In vitro and in vivo inhibition of Vibrio spp. isolated from the shrimp Litopenaeus vannamei using native lactic acid bacteria

Published 2023-06-15
Keywords
- shrimp culture,
- vibriosis,
- bacterial resistance,
- probiotic,
- alternative to antibiotics
How to Cite
Copyright (c) 2023 Vicsy Yanet Tinoco Elizalde, Tessy Peralta-Ortiz, Alberto Ordinola-Zapata

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Abstract
The diseases caused by Vibrio spp. cause the greatest economic losses in shrimp farming, antibiotic therapy has led to the emergence of resistant strains and research is being carried out into the use of probiotics for their treatment. This research aimed to obtain native lactic acid bacteria (LAB) isolated from cultured shrimp and to determine their probiotic potential against antibiotic
resistant Vibrio spp in vitro and in vivo. Nine strains of both LAB and Vibrio spp. were isolated from cultured shrimps from Tumbes. Antibiotic–resistance of Vibrio spp. was determined; as well as the in vitro inhibitory power of LAB strains against these strains by agar well trial and in vivo, by experimental infection of shrimp with Vibrio spp. strains and treatment for eight days with LAB strains added
to feed. The nine strains of Vibrio spp. isolated from cultured shrimps were resistant to fosfomycin and nalidixic acid, with a multiple antibiotic resistance index (MAR) of 0.2. In the in vitro trial, the C1L, F1L and F3L strains inhibited the largest number of Vibrio spp. strains; also in vivo, the C1L and F1L strains significantly (p < 0.05) increased survival and decreased the Vibrio spp. count of infected
shrimp in the hepatopancreas. It is concluded that antibiotic- resistant strains of Vibrio spp. isolated from cultured shrimps could be inhibited by native LAB strains, C1L and F1L, demonstrating a promising probiotic potential.
Downloads
References
- Aguirre, L.E. 2019. Efecto del neem (Azadirachta indica) y orégano (Origanum vulgare) en el crecimiento de Vibrio spp. resistentes a antibióticos, aislados de Litopenaeus vannamei. Tesis Ing. Pesq., Univ. Nacional de Tumbes, Tumbes. 62 p.
- Albuquerque, R., R.L. Araújo, O.V. Souza and R.H.S. Vieira. 2015. Antibiotic-resistant vibrios in farmed shrimp. Biomed. Res. Int., 2015:1–5. https://doi.org/10.1155/2015/505914
- Aranguren, L.F., H.N. Mai, B. Noble and A.K. Dhar. 2020. Acute hepatopancreatic necrosis disease (VPAHPND), a chronic disease in shrimp (Penaeus vannamei) population raised in Latin America. J. Invertebr. Pathol., 174:107424. https://doi.org/10.1016/j.jip.2020.107424
- Banerjee, S., M.C. Ooi, M. Shariff and H. Khatoon. 2012. Antibiotic resistant Salmonella and Vibrio associated with farmed Litopenaeus vannamei. Sci.World. J., 2012:1–6. https://doi.org/10.1100/2012/130136
- Bermúdez-Almada, M.D.C., A. Espinosa-Plascencia, M.L. Santiago-Hernández, C.J. Barajas-Borgo y E. Acedo-Félix. 2014. Comportamiento de oxitetraciclina en camarón de cultivo Litopenaeus vannamei y la sensibilidad a tres antibióticos de bacterias de Vibrio aisladas de los organismos. Biotecnia, 16(3):29. https://biotecnia.unison.mx/index.php/biotecnia/article/view/138
- Bleichenbacher, S., M.J.A. Stevens, K. Zurfluh, V. Perreten, A. Endimiani, R. Stephan and M. Nüesch-Inderbinen. 2020. Environmental dissemination of carbapenemase-producing Enterobacteriaceae in rivers in Switzerland. Environ. Pollut., 265: 115081. https://doi.org/10.1016/j.envpol.2020.115081
- Cayul, A.A. 2003. Estudio de resistencia a antimicrobianos de uso frecuente en medicina veterinaria, de patógenos bacterianos aislados de metritis bovina en rebaños lecheros de la décima región. Tesis Med. Vet., Universidad Austral de Chile, Valdivia. 95 p.
- Chandrakala, N. and S. Priya. 2017. Vibriosis in shrimp aquaculture a review. Int. J. Sci. Eng., 3(2):27–33.
- Churqui, J.M. 2020. Bacterias ácido lácticas aisladas con capacidad antagónica de cepas de Escherichia coli y Staphylococcus aureus de quesos frescos expendidos en tres mercados de la ciudad de Puno-2017. Tesis Biol., Universidad Nacional del Altiplano, Puno. 58 p.
- CLSI. 2019. Performance standards for antimicrobial susceptibility testing. CLSI Supplement M100. 29th ed. CLSI, Wayne. 282 p.
- Culot, A., N. Grosset, Q. Bruey, M. Auzou, J.-C. Giard, B. Favard, A. Wakatsuki, S. Baron, S. Frouel, C. Techer and M. Gautier. 2021. Isolation of Harveyi clade Vibrio spp. collected in aquaculture farms: How can the identification issue be addressed?. J. Microbiol. Meth., 180:106106. https://doi.org/10.1016/j.mimet.2020.106106
- de Souza, C. and A.H.L. Wan. 2021. Vibrio and major commercially important vibriosis diseases in decapod crustaceans. J. Invertebr. Pathol., 181: 107527.https://doi.org/10.1016/j.jip.2020.107527
- Devi, R., P.K. Surendran and K. Chakraborty. 2009. Antibiotic resistance and plasmid profiling of Vibrio parahaemolyticus isolated from shrimp farms along the southwest coast of India. World J. Microbiol. Biotechnol., 25(11):2005–2012. https://doi.org/10.1007/s11274-009-0101-8
- Dutta, D., A. Kaushik, D. Kumar and S. Bag. 2021. Foodborne pathogenic vibrios: Antimicrobial resistance. Front. Microbiol., 12: 638331. https://doi.org/10.3389/fmicb.2021.638331
- Esguerra, D.A. 2012. Evaluación en un sistema cerrado de cuatro aislados bacterianos con potencial probiótico en la dieta de tilapia Oreochromis niloticus. Tesis Biol. Mar., Univ. Jorge Tadeo Lozano, Santa Marta. 48 p.
- FAO. 2020. The state of world fisheries and aquaculture 2020. FAO, Rome. 224 p.
- Gómez-Gil, B., A. Roque y S. Soto-Rodríguez. 2015. Vibriosis en camarones y su diagnóstico: 137–150. En: Ruiz-Luna, A., C.A. Berlanga-Robles y M. Betancourt (Eds.). Avances en acuicultura y manejo ambiental. Trillas: CIAD, Hermosillo. 150 p.
- Huynh, T.-G., C.-C. Chi, T.-P. Nguyen, T.-T.-T.H. Tran, A.-C. Cheng and C.-H. Liu. 2018. Effects of synbiotic containing Lactobacillus plantarum 7-40 and galactooligosaccharide on the growth performance of white shrimp, Litopenaeus vannamei. Aquac. Res., 49(7):2416–2428. https://doi.org/10.1111/are.13701
- Huynh, T.-G., S.-Y. Hu,, C.-S. Chiu, Q.-P. Truong and C.-H. Liu. 2019. Bacterial population in intestines of white shrimp, Litopenaeus vannamei fed a synbiotic containing Lactobacillus plantarum and galactooligosaccharide. Aquac. Res., 50(3):807–817. https://doi.org/10.1111/are.13951
- Jeyasanta, K.I., T. Lilly and J. Patterson. 2017. Prevalence of Vibrio species in the cultured shrimp and their antibiotic resistants. Asian J. Appl. Sci., 1(8):100–111.
- Karthik, R., A.J. Hussain and R. Muthezhilan. 2014. Effectiveness of Lactobacillus sp (AMET1506) as probiotic against vibriosis in Penaeus monodon and Litopenaeus vannamei shrimp aquaculture. Biosci. Biotechnol. Res. Asia, 11(SE):297–305. https://doi.org/10.13005/bbra/1423
- Kewcharoen, W. and P. Srisapoome. 2019. Probiotic effects of Bacillus spp. from Pacific white shrimp (Litopenaeus vannamei) on water quality and shrimp growth, immune responses, and resistance to Vibrio parahaemolyticus (AHPND strains). Fish Shellfish Immunol., 94: 175–189. https://doi.org/10.1016/j.fsi.2019.09.013
- Khelissa, S., N.-E. Chihib and A. Gharsallaoui. 2020. Conditions of nisin production by Lactococcus lactis subsp. lactis and its main uses as a food preservative. Arch. Microbiol., 203(2):465-480. https://doi.org/10.1007/s00203-020-02054-z Marine and Coastal Research Institute 25
- Krishnani, K.K., V. Kathiravan, N.A. Shakil, M.K. Singh, M.P. Brahmane, K.K. Meena, B. Sarkar, K. Choudhary, M.K. Singh and J. Kumar. 2015. Bactericidal activity of nanopolymers against shrimp pathogenic bacterium Vibrio harveyi. Proc. Natl. Acad. Sci. India Sect. B Biol. Sci., 85(4):1079–1086. https://doi.org/10.1007/s40011-015-0517-x
- Kumaran, M., P.R. Anand, J.A. Kumar, T. Ravisankar, J. Paul, K.P.K. Vasagam, D.D. Vimala and K.A. Raja. 2017. Is Pacific white shrimp (Penaeus vannamei) farming in India is technically efficient? — A comprehensive study. Aquaculture, 468: 262–270. https://doi.org/10.1016/j.aquaculture.2016.10.019
- Kurdi, M.M., S. Mutalib, M. Ghani, N.A.M. Zaini and A.A. Ariffin. 2019. Multiple antibiotic resistance (MAR), plasmid profiles, and DNA polymorphisms among Vibrio vulnificus isolates. Antibiotics, 8(2):68. https://doi.org/10.3390/antibiotics8020068
- Lamari, F., K. Sadok, A. Bakhrouf and F.-J. Gatesoupe.2014. Selection of lactic acid bacteria as candidate probiotics and in vivo test on Artemia nauplii. Aquac. Int., 22(2):699–709. https://doi.org/10.1007/s10499-013-9699-5
- Le, B. and S.H. Yang. 2018. Probiotic potential of novel Lactobacillus strains isolated from salted-fermented shrimp as antagonists for Vibrio parahaemolyticus. J. Microbiol., 56(2):138–144
- Letchumanan, V., N.-S. Ab Mutalib, S.H. Wong, K.-G. Chan and L.-H. Lee. 2019. Determination of antibiotic resistance patterns of Vibrio parahaemolyticus from shrimp and shellfish in Selangor, Malaysia. Prog. Microbes Mol. Biol., 2(1):a0000019.
- Luis-Villaseñor, I.E., D. Voltolina, B. Gomez-Gil, F. Ascencio, Á.I. Campa-Córdova, J.M. Audelo-Naranjo and O.O. Zamudio-Armenta. 2015. Probiotic modulation of the gut bacterial community of juvenile Litopenaeus vannamei challenged with Vibrio parahaemolyticus CAIM 170. Lat. Am. J. Aquat. Res., 43(4):766–775. https://doi.org/10.3856/vol43-issue4-fulltext-15
- Mahjoub, M., M. Mirbakhsh, M. Afsharnasab, S. Kakoolaki and S. Hosseinzadeh. 2019. Inhibitory activity of native probiotic Bacillus vallismortis IS03 against pathogenic Vibrio harveyi under in vitro and in vivo conditions in Litopenaeus vannamei. Iran. J. Aquat. Anim. Health, 5(2): 54–66. https://doi. org/10.29252/ijaah.5.2.54
- Mulyadi, N.I. and W. Iba. 2020. Efficacy of seaweed (Sargassum sp.) extract to prevent vibriosis in white shrimp (Litopenaeus vannamei) juvenile. Int. J. Zool. Res., 16(1):1–11. https://doi.org/10.3923/ijzr.2020.1.11
- NCCLS. 1999. Methods for dilution antimicrobial susceptibility test for bacteria that grow aerobically. Approved Standard. NCCLS Document M7-A3. 3rd Edition. NCCLS, Wayne. 282 p.
- Pandiyan, P., D. Balaraman, R. Thirunavukkarasu, E.G.J. George, K. Subaramaniyan, S. Manikkam and B. Sadayappan. 2013. Probiotics in aquaculture. Drug Invent. Today, 5(1):55–59. https://doi.org/10.1016/j.dit.2013.03.003
- Quispe, G.W., M.B. Mantilla, A. Cama., Y. Ortega y N. Sandoval. 2020. Aislamiento de bacterias nativas de Oncorhynchus mykiss con potencial probiótico frente a Yersinia ruckeri. Rev. Investig. Vet. Perú, 31(4):e19024. http://dx.doi.org/10.15381/rivep.v31i4.19024
- Rebouças, R.H., O.V. de Sousa, A. Sousa, F.R. Vasconcelos, P. Barroso and R.H. Silva. 2011. Antimicrobial resistance profile of Vibrio species isolated from marine shrimp farming environments (Litopenaeus vannamei) at Ceará, Brazil. Environ. Res., 111(1):21–24. https://doi.org/10.1016/j.envres.2010.09.012
- Rodríguez, A. 2017. Probióticos en la producción piscícola. Tesis Biotec. Agr., Univ. Nal. Abierta Distancia, Neiva, Colombia. 35 p.
- Rosado, A.A. 2018. Resistencia antimicrobiana de bacterias del género Vibrio en langostino blanco (Litopenaeus vannamei) en centros de cultivo de la región Tumbes. Tesis Med. Vet., Univ. Ricardo Palma, Lima. 91 p.
- RSPCA. 2016. Humane killing and processing of crustaceans for human consumption. RSPCA Australia, Victoria. 9 p.
- Saavedra-Olivos, K.Y., T. Peralta-Ortiz, A. Ordinola-Zapata, J.E. Sandoval-Ramayoni, E.G. Vieyra-Peña, M.A. Zapata-Cruz, A. Hidalgo-Mogollón, B. Morán, O. A. Mendoza-Neyra, M.E. Mendoza-Dioses y S.Y. Campoverde-Peña. 2018. Detección de una proteína asociada a la enfermedad de la necrosis hepatopancreática aguda (AHPND) en Litopenaeus vannamei bajo cultivo semi-intensivo en Ecuador. Rev. Investig. Vet. Perú, 29(1):328. https://doi.org/10.15381/rivep.v29i1.14194
- Sabir, M., M.M. Ennaji y N. Cohen. 2013. Vibrio alginolyticus: An emerging pathogen of foodborne diseases. Int. J. Sci. Technol., 2(4):302–309.
- Tan, C.W., Y. Rukayadi, H. Hasan T.Y. Thung, E. Lee, W.D. Rollon, H. Hara, A.Y. Kayal, M. Nishibuchi and S. Radu. 2020. Prevalence and antibiotic resistance patterns of Vibrio parahaemolyticus isolated from different types of seafood in Selangor, Malaysia. Saudi J. Biol. Sci., S1319562X20300036. https://doi.org/10.1016/j.sjbs.2020.01.002
- Uppal, B., B. Mehra, P.S. Panda and S.K. Kumar. 2017. Antimicrobial susceptibility profile of Vibrio cholerae strains isolated at a tertiary care medical centre in New Delhi, India. Int. J. Com. Med. Publ. Health, 4(3):868. https://doi.org/10.18203/2394-6040.ijcmph20170775
- Varela-Mejías, A. y R. Alfaro-Mora. 2018. Revisión sobre aspectos farmacológicos a considerar para el uso de antibióticos en la camaronicultura. Rev. Investig. Vet. Perú, 29(1):1–14. https://doi.org/10.15381/rivep.v29i1.14186
- Vieco-Saiz, N., Y. Belguesmia, R. Raspoet, E. Auclair, F. Gancel, I. Kempf and D. Drider. 2019. Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Front. Microbiol., 10:57. https://doi.org/10.3389/fmicb.2019.00057
- Watts, J., H. Schreier, L. Lanska and M. Hale. 2017. The rising tide of antimicrobial resistance in aquaculture: sources, sinks and solutions. Mar. Drugs, 15(6):158. https://doi.org/10.3390/md15060158
- Zhao, Y., X. Zhang, Z. Zhao, C. Duan, H. Chen, M. Wang, H. Ren, Y. Yin and L. Ye. 2018. Metagenomic analysis revealed the prevalence of antibiotic resistance genes in the gut and living environment of freshwater shrimp. J. Hazard Mater., 350: 10–18. https://doi.org/10.1016/j.jhazmat.2018.02.004
- Zhao, Y., Q.E. Yang, X. Zhou, F.-H. Wang, J. Muurinen, M.P. Virta, K.K. Brandt and Y.-G. Zhu. 2020. Antibiotic resistome in the livestock and aquaculture industries: Status and solutions. Crit. Rev. Environ. Sci. Technol., 2020: 1–38. https://doi.org/10.1080/10643389.2020.1777815