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Changes in the life-cycle parameters and glutathione-related antioxidant defense system of rotifer Brachionus calyciflorus under the combined stress of microcystin-LR and ammonia

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Abstract

Serious cyanobacterial blooms lead to the release of harmful microcystin-LR and ammonia to eutrophic waters, thereby posing serious challenges to zooplankton. The physiological and ecological responses of Brachionus calyciflorus Pallas to microcystin-LR and ammonia stresses were evaluated. Neonates (< 2 h old) were exposed to microcystin-LR (0, 10, 50, 100, and 200 µg L−1) and ammonia (0, 740, and 1580 µg L−1) single solutions and mixtures. High doses of 200 µg L−1 microcystin-LR and 1580 µg L−1 ammonia and mixtures of these two toxicants exhibited negative effects on the rotifer net reproduction rate (R0), intrinsic growth rate (rm), and enzymatic activities of glutathione (GSH), glutathione peroxidase (GPx), and glutathione S-transferase (GST). Microcystin-LR combined with ammonia decreased the generation time (T), Na+/K+–adenosine triphosphatase (Na+/K+–ATPase) activity, and glutathione reductase (GR) activity, but promoted the reactive oxygen species (ROS) production in rotifers (p < 0.05). The ROS levels were negatively correlated with GSH-related enzymatic activities (p < 0.01). Microcystin-LR and ammonia exerted synergistic effects on R0, rm, and ROS levels and GSH, GR, and GST activities (p < 0.05), but had antagonistic effects on T, Na+/K+–ATPase activity, and GPx activity (p > 0.05). Microcystis metabolites negatively affected growth and reproductive performance of B. calyciflorus. In addition, the life-cycle parameters were related to the effects of microcystin-LR and ammonia on the GSH-related antioxidant defense system of rotifers.

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References

  • ASTM (2001) Standard guide for acute toxicity tests with the rotifer Brachionus. Annual book of ASTM standards, water and environmental technology, vol. 1105. Biological effects and environmental fates. American Society for Testing and Materials, West Conshohocken

  • Bláha L, Babica P, Maršálek B (2009) Toxins produced in cyanobacterial water blooms–toxicity and risks. Interdiscip Toxicol 2:36–41

    PubMed  PubMed Central  Google Scholar 

  • 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 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cao H, Lyu K, Xiang F, Yang Z (2014) Life history responses of Daphnia similoides simultaneously exposed to microcystin-LR and ammonia and their postexposure recovery. Environ Toxicol Chem 33:2497–2505

    CAS  PubMed  Google Scholar 

  • Chen Y, Gu R, Wang X, Nie Z, Xu G, Lu J, Huang H (2015) Acute toxicity of ammonia nitrogen to Brachionus calyciflorus and its antioxidant physiological response. J Anhui Agric Sci 43:81–84

    Google Scholar 

  • Couto N, Wood J, Barber J (2016) The role of glutathione reductase and related enzymes on cellular redox homoeostasis network. Free Radic Bio Med 95:27–42

    CAS  Google Scholar 

  • Dao TS, Do-Hong LC, Wiegand C (2010) Chronic effects of cyanobacterial toxins on Daphnia magna and their offspring. Toxicon 55:1244–1254

    CAS  PubMed  Google Scholar 

  • Emerson K, Russo RC, Lund RE, Thurston RV (1975) Aqueous ammonia equilibrium calculations: effect of pH and temperature. J Fish Res Board Can 32:2379–2383

    CAS  Google Scholar 

  • EPA US (1999) Update of ambient water quality criteria for ammonia. EPA-822/R-99-014 Office of Water, Washington, DC, pp 1–153

  • Ge J, Li J, Zhang J, Yang Z (2012) Time-dependent oxidative stress responses of submerged macrophyte Vallisneria natans seedlings exposed to ammonia in combination with microcystin under laboratory conditions. Bull Environ Contam Toxicol 89:67–72

    CAS  PubMed  Google Scholar 

  • Guo N, Xie P (2011) A study on the effects of food quantity and quality on glutathione S-transferase (GST) activity and growth rate parameters of Daphnia carinata varying in age. Aquat Ecol 45:63–73

    CAS  Google Scholar 

  • Huang L, Xi Y, Xu X, Wen X (2012) Responses in population growth and reproduction of the freshwater rotifer Brachionus calyciflorus to microcystin-LR at different temperatures. Ann Limnol Int J Lim 48:383–390

    Google Scholar 

  • Kim IS, Nguyen GH, Kim SJ, Jang A (2015) Qualitative analysis of the most toxic and abundant microcystin variants (LR, RR, and YR) by using LCMS–IT–TOF. J Ind Eng Chem 29:375–381

    CAS  Google Scholar 

  • Kim H, Lim B, Kim BD, Lee YM (2016) Effects of heavy metals on transcription and enzyme activity of Na+/K+–ATPase in the monogonont rotifer, Brachionus koreanus. Toxicol Environ Health Sci 8:128–134

    Google Scholar 

  • Kopecka-Pilarczyk J (2010) Effect of exposure to polycyclic aromatic hydrocarbons on Na+–K+–ATPase in juvenile gilthead seabream sparus aurata. J Fish Biol 76:716–722

    CAS  PubMed  Google Scholar 

  • Krebs CJ (1994) Ecology: the experimental analysis of distribution and abundance, 4th edn. Harper Collins College Publishers, New York

    Google Scholar 

  • Lave LB (2001) Hormesis: implications for public policy regarding toxicants. Annu Rev Public Health 22:63–67

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Leung J, Kumar M, Glatz P, Kind K (2011) Impacts of un-ionized ammonia in digested piggery effluent on reproductive performance and longevity of Daphnia carinata and Moina australiensis. Aquaculture 310:401–406

    CAS  Google Scholar 

  • Li JJ, Wang J, Yang L, Chen Y, Yang Z (2014) Changes in plasma osmolality and Na+/K+ATPase activity of juvenile obscure puffer Takifugu obscurus following salinity challenge. Biochem Syst Ecol 56:111–117

    Google Scholar 

  • Liang Y, Chen X, Lu X, Jin S, Min Y, Yang J (2017) Combined effects of microcystin and nitrite on the growth, lipid peroxidation, and antioxidant responses of the freshwater rotifer Brachionus calyciflorus. Aquat Toxicol 192:78–88

    CAS  PubMed  Google Scholar 

  • Liang Y, Lu X, Min Y, Liu L, Yang J (2018) Interactive effects of microcystin and ammonia on the reproductive performance and phenotypic traits of the rotifer Brachionus calyciflorus. Ecotox Environ Safe 147:413–422

    Google Scholar 

  • López-López E, Sedeño-Díaz JE, Soto C, Favari L (2011) Responses of antioxidant enzymes, lipid peroxidation, and Na+/K+–ATPase in liver of the fish Goodea atripinnis exposed to Lake Yuriria water. Fish Physiol Biochem 37:511–522

    PubMed  Google Scholar 

  • Lyu K, Zhu X, Wang Q, Chen Y, Yang Z (2013) Copper/zinc-superoxide dismutase from the Cladoceran Daphnia magna: Molecular cloning and expression in response to different acute environmental stressors. Environ Sci Technol 47:8887–8893

    CAS  PubMed  Google Scholar 

  • Lyu K, Meng Q, Zhu X, Dai D, Zhang L, Huang Y, Yang Z (2016) Changes in iTRAQ-based proteomic profiling of the cladoceran Daphnia magna exposed to microcystin-producing (MP) and microcystin-free (MF) Microcystis aeruginosa. Environ Sci Technol 50:4798–4807

    PubMed  Google Scholar 

  • Mowe MAD, Mitrovic SM, Lim RP, Furey A, Yeo DCJ (2015) Tropical cyanobacterial blooms: a review of prevalence, problem taxa, toxins and influencing environmental factors. J Limnol 74:205–224

    Google Scholar 

  • Pannala VR, Bazil JN, Camara AKS, Dash RK (2013) A biophysically based mathematical model for the catalytic mechanism of glutathione reductase. Free Radic Biol Med 65:1385–1397

    CAS  PubMed  Google Scholar 

  • Pantelić D, Svirčev Z, Simeunović J, Vidović M, Trajković I (2013) Cyanotoxins: characteristics, production and degradation routes in drinking water treatment with reference to the situation in Serbia. Chemosphere 91:421–441

    PubMed  Google Scholar 

  • Park JC, Han J, Lee MC, Seo JS, Lee JS (2017) Effects of triclosan (TCS) on fecundity, the antioxidant system, and oxidative stress-mediated gene expression in the copepod Tigriopus japonicas. Aquat Toxicol 189:16–24

    CAS  PubMed  Google Scholar 

  • Rocha S, Gomes D, Lima M, Bronze-Da-Rocha E, Santos-Silva A (2015) Peroxiredoxin 2, glutathione peroxidase, and catalase in the cytosol and membrane of erythrocytes under H2O2-induced oxidative stress. Free Radic Res 49:990–1003

    CAS  PubMed  Google Scholar 

  • Snell TW, Janssen CR (1995) Rotifers in ecotoxicology: a review. Hydrobiologia 313(314):231–247

    Google Scholar 

  • Snell TW, Joaquim-Justo C (2007) Workshop on rotifers in ecotoxicology. Hydrobiologia 593:227–232

    Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun H, Yang W, Chen YF, Yang Z (2011) Effect of purified microcystin on oxidative stress of silver carp Hypophthalmichthys molitrix larvae under different ammonia concentrations. Biochem Syst Ecol 39:536–543

    CAS  Google Scholar 

  • Sun H, Lü K, Minter EJA, Chen Y, Yang Z, Montagnes DJS (2012) Combined effects of ammonia and microcystin on survival, growth, antioxidant responses, and lipid peroxidation of bighead carp Hypophthalmythys nobilis larvae. J Hazard Mater 221(222):213–219

    PubMed  Google Scholar 

  • Sun H, Wang W, Geng L, Chen Y, Yang Z (2013) In situ studies on growth, oxidative stress responses, and gene expression of juvenile bighead carp (Hypophthalmichthys nobilis) to eutrophic lake water dominated by cyanobacterial blooms. Chemosphere 93:421–427

    CAS  PubMed  Google Scholar 

  • Sun Y, Xu W, Gu Q, Chen Y, Zhou Q, Zhang L, Gu L, Huang Y, Lyu K, Yang Z (2019) Small-sized microplastics negatively affect rotifers: changes in the key life-history traits and rotifer-Phaeocystis population dynamics. Environ Sci Technol 53:9241–9251

    CAS  PubMed  Google Scholar 

  • Thirumavalavan M, Hu YL, Lee JF (2013) Evaluation of analytical approaches linked to high performance liquid chromatography for analysis of microcystin-LR in natural water systems: effects of column and mobile phase gradient. Toxicol Environ Chem 95:221–231

    CAS  Google Scholar 

  • Wang H, Tang X, Sha J, Chen H, Sun T, Wang Y (2015) The reproductive toxicity on the rotifer Brachionus plicatilis induced by BDE-47 and studies on the effective mechanism based on antioxidant defense system changes. Chemosphere 135:129–137

    CAS  PubMed  Google Scholar 

  • Xia H, Song T, Wang L, Jiang L, Zhou Q, Wang W, Liu L, Yang P, Zhang X (2018) Effects of dietary toxic cyanobacteria and ammonia exposure on immune function of blunt snout bream (Megalabrama amblycephala). Fish Shellfish Immun 78:383–391

    CAS  Google Scholar 

  • Yang Z, Xiang F, Minter EJA, Lü K, Chen Y, Montagnes DJS (2011) The interactive effects of microcystin and nitrite on life-history parameters of the cladoceran Daphnia obtusa. J Hazard Mater 190:113–118

    CAS  PubMed  Google Scholar 

  • Yang J, Zhang X, Xie Y, Song C, Sun J, Zhang Y, Giesy JP, Yu H (2017) Ecogenomics of zooplankton community reveals ecological threshold of ammonia nitrogen. Environ Sci Technol 51:3057–3064

    CAS  PubMed  Google Scholar 

  • Yilmaz Ö, Keser S, Tuzcu M, Güvenc M, Çetintas B, Irtegün S, Tastan H, Sahin K (2009) A practical HPLC method to measure reduced (GSH) and oxidized (GSSG) glutathione concentrations in animal tissues. J Anim Vet Adv 8:343–347

    CAS  Google Scholar 

  • Yim B, Kim H, Jung MY, Lee YM (2015) Cadmium modulates the mRNA expression and activity of glutathione S-transferase in the monogonont rotifer Brachionus koreanus. Toxicol Environ Health Sci 7:217–223

    Google Scholar 

  • Zhang X, Chen C, Ding J, Hou A, Li Y, Niu Z, Su X, Xu Y, Laws EA (2010) The 2007 water crisis in Wuxi, China: Analysis of the origin. J Hazard Mater 182:130–135

    CAS  PubMed  Google Scholar 

  • Zhu X, Wang Q, Zhang L, Liu J (2015) Offspring performance of Daphnia magna after short-term maternal exposure to mixtures of microcystin and ammonia. Environ Sci Pollut Res 22:2800–2807

    CAS  Google Scholar 

  • Zong W, Wang Q, Zhang S, Teng Y, Du Y (2018) Regulation on the toxicity of microcystin-LR target to protein phosphatase 1 by biotransformation pathway: effectiveness and mechanism. Environ Sci Pollut Res 25:26020–26029

    CAS  Google Scholar 

  • Zweerus NL, Sommer S, Fontaneto D, Ozgul A (2017) Life-history responses to environmental change revealed by resurrected rotifers from a historically polluted lake. Hydrobiologia 796:121–130

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Numbers: 31772458 and 31272388), Science Foundation for Young Scientists of Jiangsu in China (Grant Number: 20171093), the Natural Science Foundation of the Jiangsu Higher Education Institutions of China (Grant Number: 19KJB180020), and the Startup Foundation for Introducing Talent of NUIST (Grant Number: 131061901013).

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Authors and Affiliations

  1. School of Marine Science and Engineering, Nanjing Normal University, No. 1 Wenyuan Road, Nanjing, 210023, People’s Republic of China

    Ye Liang, Li Shao & Jiaxin Yang

  2. School of Marine Sciences, Nanjing University of Information Science and Technology, No. 219 Ningliu Road, Nanjing, 210044, People’s Republic of China

    Ye Liang

  3. Freshwater Fisheries Research Institute of Jiangsu Province, No. 79 Chating East Street, Nanjing, 210017, People’s Republic of China

    Qichen Jiang

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  1. Ye Liang
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Correspondence to Jiaxin Yang.

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Liang, Y., Shao, L., Jiang, Q. et al. Changes in the life-cycle parameters and glutathione-related antioxidant defense system of rotifer Brachionus calyciflorus under the combined stress of microcystin-LR and ammonia. Aquat Ecol 54, 243–256 (2020). https://doi.org/10.1007/s10452-019-09739-8

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