978-94-009-4059-8_38
Hirayama K, Funamoto H (1983) Supplementary effects of several nutrients on nutritive deficiency of Baker’s yeast for population growth of the rotifer Brachionus plicatilis. Bull Jpn Soc Sci Fish 49(4):505–510. https://doi.org/10.2331/suisan.49.505
Hirayama K, Watanabe K (1973) Fundamental studies on physiology of rotifer for its mass culture 4: nutritional effect of yeast on population growth of rotifer. Bull Jpn Soc Sci Fish 39:1129–1133
Jeong CB, Kang HM, Lee MC, Byeon E, Park HG, Lee JS (2019) Effects of polluted seawater on oxidative stress, mortality, and reproductive parameters in the marine rotifer Brachionus koreanus and the marine copepod Tigriopus japonicus. Aquat Toxicol 208:39–46. https://doi.org/10.1016/j.aquatox.2018.12.019
Johnston RK, Siegfried EJ, Snell TW, Carberry J, Carberry M, Brown C, Farooq S (2018) Effects of astaxanthin on Brachionus manjavacas (Rotifera) population growth. Aquac Res 49:2278–2287. https://doi.org/10.1111/are.13688
Kang HM, Jeong CB, Kim MS, Lee JS, Zhou J, Lee YH, Kim DH, Moon E, Kweon HS, Lee SJ, Lee JS (2018) The role of the p38-activated protein kinase signaling pathway-mediated autophagy in cadmium-exposed monogonont rotifer Brachious koreanus. Aquat Toxicol 194:46–56. https://doi.org/10.1016/j.aquatox.2017.11.002
Kim RO, Rhee JS, Won EJ, Lee KW, Kang CM, Lee YM, Lee JS (2011) Ultraviolet B retards growth, induces oxidative stress, and modulates DNA repair-related gene and heat shock protein gene expression in the monogonont rotifer, Brachionus sp. Aquat Toxicol 101(3-4):529–539. https://doi.org/10.1016/j.aquatox.2010.12.005
Latta LC, Tucker KN, Haney RA (2019) The relationship between oxidative stress, reproduction, and survival in a bdelloid rotifer. BMC Ecol 19(1):1–10. https://doi.org/10.1186/s12898-019-0223-2
Lee YH, Kim DH, Kang HM, Wang M, Jeong CB, Lee JS (2017) Adverse effects of methylmercury (MeHg) on life parameters, antioxidant systems, and MAPK signaling pathways in the rotifer Brachionus koreanus and the copepod Paracyclopina nana. Aquat Toxicol 190:181–189. https://doi.org/10.1016/j.aquatox.2017.07.006
Liang Z, Liu R, Zhao D, Wang L, Sun M, Wang M, Song L (2016) Ammonia exposure induces oxidative stress, endoplasmic reticulum stress and apoptosis in hepatopancreas of Pacific white shrimp (Litopenaeus vannamei). Fish & shellfish Immunology 54:523–528. https://doi.org/10.1016/j.fsi.2016.05.009
Livingstone DR (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Rev Med Vet 154:427–430
Lubzens E, Zmora O (2003) Production and nutritional value of rotifers. In: Støttrup JG, McEvoy LA (eds) Live feeds in marine aquaculture. Blackwell Science, Oxford, pp 300–303
Maltez LC, Stringhetta GR, Enamorado AD, Okamoto MH, Romano LA, Monserrat JM, Sampaio LA, Garcia L (2017) Ammonia exposure and subsequent recovery trigger oxidative stress responses in juveniles of Brazilian flounder Paralichthys orbignyanus. Fish Physiol Biochem 43(6):1747–1759. https://doi.org/10.1007/s10695-017-0406-8
Nagata WD (1986) Mariculture in Japan: past, present and future perspectives. Mini Review and Data File of Fisheries Research 4:1–38
Oakes KD, Van der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations. Aquat Toxicol 63:447–463. https://doi.org/10.1016/S0166-445X(02)00204-7
Øie G, Reitan KI, Evjemo JO, Støttrup J, Olsen Y (2011) Live feeds. In: Holt GJ (ed) Larval fish nutrition. Wiley-Blackwell, West Sussex, pp 307–334
Pandey VN, Mishra SK, Srivastava AK, Gupta N (2015) Antioxidant potential of marine microorganisms: a review. In: Dubey NK (ed) Plants as a source of natural antioxidants. CAB International, United Kingdom, pp 129–147
Park JC, Yoon DS, Byeon E, Seo JS, Hwang UK, Han J, Lee JS (2018) Adverse effects of two pharmaceuticals acetaminophen and oxytetracycline on life cycle parameters, oxidative stress, and defensome system in the marine rotifer Brachionus rotundiformis. Aquat Toxicol 204:70–79. https://doi.org/10.1016/j.aquatox.2018.08.018
Snell TW, Childress MJ, Boyer EM, Hoff FH (1987) Assessing the status of rotifer mass cultures. J World Aquacult Soc 18(4):270–277. https://doi.org/10.1111/j.1749-7345.1987.tb01038.x
Snell TW, Fields AM, Johnston RK (2012) Antioxidants can extend lifespan of Brachionus manjavacas (Rotifera), but only in a few combinations. Biogerontology 13(3):261–275. https://doi.org/10.1007/s10522-012-9371-x
UNESCO (1983) Chemical methods for use in marine environmental monitoring. Manual and Guides 12. Intergovernamental Oceanographic Commissiony, Paris, France.
Xie F, Koziar SA, Lampi MA, Dixon DG, Norwood WP, Borgmann U, Huang H, Greenberg BM (2006) Assessment of the toxicity of mixtures of copper, 9, 10-phenanthrenequinone, and phenanthrene to Daphnia magna: evidence for a reactive oxygen mechanism. Environ Toxicol Chem 25(2):613–622. https://doi.org/10.1897/05-256R.1
Yu JP, Hirayama K (1986) The effect of un-ionized ammonia on the population growth of the rotifer in mass culture 1, 2. Bull Jpn Soc Sci Fish 52(9):1509–1513. https://doi.org/10.2331/suisan.52.1509
Zhang J, Wang Y, Sun K, Fang K, Tang X (2016) A study of oxidative stress induced by two polybrominated diphenyl ethers in the rotifer Brachionus plicatilis. Mar Pollut Bull 113:408–413. https://doi.org/10.1016/j.marpolbul.2016.10.032
Zhao C, Xu J, Xu X, Wang Q, Kong Q, Xu F, Du Y (2019) Organ-specific responses to total ammonia nitrogen stress on juvenile grass carp (Ctenopharyngodon idellus). Environ Sci Pollut Res 26:10826–10834. https://doi.org/10.1007/s11356-019-04524-4
Zhu Y, Dunford NT (2013) Growth and biomass characteristics of Picochlorum oklahomensis and Nannochloropsis oculata. J Am Oil Chem Soc 90:841–849. https://doi.org/10.1007/s11746-013-2225-0
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This study was financed in part by the COORDENAÇÃO DE APERFEIÇOAMENTO DE PESSOAL DE NÍVEL SUPERIOR - Brasil (CAPES). T.P.A.P. Oliveira was a graduate student of Aquaculture Post-graduate Program at FURG and supported by CAPES. L.A. Sampaio and J.M. Monserrat are research fellows of Brazilian CNPq.
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Rodrigues, R.V., Maltez, L.C., Ferreira, C.C. et al. ROS in vivo determination and antioxidant responses in rotifers Brachionus plicatilis fed with commercial yeast Saccharomyces cerevisiae or microalgae Nannochloropsis oculata. Aquacult Int 29, 1657–1667 (2021). https://doi.org/10.1007/s10499-021-00707-4
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DOI: https://doi.org/10.1007/s10499-021-00707-4