Effects of Microcystis on Hypothalamic-Pituitary-Gonadal-Liver Axis in Nile Tilapia (Oreochromis niloticus)

  • Jiazhang Chen
  • Shunlong Meng
  • Hai XuEmail author
  • Zhen Zhang
  • Xiangyang Wu


In the present study, Nile tilapia (Oreochromis niloticus) were used to assess the endocrine disruption potential of Microcytis aeruginosa. Male Nile tilapia were exposed to lyophilized M. aeruginosa or purified microcystin-LR (8.3 μg/L) for 28 days. The levels of serum hormones (17β-estradiol and testosterone) and transcripts of selected genes in the hypothalamus-pituitary-gonadal-liver axis were analyzed. The results showed that serum hormones were significantly up-regulated, and transcripts of 13 genes (GHRH, PACAP, GH, GHR1, GHR2, IGF1, IGF2, CYP19a, CYP19b, 3β-HSD1, 20β-HSD, 17β-HSD1 and 17β-HSD8) were significantly altered after Microcytis exposure. These results indicate that fish reproduction can be altered in a Microcystis bloom-contaminated aquatic environment.


Microcystis MC-LR Brain Hypothalamus-pituitary-gonadal-liver axis Nile tilapia 



This work was supported financially by the National Major Project on Quality & Safety Risk Assessment for Agricultural Products (Grants GJFP2014009), Natural Science Foundation of Jiangsu Province of China (Grants BK20130488).

Supplementary material

128_2017_2051_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 18 KB)


  1. Chang X, Kobayashi T, Senthilkumaran B, Kobayashi-Kajura H, Sudhakumari CC, Nagahama Y (2005) Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus). Gen Comp Endocrinol 141:101–115CrossRefGoogle Scholar
  2. Chen L, Chen J, Zhang X, Xie P (2016) A review of reproductive toxicity of microcystins. J Hazard Mater 301:381–399CrossRefGoogle Scholar
  3. Dong GF, Xie SQ, Zhu XM, Han D, Yang YX (2012) Nutri-toxicological effects of cyanobacteria on fish. Acta Ecol Sin 32:6233–6241CrossRefGoogle Scholar
  4. Ishida K, Okita Y, Matsuda H, Okino T, Murakami M (1999) Aeruginosins, protease inhibitors from the cyanobacterium Microcystis aeruginosa. Tetrahedron 55:10971–10988CrossRefGoogle Scholar
  5. Jo A, Ji K, Choi K (2014) Endocrine disruption effects of long-term exposure to perfluorodecanoic acid (PFDA) and perfluorotridecanoic acid (PFTrDA) in zebrafish (Danio rerio) and related mechanisms. Chemosphere 108:360–366CrossRefGoogle Scholar
  6. Kamjunke N, Schmidt K, Pflugmacher S, Mehner T (2002) Consumption of cyanobacteria by roach (Rutilus rutilus): useful or harmful to the fish? Fresh Biol 47:243–250CrossRefGoogle Scholar
  7. Liang H, Zhou W, Zhang Y, Qiao Q, Zhang X (2015) Are fish fed with cyanobacteria safe, nutritious and delicious? A laboratory study. Sci Rep 5:15166 doi: 10.1038/srep15166 CrossRefGoogle Scholar
  8. Liu W, Chen C, Chen L, Wang L, Li J, Chen Y, Jin J, Kawan A, Zhang X (2016) Sex-dependent effects of microcystin-LR on hypothalamic-pituitary-gonad axis and gametogenesis of adult zebrafish. Sci Rep 6:22819 doi: 10.1038/srep22819 CrossRefGoogle Scholar
  9. Ma Y, Han J, Guo Y, Lam PKS, Wu RSS, Giesy JP, Zhang X, Zhou B (2012) Disruption of endocrine function in in vitro H295R cell-based and in in vivo assay in zebrafish by 2,4-dichlorophenol. Aquat Toxicol 106–107:173–181CrossRefGoogle Scholar
  10. Malbrouck C, Kestemont P (2006) Effects of microcystins on fish. Environ Toxicol Chem 25:72–86CrossRefGoogle Scholar
  11. Palikova M, Mares J, Kopp R, Hlavkova J, Navratil S, Adamovsky O, Chmelar L, Blaha L (2011) Accumulation of microcystins in Nile tilapia, Oreochromis niloticus L., and effects of a complex cyanobacterial bloom on the dietetic quality of muscles. Bull Environ Contam Toxicol 87:26–30CrossRefGoogle Scholar
  12. Palíková M, Krejčí R, Hilscherová R, Babica P, Navrátil S, Kopp R, Bláha L (2007) Effect of different cyanobacterial biomasses and their fractions with variable microcystin content on embryonal development of carp (Cyprinus carpio L.). Aquat Toxicol 81:312–318CrossRefGoogle Scholar
  13. Puddick J, Prinsep MR, Wood SA, Kaufononga SAF, Cary SC, Hamilton DP (2014) High levels of structural diversity observed in microcystins from microcystis CAWBG11 and characterization of six new microcystin congeners. Mar Drugs 12:5372–5395CrossRefGoogle Scholar
  14. Reinecke M, Björnsson BT, Dickhoff WW, McCormick SD, Navarro I, Power DM, Gutiérrez J (2005) Growth hormone and insulin-like growth factors in fish: Where we are and where to go. Gen Comp Endocrinol 142:20–24CrossRefGoogle Scholar
  15. Rogers ED, Henry TB, Twiner MJ, Gouffon JS, McPherson JT, Boyer GL, Sayler GS, Wilhelm SW (2011) Global gene expression profiling in larval zebrafish exposed to microcystin-LR and Microcystis reveals endocrine disrupting effects of cyanobacteria. Environ Sci Technol 45:1962–1969CrossRefGoogle Scholar
  16. Rohrlack T, Christoffersen K, Hansen PE, Zhang W, Czarnecki O, Henning M, Fastner J, Erhard M, Neilan BA, Kaebernick M (2003) Isolation, characterization, and quantitative analysis of microviridin J, a new Microcystis metabolite toxic to Daphnia. J Chem Ecol 29:1757–1770CrossRefGoogle Scholar
  17. Senthilkumaran B, Sudhakumari CC, Chang XT, Kobayashi T, Oba Y, Guan G, Yoshiura Y, Yoshikuni M, Nagahama Y (2002) Ovarian carbonyl reductase-like 20beta-hydroxysteroid dehydrogenase shows distinct surge in messenger RNA expression during natural and gonadotropin-induced meiotic maturation in Nile tilapia. Biol Reprod 67:1080–1086CrossRefGoogle Scholar
  18. Senthilkumaran B, Sudhakumari CC, Wang DS, Sreenivasulu G, Kobayashi T, Kobayashi HK, Yoshikuni M, Nagahama Y (2009) Novel 3beta-hydroxysteroid dehydrogenases from gonads of the Nile tilapia: phylogenetic significance and expression during reproductive cycle. Mol Cell Endocrinol 299:146–152CrossRefGoogle Scholar
  19. Smith JL, Boyer GL, Zimba PV (2008) A review of cyanobacterial odorous and bioactive metabolites: Impacts and management alternatives in aquaculture. Aquaculture 280:5–20CrossRefGoogle Scholar
  20. Sychrová E, Štěpánková T, Nováková K, Bláha L, Giesy JP, Hilscherová K (2012) Estrogenic activity in extracts and exudates of cyanobacteria and green algae. Environ Int 39:134–140CrossRefGoogle Scholar
  21. Yamaki H, Sitachitta N, Sano T, Kaya K (2005) Two new chymotrypsin inhibitors isolated from the cyanobacterium Microcystis aeruginosa NIES-88. J Nat Prod 68:14–18CrossRefGoogle Scholar
  22. Zhao M, Xie S, Zhu X, Yang Y, Gan N, Song L (2006) Effect of dietary cyanobacteria on growth and accumulation of microcystins in Nile tilapia (Oreochromis niloticus). Aquaculture 261:960–966CrossRefGoogle Scholar
  23. Zhou LY, Wang DS, Senthilkumaran B, Yoshikuni M, Shibata Y, Kobayashi T, Sudhakumari CC, Nagahama Y (2005) Cloning, expression and characterization of three types of 17beta-hydroxysteroid dehydrogenases from the Nile tilapia, Oreochromis niloticus. J Mol Endocrinol 35:103–116CrossRefGoogle Scholar
  24. Ziková A, Trubiroha A, Wiegand C, Wuertz S, Rennert B, Pflugmacher S, Kopp R, Mareš J, Kloas W (2010) Impact of microcystin containing diets on physiological performance of Nile tilapia (Oreochromis niloticus) concerning stress and growth. Environ Toxicol Chem 29:561–568CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Freshwater Fisheries Research CenterChinese Academy of Fishery SciencesWuxiChina
  2. 2.Key Laboratory of Fishery Eco-environment Assessment and Resource Conservation in Middle and Lower Reaches of the Yangtze RiverCAFSWuxiChina
  3. 3.School of Environment and Safety EngineeringJiangsu UniversityZhenjiangChina

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