Abstract
The effectiveness of silver nanoparticles (AgNPs) in aquaculture has been investigated recently; however, understanding AgNPs cytotoxicity in aquatic organisms is still limited. This study examines the histopathological effects of the interaction AgNPs with white spot syndrome virus (WSSV) virions on the white shrimp Penaeus vannamei after intramuscular application. Two tests were carried out: in the first test, nine solutions were prepared: two individual AgNPs concentrations, two individual viral loads (vcWS), and four treatments derived from an interaction of AgNPs and vcWS, and a distilled water control, the toxicity and histopathological effects were also evaluated. For the second test, four solutions were prepared: AgNPs concentration, two AgNPs concentrations with a viral load, and distilled water control, to evaluate the progression of WSSV infection. In test 1, the individual and combined AgNPs treatments gave a dose-dependent negative effect on shrimp survival in the first 36 h post-injection (hpi). At 96 hpi no significant differences (p > 0.05) were found in the higher AgNPs concentrations vs. their interaction with vcWS and vcWS individual concentrations. In test 2, a cytotoxic effect associated with AgNPs was observed after 24 hpi in all treatments. WSSV severity was low and identified at 72 and 96 hpi in all interaction treatments. The results show that AgNPs affect vcWS when in direct contact, while, AgNPs + WS inoculum cause severe damage to shrimp tissue and WSSV infection development is only temporarily delayed.
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The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.
References
Abad-Rosales SM, Frías-Espericueta MG, Romero-Bernal OG, Lozano-Olvera R, García-Gasca SA, Montoya-Rodríguez L, Voltolina D (2019) White spot syndrome virus (WSSV) infection and immunity responses in white shrimp (Litopenaeus vannamei) exposed to sublethal levels of metals. Aquac Res 50:758–764. https://doi.org/10.1111/are.13932
Akter M, Sikder MT, Rahman MM, Ullah AKMA, Hossain KFB, Banik S, Hosokawa T, Saito T, Kurasaki M (2018) A systematic review on silver nanoparticles-induced cytotoxicity: physicochemical properties and perspectives. J Adv Res 9:1–16. https://doi.org/10.1016/j.jare.2017.10.008
Ashley P (2007) Fish welfare: current issues in aquaculture. Appl Anim Behave Sci 104:199235. https://doi.org/10.1016/j.applanim.2006.09.001
Banumathi B, Vaseeharan B, Suganya P, Citarasu T, Govindarajan M, Alharbi NS, Kadaikunnan S, Khaled JM, Benelli G (2017) Toxicity of Camellia sinensis fabricated silver nanoparticles on invertebrate and vertebrate organisms: morphological abnormalities and DNA damages. J Clust Sci 28:2027–2040. https://doi.org/10.1007/s10876-017-1201-5
Bell TA, Lightner DV (1988) A handbook of normal shrimp histology. Special publication No. 1. World Aquaculture Society, Baton Rouge, LA
Borrego B, Lorenzo G, Mota-Morales J, Almanza-Reyes H, Mateos F, Lopez-Gill E, De la Rosa N, Burmostrov VA, Pestryakov AN, Brun A, Bugdanchikova N (2016) Potential application of silver nanoparticles to control the infectivity of Rift Valley Fever Virus in vitro and in vivo. Nanomedicine 12:1185–1192. https://doi.org/10.1016/j.nano.2016.01.021
Carlson C, Hussain SM, Schrand AM, Braydich-Stolle LK, Hess KL, Jones RL, Schlager JJ (2008) Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 30:112. https://doi.org/10.1021/jp712087m
Chang YS, Liu WJ, Lee CC, Chou TL, Lee YT, Wu TS, Huang JY, Huang WT, Lee TL, Kou GH, Wang AHJ, Lo CF (2010) A 3D model of the membrane protein complex formed by the white spot syndrome virus structural proteins. PLoS ONE 5:e10718. https://doi.org/10.1371/journal.pone.0010718
Chávez-Sánchez MC, Abad-Rosales S, Lozano-Olvera R, Montoya-Rodríguez L, Franco-Nava M, Mejía-Ruíz CH, Pestryakov A, Bogdanchikova N (2021) Silver nanoparticles induce histopathological alterations in juvenile Penaeus vannamei. Environ Sci Pollut Res 28:8224–8234. https://doi.org/10.1007/s11356-020-11175-3
Chen IT, Aoki T, Huang YT, Hirono I, Chen TC, Huang JY, Lo CF, Wang HC (2011) White spot syndrome virus induces metabolic changes resembling the warburg effect in shrimp hemocytes in the early stage of infection. J Virol 85:12919–12928. https://doi.org/10.1128/JVI.05385-11
Chinnasamy A, Samou-Michael J, Durai P, Devakumar C (2014) Toxicity effect of silver nanoparticles in brine shrimp Artemia. Sci World J 256919:1–10. https://doi.org/10.1155/2014/256919
Conover WJ (2012) The rank transformation-an easy and intuitive way to connect many nonparametric methods to their parametric counterparts for seamless teaching introductory statistics courses. Wires Comp Stat 4:432–438. https://doi.org/10.1002/wics.1216
Conover WJ, Iman RL (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35:124–129. https://doi.org/10.2307/2683975
Dos-Santos CA, Martins SM, Ingle AP, Gupta I, Galdiero S, Galdiero M, Gade A, Rai M (2014) Silver nanoparticles: therapeutical uses, toxicity and safety issues. J Pharm Sci 103:1931–1944. https://doi.org/10.1002/jps.24001
Flegel TW (2012) Historic emergence, impact and current status of shrimp pathogens in Asia. J Invertebr Pathol 110:166–173. https://doi.org/10.1016/j.jip.2012.03.004
Flegel TW (2019) A future vision for disease control in shrimp aquaculture. J World Aquac Soc 50:249–266. https://doi.org/10.1111/jwas.12589
Galdiero S, Falanga A, Vitiello M, Cantisani M, Marra V, Galdiero M (2011) Silver nanoparticles as potential antiviral agents. Molecules 16:8894–8918. https://doi.org/10.3390/molecules16108894
Gliga AR, Skoglund S, Wallinder IO, Fadeel B, Karlsson HL (2014) Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and ag release. Part Fibre Toxicol 11:11. https://doi.org/10.1186/1743-8977-11-11
Hsiao IL, Hsieh YK, Wang CF, Chen IC, Huang YJ (2015) Trojan-horse mechanism in the cellular uptake of silver nanoparticles verified by direct intra- and extracellular silver speciation analysis. Environ Sci Technol 49:3813–3821. https://doi.org/10.1021/es504705p
Ishwarya R, Vaseeharan B, Shanthi S, Ramesh S, Manogari P, Dhanalakshmi K, Vijayakumar S, Benelli G (2017) Green synthesized silver nanoparticles: toxicity against Poecilia reticulata fishes and Ceriodaphnia cornuta crustaceans. J Clust Sci 28:519–527. https://doi.org/10.1007/s10876-016-1126-4
Jimeno-Romero A, Bilbao E, Izagirre U, Cajaraville MP, Marigómez I, Soto M (2017) Digestive cell lysosomes as main targets for ag accumulation and toxicity in marine mussels, Mytilus galloprovincialis, exposed to maltose-stabilised Ag nanoparticles of different sizes. Nanotoxicology 11:168–183. https://doi.org/10.1080/17435390.2017.1279358
Juarez-Moreno K, Mejía-Ruiz CH, Díaz F, Reyna-Verdugo H, Re AD, Vazquez-Felix EF, Sánchez-Castrejón E, Mota-Morales JD, Pestryakov A, Bogdanchikova N (2017) Effect of silver nanoparticles on the metabolic rate, hematological response, and survival of juvenile white shrimp Litopenaeus vannamei. Chemosphere 169:716–724. https://doi.org/10.1016/j.chemosphere.2016.11.054
Karunasagar I, Ababouch L (2012) Shrimp viral diseases, import risk assessment and international trade. Indian J Virol 23:141–148. https://doi.org/10.1007/s13337-012-0081-4
Khadijah S, Ying-Neo S, Hossain MS, Miller LD, Mathavan S, Kwang J (2003) Identification of white spot syndrome virus latency-related genes in specific-pathogen-free shrimps by use of a microarray. J Virol 77:10162–10167. https://doi.org/10.1128/JVI.77.18.10162-10167.2003
Lara HH, Ayala-Nuñez NV, Ixtepan-Turrent L, Rodriguez-Padilla C (2010a) Mode of antiviral action of silver nanoparticles against HIV-1. J Nanobiotechnol 8:1. https://doi.org/10.1186/1477-3155-8-1
Lara HH, Ixtepan-Turrent L, Garza-Treviño EN, Rodriguez-Padilla C (2010b) PVP-coated silver nanoparticles block the transmission of cell-free and cell-associated HIV-1 in human cervical culture. J Nanobiotechnol 8(1):1–11. https://doi.org/10.1186/1477-3155-8-15
Lara HH, Romero-Urbina DG, Pierce C, Lopez-Ribo JL, Arellano-Jiménez MJ, Yacaman MJ (2015) Effect of silver nanoparticles on Candida albicans biofilms: an ultrastructural study. J Nanobiotechnol 13:2–12. https://doi.org/10.1186/s12951-015-0147-8
Lekamge S, Miranda AF, Abraham A, Li V, Shukla R, Bansal V, Nugegoda D (2018) The toxicity of silver nanoparticles (AgNPs) to three freshwater invertebrates with different life strategies: Hydra Vulgaris, Daphnia carinata, and Paratya australiensis. Front Environ Sci 6:152. https://doi.org/10.3389/fenvs.2018.00152
Lekamge S, Miranda AF, Ball AS, Shukla R, Nugegoda D (2019) The toxicity of coated silver nanoparticles to Daphnia carinata and trophic transfer from alga Raphidocelis subcapitata. PLoS ONE 14:e0214398. https://doi.org/10.1371/journal.pone.0214398
Liang Y, Meng-Lin X, Xiao-Wen W, Xiao-Xiao G, Jun-Jun Ch, Chen L, Jie H (2015) ATP synthesis is active on the cell surface of the shrimp Litopenaeus vannamei and is suppressed by WSSV infection. Virol J 12:49. https://doi.org/10.1186/s12985-015-0275-7
Lightner DV (1996) A handbook of shrimp pathology and diagnostic procedures for diseases of cultured penaeid shrimp. World Aquaculture Society: Baton Rouge, LA. USA
Lightner DV (2011) Virus diseases of farmed shrimp in the western hemisphere (the Americas): a review. J Invert Pathol 106:110–130. https://doi.org/10.1016/j.jip.2010.09.012
Lightner DV, Hasson KW, White BL, Redman RM (1998) Experimental infection of western hemisphere penaeid shrimp with asian white spot syndrome virus and asian yellow head virus. J Aquat Anim Health 10:271–281. https://doi.org/10.1577/1548-8667(1998)010%3C;0271:EIOWHP%3E;2.0.CO;2
Lu L, Kwang J (2004) Identification of a novel shrimp protein phosphatase and its association with latency-related ORF427 of white spot syndrome virus. FEBS Lett 577:141–146. https://doi.org/10.1016/j.febslet.2004.08.087
MacLachlan NJ, Dubovi EJ (2017) The nature of virus in Fenner’s veterinary virology. 5 edition Elsevier
Maldonado-Muñiz M, Luna C, Mendoza-Reséndez R, Barriga-Castro ED, Soto-Rodriguez S, Ricque-Marie D, Cruz-Suarez LE (2020) Silver nanoparticles against acute hepatopancreatic necrosis disease (AHPND) in shrimp and their depuration kinetics. J Appl Phycol 32:2431–2445. https://doi.org/10.1007/s10811-019-01948-w
Mehrbod P, Motamed N, Tabatabaian M, Soleimani ER, Amini E, Shahidi M, Kheri MT (2009) in vitro antiviral effect of Nanosilver. On Influenza Virus DARU 17:88–93
Mori Y, Ono T, Miyahira Y, Quang-Nguyen V, Matsui T, Ishinara M (2013) Antiviral activity of silver nanoparticle chitosan composites against H1N1 influenza a virus. Nanoscale Res Lett 8:93. https://doi.org/10.1186/1556-276X-8-93
Nunan LM, Poulos BT, Lightner DV (1998) The detection of white spot syndrome virus WSSV and yellow head virus YHV in imported commodity shrimp. Aquaculture 160:19–30. https://doi.org/10.1016/S0044-8486(97)00222-6
Ochoa-Meza AR, Álvarez-Sánchez AR, Romo-Quiñonez CR, Barraza A, Magallón-Barajas FJ, Chávez-Sánchez A, García-Ramos JC, Toledo-Magaña Y, Bogdanchikova N, Pestryakov A, Mejía-Ruíz CH (2019) Silver nanoparticles enhance survival of white spot syndrome virus infected Penaeus vannamei shrimps by activation of its immunological system. Fish Shellfish Immunol 84:1083–1089. https://doi.org/10.1016/j.fsi.2018.10.007
OIE (World Organization for Animal Health) (2019) Manual of Diagnostic Tests for Aquatic Animals. Available in https://www.oie.int/index.php?id=2439&L=2&htmfile=chapitre_wsd.htm
Perde-Schrepler M, Florea A, Brie I, Virag P, Fischer-Fodor E, Vâlcan A, Gurzău E, Lisencu C, Maniu A (2019) Size-dependent cytotoxicity and genotoxicity of silver nanoparticles in cochlear cells in vitro. J Nanomater 2019:6090259. https://doi.org/10.1155/2019/6090259
Romo-Quiñonez CR, Álvarez-Sánchez AR, Álvarez-Ruiz P, Chávez-Sánchez MC, Bogdanchikova N, Pestryakov A, Mejia-Ruiz CH (2020) Evaluation of a new Argovit as an antiviral agent included in feed to protect the shrimp Litopenaeus vannamei against white spot syndrome virus infection. PeerJ 8:e8446. https://doi.org/10.7717/peerj.8446
Sonnenholzner S, Rodríguez J, Pérez F, Betancourt I, Echeverría F, Calderón J (2002) Supervivencia y respuesta inmune de camarones juveniles L. vannamei desafiados por vía oral a WSSV a diferentes temperaturas. Manejo de enfermedades en camarones. Contribuciones del Centro Nacional de Acuicultura e Investigaciones Marinas (CENAIM) durante el VI Congreso Ecuatoriano de Acuicultura
Sooklert K, Wongjarupong A, Cherdchom S, Wongjarupong N, Jindatip D, Phungnoi Y, Rojanathanes R, Sreemaspun A (2019) Molecular and morphological evidence of hepatotoxicity after silver nanoparticle exposure: a systematic review, in silico, and ultrastructure investigation. Toxicol Res 35:257–270. https://doi.org/10.5487/TR.2019.35.3.257
Sritunyalucksana K, Wannapapho W, Lo CF, Flegel TW (2006) PmRab7 is a VP28-binding protein involved in white spot syndrome virus infection in shrimp. J Virol 80:10734–10742. https://doi.org/10.1128/JVI.00349-06
Verbruggen B, Bickley LK, Van-Aerle R, Bateman KS, Stentiford KD, Santos EM, Tyler CR (2016) Molecular mechanisms of white spot syndrome virus infection and perspectives on treatments. Viruses 8:23. https://doi.org/10.3390/v8010023
Wang KC, Kondo H, Hirono I, Aoki T (2010) The Marsupenaeus japonicus voltage-dependent anion channel (MjVDAC) protein is involved in white spot syndrome virus (WSSV) pathogenesis. Fish Shellfish Immunol 29:94–103. https://doi.org/10.1016/j.fsi.2010.02.020
Xiang D, Chen Q, Pang L, Zheng C (2011) Inhibitory effects of silver nanoparticles on H1N1 influenza a virus in vitro. J Virol Methods 178:137–142. https://doi.org/10.1016/j.jviromet.2011.09.003
Zhang JY, Liu QH, Huang J (2014) Multiple proteins of white spot syndrome virus involved in recognition of β-integrin. J Biosci 39:381–388. https://doi.org/10.1007/s12038-014-9418-z
Zook JM, Maccuspie RI, Locascio LE, Halter MD, Elliott JT (2011) Stable nanoparticle aggregates/agglomerates of different sizes and the effect of their size on hemolytic cytotoxicity. Nanotoxicology 5:517–530. https://doi.org/10.3109/17435390.2010.536615
Acknowledgements
This study was supported by the National Council of Science and Technology (CONACyT), Project number 258607: “Estudio del efecto de nanopartículas de plata en virus, bacterias y parásitos de organismos acuáticos”. The authors wish to thank the University of Texas at San Antonio, USA (UTSA) for providing AgNPs. Special thanks to Valerie Williams Holland for the careful revision of the English.
Funding
All sources of funding for the research have been declared. Funding for this research was awarded to María Cristina Chávez-Sánchez by The National Council of Science and Technology (CONACyT) research (Grant number 258607), while the Department of Physics at the University of Texas (UTSA) in San Antonio, USA provided the silver nanoparticles.
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SMAR: Conceptualization; Data curation; Formal analysis; Investigation; Resources; Writing - original draft Writing - review & editing; visualization.RLO: Data curation; Formal analysis; Investigation; Resources; Writing - original draft; Writing - review & editing; visualizationBBVE: Methodology; Formal analysis; Data curation.MCCHS: Funding acquisition; Project administration; Resources; Writing - review & editing; Validation; Supervision.LMR: Methodology; Investigation; Resources; Validation; Writing - review & editing; Supervision.MAFN: Writing - review & editing.VJAL: Methodology; Writing - review & editing.MGFE: Writing - review & editing.LHH: Resources; Writing - review & editing.
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All procedures were performed according to Mexican guidelines and policies stated in the NOM-062-ZOO-1999 (these guidelines apply mostly to mammalian species but we applied the same principles regarding animal welfare and care) and British guidelines for fish welfare reported by Ashley (2007).
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Abad-Rosales, S.M., Lozano-Olvera, R., Vallin-Enríquez, B.B. et al. Interaction of Silver Nanoparticles with White spot Syndrome Virus and Their Histopathological Effects on Penaeus vannamei After Intramuscular Application. Thalassas 39, 687–696 (2023). https://doi.org/10.1007/s41208-023-00602-0
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DOI: https://doi.org/10.1007/s41208-023-00602-0