Salinity modulates biochemical and histopathological changes caused by silver nanoparticles in juvenile Persian sturgeon (Acipenser persicus)

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The objective of this study was to evaluate the effect of salinity on the acute and sub-chronic toxicity of silver nanoparticles (AgNPs) in Persian sturgeon. This was evaluated by exposing Persian sturgeon to AgNPs in three salinities: freshwater (F: 0.4 ppt), brackish water 1 (B1: 6 ± 0.2 ppt), and brackish water 2 (B2: 12 ± 0.3 ppt) for 14 days, which was followed by analysis of alterations in plasma chemistry and histopathology of the gills, liver, and intestine. Values of 96-h median lethal concentration (LC50) were calculated as 0.89 mg/L in F, 2.07 mg/L in B1, and 1.59 mg/L in B2. After sub-chronic exposures, plasma cortisol, glucose, potassium, and sodium levels illustrated no significant changes within each salinity level. In F, 0.2 mg/L AgNP caused the highest levels of alkaline phosphatase and osmolality levels. In B1, 0.6 mg/L AgNP induced the highest level of alkaline phosphatase and elevated plasma osmolality was recorded in all AgNP-exposed treatments in comparison with the controls. The B2 treatment combined with 0.6 mg/L AgNP significantly reduced plasma chloride level. The results showed elevating salinity significantly increased osmolality, chloride, sodium, and potassium levels of plasma in the fish exposed to AgNPs. The abundance of the tissue lesions was AgNP concentration-dependent, where the highest number of damages was observed in the gills, followed by liver and intestine, respectively. The histopathological study also confirmed alterations such as degeneration of lamella, lifting of lamellar epithelium, hepatic vacuolation, pyknotic nuclei, and cellular infiltration of the lamina propria elicited by AgNPs in the gills, liver, and intestine of Persian sturgeon. In conclusion, the stability of AgNPs in aquatic environments can be regulated by changing the salinity, noting that AgNPs are more stable in low salinity waters.

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  1. Abedi S, Sharifpour I, Mozanzadeh MT, Zorriehzahra J, Khodabandeh S, Gisbert E (2015) A histological and ultrastructural study of the skin of rainbow trout (Oncorhynchus mykiss) alevins exposed to different levels of ultraviolet B radiation. J Photochem Photobiol B 147:56–62

  2. Afshinnia K, Marrone B, Baalousha M (2018) Potential impact of natural organic ligands on the colloidal stability of silver nanoparticles. Sci Total Environ 625:1518–1526

  3. Al-Bairuty GA, Shaw BJ, Handy RD, Henry TB (2013) Histopathological effects of waterborne copper nanoparticles and copper sulphate on the organs of rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 126:104–115

  4. Ale A, Rossi AS, Bacchetta C, Gervasio S, de la Torre FR, Cazenave J (2018) Integrative assessment of silver nanoparticles toxicity in Prochilodus lineatus fish. Ecol Indic 93:1190–1198

  5. APHA, American Public Health Association, American Water Works Association, Water Environment Association (1998) Standard methods for the examination of water and wastewater. 20th edition. American Public Health Association, Washington, D.C., USA

  6. Ansar S, Abudawood M, Hamed SS, Aleem MM (2017) Sodium selenite protects against silver nanoparticle-induced testicular toxicity and inflammation. Biol Trace Elem Res 175:161

  7. Asghari S, Johari SA, Lee JH, Kim YS, Jeon YB, Choi HJ, Moon MC, Yu IJ (2012) Toxicity of various silver nanoparticles compared to silver ions in Daphnia magna. J Nanobiotechnol 10:1–14

  8. Bacchetta C, Ale A, Simoniello MF, Gervasio S, Davico C, Rossi AS, Desimone MF, Poletta G, López G, Monserrat JM, Cazenave J (2017) Genotoxicity and oxidative stress in fish after a short-term exposure to silver nanoparticles. Ecol Indic 76:230–239

  9. Banan A, Kalbassi Masjed Shahi MR, Bahmani M, Yazdani Sadati MA (2016) Toxicity assessment of silver nanoparticles in Persian sturgeon (Acipenser persicus) and starry sturgeon (Acipenser stellatus) during early life stages. Environ Sci Pollut Res Int 23:10139–10144

  10. Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34

  11. Best JH, Eddy FB, Codd GA (2003) Effects of microcystis cells, cell extracts and lipopolysaccharide on drinking and liver function in rainbow trout Oncorhynchus mykiss Walbaum. Aquat Toxicol 64:419–426

  12. Bronzi P, Rosenthal H, Gessner J (2011) Global sturgeon aquaculture production: an overview. J Appl Ichthyol 27(2):169–175

  13. Burke J, Handy RD, Roast SD (2003) Effect of low salinity on cadmium accumulation and calcium homeostasis in the shore crab (Carcinus maenas) at fixed free Cd2+ concentrations. Environ Toxicol Chem 22:2761–2767

  14. Cambier S, Rogeberg M, Georgantzopoulou A, Serchi T, Karlsson C, Verhaegen S, Iversen TG, Guignard C, Kruszewski M, Hoffmann L, Audinot JN, Ropstad E, Gutleb AC (2018) Fate and effects of silver nanoparticles on early life-stage development of zebrafish (Danio rerio) in comparison to silver nitrate. Sci Total Environ 610-611:972–982

  15. Christensen EAF, Svendsen MBS, Steffensen JF (2017) Plasma osmolality and oxygen consumption of perch Perca fluviatilis in response to different salinities and temperatures. J Fish Biol 90:819–833

  16. Du J, Tang J, Xu S, Ge J, Dong Y, Li H, Jin M (2018) A review on silver nanoparticles-induced ecotoxicity and the underlying toxicity mechanisms. Regul Toxicol Pharmacol 98:231–239

  17. Erfan Shahkar, Dae-jung Kim, Mahmoud Mohseni, Hyeonho Yun, Sungchul C. Bai, (2015) Effects of Salinity Changes on Hematological Responses in Juvenile Ship Sturgeon Acipenser nudiventris. Fisheries and aquatic sciences 18 (1):45–50

  18. Firat Ö, Cogun HY, Yüzereroğlu TA, Gök G, Firat Ö, Kargin F, Kötemen Y (2011) A comparative study on the effects of a pesticide (cypermethrin) and two metals (copper, lead) to serum biochemistry of Nile tilapia, Oreochromis niloticus. Fish Physiol Biochem 37:657–666

  19. Gambardella C, Costa E, Piazza V, Fabbrocini A, Magi E, Faimali M, Garaventa F (2015) Effect of silver nanoparticles on marine organisms belonging to different trophic levels. Mar Environ Res 111:41–49

  20. Giese B, Klaessig F, Park B, Kaegi R, Steinfeldt M, Wigger H, von Gleich A, Gottschalk F (2018) Risks, release and concentrations of engineered nanomaterial in the environment. Sci Rep 81:1565

  21. Griffitt RJ, Lavelle CM, Kane AS, Denslow ND, Barber DS (2013) Chronic nanoparticulate silver exposure results in tissue accumulation and transcriptomic changes in zebrafish. Aquat Toxicol 130-131:192–200

  22. Handy RD, Al-Bairuty G, Al-Jubory A, Ramsden CS, Boyle D, Shaw BJ, Henry TB (2011) Effects of manufactured nanomaterials on fishes: a target organ and body systems physiology approach. J Fish Biol 79:821–853

  23. Imsland AK, Gunnarsson S, Foss A, Stefansson SO (2003) Gill Na+,K+-ATPase activity, plasma chloride and osmolality in juvenile turbot (Scophthalmus maximus) reared at different temperatures and salinities. Aquaculture 218:671–683

  24. INIC (2019) Iran Nanotechnology Initiative Council’s website. Accessed 10 Aug 2019

  25. Jang MH, Kim WK, Lee SK, Henry TB, Park JW (2014) Uptake, tissue distribution, and depuration of total silver in common carp (Cyprinus carpio) after aqueous exposure to silver nanoparticles. Environ Sci Technol 48(19):11568–11574

  26. Johari SA, Kalbassi MR, Soltani M, Yu IJ (2013) Toxicity comparison of colloidal silver nanoparticles in various life stages of rainbow trout (Oncorhynchus mykiss). Iran J Fish Sci 12(1):76–95

  27. Johari SA, Kalbassi MR, Yu IJ, Lee JH (2015) Chronic effect of waterborne silver nanoparticles on rainbow trout (Oncorhynchus mykiss): histopathology and bioaccumulation. Comp Clin Pathol 24(5):995–1007

  28. Johari SA, Sarkheil M, Tayemeh MB, Veisi S (2018) Influence of salinity on the toxicity of silver nanoparticles (AgNPs) and silver nitrate (AgNO3) in halophilic microalgae, Dunaliella salina. Chemosphere 209:156–162

  29. Joo HS, Kalbassi MR, Yu IJ, Lee JH, Johari SA (2013) Bioaccumulation of silver nanoparticles in rainbow trout (Oncorhynchus mykiss): influence of concentration and salinity. Aquat Toxicol 140-141(7):398–406

  30. Joo HS, Kalbassi MR, Johari SA (2018) Hematological and histopathological effects of silver nanoparticles in rainbow trout (Oncorhynchus mykiss)—how about increase of salinity? Environ Sci Pollut Res 25:15449

  31. Katuli KK, Massarsky A, Hadadi A, Pourmehran Z (2014) Silver nanoparticles inhibit the gill Na+/K+-ATPase and erythrocyte AChE activities and induce the stress response in adult zebrafish (Danio rerio). Ecotoxicol Environ Saf 106:173–180

  32. Khosravi-Katuli K, Shabani A, Paknejad H, Imanpoor MR (2018) Comparative toxicity of silver nanoparticle and ionic silver in juvenile common carp (Cyprinus carpio): accumulation, physiology and histopathology. J Hazard Mater 359:373–381

  33. Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life-cycle emissions of engineered nanomaterials. J Nanopart Res 15:1692

  34. Lacave JM, Vicario-Parés U, Bilbao E, Gilliland D, Mura F, Dini L, Cajaraville MP, Orbea A (2018) Waterborne exposure of adult zebrafish to silver nanoparticles and to ionic silver results in differential silver accumulation and effects at cellular and molecular levels. Sci Total Environ 642:1209–1220

  35. Lee B, Duong CN, Cho J, Lee J, Kim K, Seo Y, Kim P, Choi K, Yoon J (2012) Toxicity of citrate-capped silver nanoparticles in common carp (Cyprinus carpio). J Biomed Biotechnol 2012:14

  36. Lee JW, Kim JE, Shin YJ, Ryu JS, Eom IC, Lee JS, Kim Y, Kim PJ, Choi KH, Lee BC (2014) Serum and ultrastructure responses of common carp (Cyprinus carpio L.) during long-term exposure to zinc oxide nanoparticles. Ecotoxicol Environ Saf 104:9–17

  37. Martínez-Alvarez RM, Hidalgo MC, Domezain A, Morales AE, García-Gallego M, Sanz A (2002) Physiological changes of sturgeon Acipenser naccarii caused by increasing environmental salinity. J Exp Biol 205:3699–3706

  38. Masouleh FF, Amiri BM, Mirvaghefi A, Ghafoori H, Madsen SS (2017) Silver nanoparticles cause osmoregulatory impairment and oxidative stress in Caspian kutum (Rutilus kutum, Kamensky 1901). Environ Monit Assess 189(9):448

  39. McCarthy MP, Carroll DL, Ringwood AH (2013) Tissue specific responses of oysters, Crassostrea virginica, to silver nanoparticles. Aquat Toxicol 138:123–128

  40. Murray LM, Rennie MD, Enders EC, Pleskach K, Martin JD (2017) Effect of nanosilver on cortisol release and morphometrics in rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 36:1606–1613

  41. Nia JR (2011) Preparation of colloidal nanosilver. Google US Patent

  42. Nickum JG, Bart HL Jr, Bowser PR, Greer IE, Hubbs C, Jenkins JA, MacMillan JR, Rachlin JW, Rose JD, Sorensen PW, Tomasso JR (2004) Guidelines for the use of fishes in research. American Fisheries Society, Bethesda, 54 pages

  43. NIOSH (National Institute for Occupational Safety and Health) (1999) NIOSH manual of analytical methods, method no. 7300. NIOSH, Cincinnati

  44. OECD (1992) OECD guidelines for the testing of chemicals. Guideline No. 203: Acute Toxicity for Fish. Organization for Economic Cooperation and Development, Paris

  45. OECD (1984) OECD guidelines for the testing of chemicals. Guideline No. 204: Fish, Prolonged Toxicity Test: 14-Day Study. Organization for Economic Cooperation and Development, Paris, France

  46. Ostaszewska T, Chojnacki M, Kamaszewski M, Sawosz-Chwalibóg E (2016) Histopathological effects of silver and copper nanoparticles on the epidermis, gills, and liver of Siberian sturgeon. Environ Sci Pollut Res 23(2):1621–1633

  47. Pulit-Prociak J, Banach M (2016) Silver nanoparticles—a material of the future...? Open Chem 14:76–91

  48. Redding JM, Schreck CB, Birks EK, Ewing RD (1984) Cortisol and its effect on plasma thyroid hormone and electrolyte concentrations in freshwater and during seawater acclimation in yearling coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 56:146–155

  49. Ribeiro F, Gallego-Urrea JA, Jurkschat K, Crossley A, Hassellöv M, Taylor C, Soares AMVM, Loureiro S (2014) Silver nanoparticles and silver nitrate induce high toxicity to Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio. Sci Total Environ 466-467:232–241

  50. Hischier R (2014) Life cycle assessment of manufactured nanomaterials: inventory modelling rules and application example. The International Journal of Life Cycle Assessment 19 (4):941–943

  51. Salari Joo H, Kalbassi MR, Johari SA (2012) Effect of water salinity on acute toxicity of colloidal silver nanoparticles in rainbow trout (Oncorhynchus mykiss) larvae. Iran J Health Environ 5(2):121–131

  52. Sendra M, Yeste M, Gatica J, Moreno-Garrido I, Blasco J (2017) Direct and indirect effects of silver nanoparticles on freshwater and marine microalgae (Chlamydomonas reinhardtii and Phaeodactylum tricornutum). Chemosphere 179:279–289

  53. Shaluei F, Hedayati A, Jahanbakhshi A, Kolangi H, Fotovat M (2013) Effect of subacute exposure to silver nanoparticle on some hematological and plasma biochemical indices in silver carp (Hypophthalmichthys molitrix). Hum Exp Toxicol 32(12):1270–1277

  54. Shobana C, Rangasamy B, Poopal RK, Renuka S, Ramesh M (2018) Green synthesis of silver nanoparticles using Piper nigrum: tissue-specific bioaccumulation, histopathology, and oxidative stress responses in Indian major carp Labeo rohita. Environ Sci Pollut Res 25(12):11812–11832

  55. Skeggs L Jr, Hochstrassat J (1964) Colorimetric determination of chloride in serum and plasma. Clin Chem 10:918–936

  56. Sotoudeh E, Mardani F (2018) Antioxidant-related parameters, digestive enzyme activity and intestinal morphology in rainbow trout (Oncorhynchus mykiss) fry fed graded levels of red seaweed, Gracilaria pygmaea. Aquac Nutr 24:777–785

  57. Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D, Hull MS (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory, Beilstein J. Nanotechnol. 6:1769–1780

  58. Wang J, Wang W (2014) Salinity influences on the uptake of silver nanoparticles and silver nitrate by marine medaka (Oryzias melastigma). Environ Toxicol Chem 33(3):632–640

  59. Wang H, Burgess RM, Cantwell MG, Portis LM, Perron MM, Wu F, Ho KT (2014) Stability and aggregation of silver and titanium dioxide nanoparticles in seawater: role of salinity and dissolved organic carbon. Environ Toxicol Chem 33(5):1023–1029

  60. Wu Y, Zhou Q (2013) Silver nanoparticles cause oxidative damage and histological changes in medaka (Oryzias latipes) after 14 days of exposure. Environ Toxicol Chem 32:165–173

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The corresponding authors would like to acknowledge the support of Lorestan University, Tarbiat Modares University, University of Nebraska at Omaha and Iran Nanotechnology Initiative Council.

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This study was financially supported by Iran’s Ministry of Science, Research and Technology (MSRT, IRAN) (grant number 92-5641).

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Correspondence to Ashkan Banan or Mohammad Reza Kalbassi.

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Banan, A., Kalbassi, M.R., Bahmani, M. et al. Salinity modulates biochemical and histopathological changes caused by silver nanoparticles in juvenile Persian sturgeon (Acipenser persicus). Environ Sci Pollut Res (2020).

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  • Metal nanoparticles
  • Nanoecotoxicology
  • Histopathology
  • Colloidal silver
  • Persian sturgeon
  • Gills