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Silver nanoparticles against acute hepatopancreatic necrosis disease (AHPND) in shrimp and their depuration kinetics

  • 23rd INTERNATIONAL SEAWEED SYMPOSIUM, JEJU
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Abstract

Ag-based nanoparticles (NPs) were successfully produced through green synthesis using an aqueous extract from the cultivated seaweed Ulva clathrata as the reducing and stabilizing agent. The biosynthesized NPs had spherical to polymorphic shapes with an average size of 9.5 nm. Microstructural and compositional studies revealed that these particles contained face-centred cubic crystallites of metallic Ag and AgCl. Characteristic peaks in the Fourier-transform infrared spectrum (FTIR) and Raman studies revealed the presence of functional bioactive metabolites from the seaweed extract, such as proteins, polysaccharides, and polyphenols, which are responsible for forming and stabilizing Ag/AgCl NPs. The biosynthesized Ag/AgCl NPs exhibited an important in vitro antibacterial effect against three Vibrio parahaemolyticus strains isolated from farmed shrimp affected with acute hepatopancreatic necrosis disease (AHPND) in northwestern Mexico. Litopenaeus vannamei shrimp were exposed for 7 days to feeds supplemented with Ag/AgCl NPs at 10, 100, 1000, or 10,000 ppm (Ag nominal dietary concentrations). Dietary NP supplement did not affect shrimp survival, growth, or feed conversion ratio, but high concentrations (1000 and 10,000 ppm) decreased the hepatosomatic index significantly. The short-term consumption of Ag/AgCl NPs produced a significant dose-dependent bioaccumulation of Ag in the hepatopancreas and to a lesser extent in the cuticle, while bioaccumulation in the muscle was not significant. The depuration study confirmed a fast Ag assimilation in shrimp’s hepatopancreas and showed a fast depuration rate in the hepatopancreas as well.

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References

  • Abdel-Raouf N, Al-Enazi NM, Ibraheem IBM (2017) Green biosynthesis of gold nanoparticles using Galaxaura elongata and characterization of their antibacterial activity. Arab J Chem 10:S3029–S3039

    CAS  Google Scholar 

  • Abirami RG, Kowsalya S (2015) Ulva fasciata nanoparticles characterization and its anticancer activity. World J Pharm Pharm Sci 4:1164–1175

    CAS  Google Scholar 

  • Aguirre-Guzmán G, Ruíz HM, Ascencio F (2004) A review of extracellular virulence product of Vibrio species important in diseases of cultivated shrimp. Aquac Res 35:1395–1404

    Google Scholar 

  • AOAC (ed) (1997) Official Method of Analysis, 16th edn. AOAC International, Gaithersburg

    Google Scholar 

  • Biswas N, Kapoor S, Mahal HS, Mukherjee T (2007) Adsorption of CGA on colloidal silver particles: DFT and SERS study. Chem Phys Lett 444:338–345

    CAS  Google Scholar 

  • Carvalho RA, Benfield MC, Santschi PH (1999) Comparative bioaccumulation studies of colloidally complexed and free-ionic heavy metals in juvenile brown shrimp Penaeus aztecus (Crustacea: Decapoda: Penaeidae). Limnol Oceanogr 44:403–414

    CAS  Google Scholar 

  • Choi O, Deng KK, Kim NJ, Ross L Jr, Surampallie RY, Hu Z (2008) The inhibitory effects of silver nanoparticles, silver ions, and silver chloride colloids on microbial growth. Water Res 42:3066–3074

    CAS  PubMed  Google Scholar 

  • Conapesca (2017) Anuario estadístico de acuacultura y pesca. Comisión Nacional de Acuacultura y Pesca, Mazatlan, Sinaloa, Mexico. pp 28 https://www.conapesca.gob.mx/work/sites/cona/dgppe/2017/ANUARIO_ESTADISTICO_2017.pdf. Access 26 Oct 2019

  • Connolly M, Fernández M, Conde E, Torrent F, Navas JM, Fernandez-Cruz ML (2016) Tissue distribution of zinc and subtle oxidative stress effects after dietary administration of ZnO nanoparticles to rainbow trout. Sci Total Environ 551–552:334–343

    PubMed  Google Scholar 

  • Cruz-Suarez LE, Tapia-Salazar M, Nieto-Lopez MG, Guajardo-Barbosa C, Ricque-Marie D (2009) Comparison of Ulva clathrata and the kelps Macrocystis pyrifera and Ascophyllum nodosum as ingredients in shrimp feeds. Aquac Nutr 15:421–430

    CAS  Google Scholar 

  • Cruz-Suarez LE, León A, Peña-Rodríguez A, Rodríguez-Peña G, Moll B, Ricque-Marie D (2010) Shrimp/Ulva Co-Culture: A sustainable alternative to diminish the need for artificial feed and improve shrimp quality. Aquaculture 301:64–68

  • Cruz-Suarez LE, Nieto-Lopez M, Tapia-Salazar M, Maldonado-Muñiz M, Villarreal-Cavazos D, Ricque-Marie D (2013) Avances en la valoración de macroalgas del género Ulva como nutracéutico en Litopenaeus vannamei. In: Cruz-Suárez LE, Ricque-Marie D, Tapia-Salazar M, Nieto-Lopez MG, Villarreal-Cavazos DA, Gamboa-delgado J, Alvarez-Gonzalez C (eds) Contribuciones recientes en alimentacion acuicola. Universidad Autonoma de Nuevo León, San Nicolas de los Garza, pp 553–598 https://www.uanl.mx/utilerias/nutricion_acuicola/xii/LibroCRANA-ISBN.pdf. Access 08 July 2018

  • Defoirdt T, Sorgeloos P, Bossier P (2011) Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr Opin Microbiol 14:251–258

    PubMed  Google Scholar 

  • Dehnavi AS, Raisi A, Aroujalian A (2013) Control size and stability of colloidal silver nanoparticles with antibacterial activity prepared by a green synthesis method. Synth React Inorganic Met Nano-Metal Chem 43:543–551

    CAS  Google Scholar 

  • Devi JS, Bhimba BV (2012) Anticancer activity of silver nanoparticles synthesized by the seaweed Ulva lactuca In vitro. J Nanomedine Biotherapeutic Discov 1:1–5

    Google Scholar 

  • Dhas TS, Kumar VG, Karthick V, Jini AK, Govindaraju K (2014) Facile synthesis of silver chloride nanoparticles using marine alga and its antibacterial efficacy. Spectrochim Acta A 120:416–420

    Google Scholar 

  • El-Kassas EK, El-Kassas H, E-K MM (2014) Biogenic silver nanoparticles using seaweed Ulva rigida and their fungicidal and cytotoxic effects. JKAU Mar Sci 25:3–20

    Google Scholar 

  • Ibañez E, Herrero M, Mendiola JA, Castro-Puyana M (2012) Extraction and characterization of bioactive compounds with health benefits from marine resources: Macro and micro algae, cyanobacteria, and invertebrates. In: Hayes M (ed) Marine Bioactive Compounds: Sources, Characterization and Applications. Springer US, Boston, pp 55–98

    Google Scholar 

  • Joshi J, Srisala J, Truong VH, Chen I-T, Nuangsaeng B, Suthienkul O, Lo CF, Flegel TW, Sritunyalucksana K, Thitamadee S (2014) Variation in Vibrio parahaemolyticus isolates from a single Thai shrimp farm experiencing an outbreak of acute hepatopancreatic necrosis disease (AHPND). Aquaculture 428:297–302

    Google Scholar 

  • Kandasamy K, Alikunhi NM, Manickaswami G, Nabikhan A, Ayyavu G (2012) Synthesis of silver nanoparticles by coastal plant Prosopis chilensis (L.) and their efficacy in controlling vibriosis in shrimp Penaeus monodon. Appl Nanosci 3:65–73

    Google Scholar 

  • Kannan RRR, Arumugam R, Ramya D, Manivannan K, Anantharaman P (2013a) Green synthesis of silver nanoparticles using marine macroalga Chaetomorpha linum. Appl Nanosci 3:229–233

    CAS  Google Scholar 

  • Kannan RRR, Stirk WA, Van Staden J (2013b) Synthesis of silver nanoparticles using the seaweed Codium capitatum P.C. Silva (Chlorophyceae). S Afr J Bot 86:1–4

  • Kora AJ, Sashidhar RB, Arunachalam J (2012) Aqueous extract of gum olibanum (Boswellia serrata): A reductant and stabilizer for the biosynthesis of antibacterial silver nanoparticles. Process Biochem 47:1516–1520

    CAS  Google Scholar 

  • Kumar P, Selvi SS, Prabha AL, Kumar KP, Ganeshkumar RS, Govindaraju M (2012) Synthesis of silver nanoparticles from Sargassum tenerrimum and screening phytochemicals for its antibacterial activity. Nano Biomed Eng 4:12–16

    Google Scholar 

  • Laramore S, Baptiste R, Wills PS, Hanisak MD (2018) Utilization of IMTA-produced Ulva lactuca to supplement or partially replace pelleted diets in shrimp (Litopenaeus vannamei) reared in a clear water production system. J Appl Phycol 30:3603–3610

    CAS  Google Scholar 

  • Lee T-M, Liu C-H (1999) Correlation of decreased calcium contents with proline accumulation in the marine green macroalga Ulva fasciata exposed to elevated NaCl contents in seawater. J Exp Bot 50:1855–1862

    CAS  Google Scholar 

  • Liu J, He F, Gunn TM, Zhao D, Roberts CB (2009) Precise seed-mediated growth and size-controlled synthesis of palladium nanoparticles using a green chemistry approach. Langmuir 25:7116–7128

    CAS  PubMed  Google Scholar 

  • Luna C, Cruz-Suarez LE, Mendoza-Resendez R, Ricque-Marie D, Gonzalez-Dueñas C, Maldonado-Muñiz M (2015a) Instituto Mexicano de la Propiedad Intelectual (IMPI) Solicitud de Patente MX/a/2015/002621 https://siga.impi.gob.mx/newSIGA/content/common/principal.jsf. Access 26 Oct 2019

  • Luna C, Chávez VHG, Barriga-Castro ED, Nuñez N, Mendoza-Resendez R (2015b) Biosynthesis of silver fine particles and particles decorated with nanoparticles using the extract of Illicium verum (star anise) seeds. Spectrochim Acta A 141:43–50

    CAS  Google Scholar 

  • McLeod MC, Kitchens CL, Roberts CB (2005) CO2-expanded liquid deposition of ligand-stabilized nanoparticles as uniform, wide-area nanoparticle films. Langmuir 21:2414–2418

    CAS  PubMed  Google Scholar 

  • Mendoza-Reséndez R, Núñez NO, Barriga-Castro ED, Luna C (2013) Synthesis of metallic silver nanoparticles and silver organometallic nanodisks mediated by extracts of Capsicum annuum var. aviculare (piquin) fruits. RSC Adv 3:20765–20771

    Google Scholar 

  • Mendoza-Reséndez R, Gómez-Treviño A, Barriga-Castro ED, Nuñez N, Luna C (2014) Synthesis of antibacterial silver-based nanodisks and dendritic structures mediated by royal jelly. RSC Adv 4:1650–1658

    Google Scholar 

  • Metian M, Hédouin L, Eltayeb MM, Lacoue-Labarthe T, Teyssié JL, Mugnier C, Bustamante P, Warnau M (2010) Metal and metalloid bioaccumulation in the Pacific blue shrimp Litopenaeus stylirostris (Stimpson) from New Caledonia: Laboratory and field studies. Mar Pollut Bull 61:576–584

    CAS  PubMed  Google Scholar 

  • Monfared AL, Soltani S (2013) Effects of silver nanoparticles administration on the liver of rainbow trout ( Oncorhynchus mykiss ): histological and biochemical studies. Pelagia Res Libr 3:285–289

    CAS  Google Scholar 

  • Morales-Covarrubias MS, García-Aguilar N, Bolan-Mejía MDC, Puello-Cruz AC (2016) Evaluation of medicinal plants and colloidal silver efficiency against Vibrio parahaemolyticus infection in Litopenaeus vannamei cultured at low salinity. Dis Aquat Org 122:57–65

    CAS  PubMed  Google Scholar 

  • Mukherjee P, Roy M, Mandal BP, Dey GK, Mukherjee PK, Ghatak J, Tyagi AK, Kale SP (2008) Green synthesis of highly stabilized nanocrystalline silver particles by a non-pathogenic and agriculturally important fungus T. asperellum. Nanotechnology 19:1–7

    Google Scholar 

  • Nezamdoost T, Bagherieh-Najjar MB, Aghdasi M (2014) Biogenic synthesis of stable bioactive silver chloride nanoparticles using Onosma dichroantha Boiss. root extract. Mater Lett 137:225–228

    CAS  Google Scholar 

  • Nieto-López M, Tapia-Salazar M, Ricque-Marie D, Villarreal-Cavazos D, Lemme A, Cruz-Suarez LE (2011) Digestibility of different wheat products in white shrimp Litopenaeus vannamei juveniles. Aquaculture 319:369–376

    Google Scholar 

  • Novak JP, Nickerson C, Franzen S, Feldheim DL (2001) Purification of molecularly bridged metal nanoparticle arrays by centrifugation and size exclusion chromatography. Anal Chem 73:5758–5761

    CAS  PubMed  Google Scholar 

  • OECD (2005) OECD Detailed review paper on aquatic arthropods in life cycle and two-generation toxicity tests. OECD Environment Health and Safety Publications, OECD Publishing, Paris, http://www.oecd.org/chemicalsafety/testing/34241659.pdf. Accessed 15 Feb 2017

  • OECD (2012) Test No. 305: Bioaccumulation in Fish: Aqueous and Dietary Exposure, OECD Guidelines for the Testing of Chemicals, Section 3, OECD Publishing, Paris https://doi.org/10.1787/9789264185296-en

  • OIE (2014)Antimicrobial use in aquatic animals. In: Aquatic animal health code, Seventeent. World organisation for animal health, Paris, pp 109-117

  • Pal S, Tak YK, Song JM (2015) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli. J Biol Chem 290:1712–1720

    Google Scholar 

  • Peña-Rodríguez A, León A, Moll B, Tapia-Salazar M, Nieto-López MG, Villarreal-Cavazos D, Ricque-Marie D, Cruz-Suárez LE (2010) Uso de Ulva clathrata en la nutrición del camarón blanco: revisión. En: Cruz-Suarez LE, Ricque-Marie D, TapiaSalazar M, Nieto-López MG, Villarreal-Cavazos A, Gamboa-Delgado J (Eds), Avances en Nutrición Acuícola X - Memorias del X Simposio Internacional de Nutrición Acuícola, 8-10 de Noviembre, San Nicolás de los Garza, N. L., México.Universidad Autónoma de Nuevo León, Monterrey, México, pp 700–712

  • Peña-Rodríguez A, Mawhinney TP, Ricque-Marie D, Cruz-Suárez LE (2011) Chemical composition of cultivated seaweed Ulva clathrata (Roth) C. Agardh. Food Chem 129:491–498

    PubMed  Google Scholar 

  • Petrus EM, Tinakumari S, Chai LC, Ubong A, Tunung R, Elexson N, Chai LF, Son R (2011) A study on the minimum inhibitory concentration and minimum bactericidal concentration of nano colloidal silver on food-borne pathogens. Int Food Res J 18:55–66

    CAS  Google Scholar 

  • Prasad TNVKV, Kambala VSR, Naidu R (2013) Phyconanotechnology: synthesis of silver nanoparticles using brown marine algae Cystophora moniliformis and their characterisation. J Appl Phycol 25:177–182

    CAS  Google Scholar 

  • Rai M, Yadav A, Gade A (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv 27:76–83

    CAS  PubMed  Google Scholar 

  • Ramkumar VS, Pugazhendhi A, Gopalakrishnan K, Sivagurunathan P, Saratale GD, Dung TNB, Kannapiranf K (2017) Biofabrication and characterization of silver nanoparticles using aqueous extract of seaweed Enteromorpha compressa and its biomedical properties. Biotechnol Rep 14:1–7

    Google Scholar 

  • Rauwel P, Küünal S, Ferdov S, Rauwel E (2015) A review on the green synthesis of silver nanoparticles and their morphologies studied via TEM. Adv Mater Sci Eng 2015:1–9

    Google Scholar 

  • Rebecca LJ, Dhanalakshmi V, Sharmila S (2012) Effect of the extract of Ulva sp on pathogenic microorganisms. J Chem Pharm Res 4:4875–4878

    Google Scholar 

  • Saritha K, Mani AE, Priyalaxmi M, Patterson J (2013) Antibacterial activity and biochemical constituents of seaweed Ulva lactuca. Glob J Pharmacol 7:276–282

    CAS  Google Scholar 

  • Sarker SD, Nahar L, Kumarasamy Y (2007) Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 42:321–324

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shanmugam N, Rajkamal P, Cholan S, Kannadasan N, Sathishukumar K, Viruthagiri G, Sundaramanickam A (2014) Biosynthesis of silver nanoparticles from the marine seaweed Sargassum wightii and their antibacterial activity against some human pathogens. Appl Nanosci 4:881–888

    CAS  Google Scholar 

  • Sharma A, Sharma S, Sharma K, Chetri S, Vashishtha A, Singh P, Kumar R, Rathi B, Agrawa V (2016) Algae as crucial organisms in advancing nanotechnology: a systematic review. J Appl Phycol 28:1759–1774

    CAS  Google Scholar 

  • Singh CR, Kathiresan K, Anandhan S (2015) A review on marine based nanoparticles and their potential applications. Afr J Biotechnol 14:1525–1532

    CAS  Google Scholar 

  • Sirvakumar K, Kannappan S, Masilamani D, Prasanna KP (2014) Evaluation of marine macro alga, Ulva fasciata against bio-luminescent causing Vibrio harveyi during Penaeus monodon larviculture. Afr J Microbiol Res 8:803–813

    Google Scholar 

  • Sivaramasamy E, Zhiwei W (2016) Enhancement of vibriosis resistance in Litopenaeus vannamei by supplementation of biomastered silver nanoparticles by Bacillus subtilis. J Nanomed Nanotechnol 7:1–10

    Google Scholar 

  • Sivaramasamy E, Zagorsek K, Li F, Xiang J (2017) In situ synthesis of silver nanoparticles into TEMPO-mediated oxidized bacterial cellulose and their antivibriocidal activity against shrimp pathogens. Carbohydr Polym 166:329–337

    Google Scholar 

  • Soto-Rodriguez SA, Gomez-Gil B, Lozano-Olvera R, Betancourt-Lozano M, Morales-Covarrubias MS (2015) Field and experimental evidence of Vibrio parahaemolyticus as the causative agent of acute hepatopancreatic necrosis disease of cultured shrimp (Litopenaeus vannamei) in Northwestern Mexico. Appl Environ Microbiol 81:1689–1699

    PubMed  PubMed Central  Google Scholar 

  • Sun Y, Xia Y (2002) Shape-controlled synthesis of gold and silver nanoparticles. Science 298:2176–2179

    CAS  PubMed  Google Scholar 

  • Swain P, Sasmal A, Nayak SK, Barik S, Mishra SS, Mohapatra KD, Swain SK, Saha JN, Sen AK, Jayasankar P (2014) Evaluation of selected metal nanoparticles on hatching and survival of larvae and fry of Indian major carp, rohu ( Labeo rohita ). Aquac Res 47:498–511

    Google Scholar 

  • Venkatesan J, Kim S-K, Shim M (2016) Antimicrobial, antioxidant, and anticancer activities of biosynthesized silver nanoparticles using marine algae Ecklonia cava. Nanomaterials 6:1–18

    Google Scholar 

  • Vieira AP, Stein EM, Andreguetti DX, Colepicolo P, da Costa Ferreira AM (2016) Preparation of silver nanoparticles using aqueous extracts of the red algae Laurencia aldingensis and Laurenciella sp. and their cytotoxic activities. J Appl Phycol 28:2615–2622

    Google Scholar 

  • Vijayan SR, Santhiyagu P, Ramasamy R, Aravalagan P, Kumar G, Ethiraj K, Ramaswamy BR (2016) Seaweeds: A resource for marine bionanotechnology. Enzym Microb Technol 95:45–57

    CAS  Google Scholar 

  • Xie J, Lee JY, Wang DIC, Ting YP (2007) Identification of active biomolecules in the high-yield synthesis of single-crystalline gold nanoplates in algal solutions. Small 3:672–682

    CAS  PubMed  Google Scholar 

  • Yang YT, Chen IT, Lee CT, Chen CY, Lin SS, Hor LI, Tseng TC, Huang YT, Sritunyalucksana K, Thitamadee S, Wang HC, Lo CF (2014) Draft genome sequences of four strains of Vibrio parahaemolyticus, three of which cause Early Mortality Syndrome/Acute Hepatopancreatic Necrosis Disease in shrimp in China and Thailand. Genome Announc 2:e00816–e00814

    PubMed  PubMed Central  Google Scholar 

  • Yousefzadi M, Rahimi Z, Ghafori V (2014) The green synthesis , characterization and antimicrobial activities of silver nanoparticles synthesized from green alga Enteromorpha flexuosa (Wulfen). J Agardh Mater Lett 137:1–4

    CAS  Google Scholar 

  • Zhao G, Stevens SE (1998) Multiple parameters for the comprehensive evaluation of the susceptibility of Escherichia coli to the silver ion. BioMetals 11:27–32

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors sincerely thank the company FITMAR for their support with the organisms used during the experimental tests in this research project.

Author contributions statement

MM-M synthetized the particles, performed the experiments, analysed the results and wrote the manuscript. CL conceived the synthesis and characterization of particles. RM-R conceived the synthesis and characterization of particles. EDB-C performed the characterization studies. SS-R provided the bacterial strains and conceived the microbiological studies. DR-M performed statistical and mathematical analyses, and wrote the manuscript. LEC-S designed and conceived all the experiments and wrote the manuscript. All authors reviewed the manuscript.

Funding

This study was part of the project ‘Evaluación multidisciplinaria del potencial nutraceutico de macroalgas en camarones y murinos y su repercusión en el manejo de enfermedades bacterianas y metabólicas’, which received financial support from the Consejo Nacional de Ciencia y Tecnología (CONACyT) (Ciencia Basica #2014-238458).

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Maldonado-Muñiz, M., Luna, C., Mendoza-Reséndez, R. et al. Silver nanoparticles against acute hepatopancreatic necrosis disease (AHPND) in shrimp and their depuration kinetics. J Appl Phycol 32, 2431–2445 (2020). https://doi.org/10.1007/s10811-019-01948-w

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