Potential aquaculture probiont Lactococcus lactis TW34 produces nisin Z and inhibits the fish pathogen Lactococcus garvieae

Archiv für Mikrobiologie - Tập 197 - Trang 449-458 - 2014
Cynthia Sequeiros1, Marisa E. Garcés1, Marisol Vallejo2, Emilio R. Marguet2, Nelda L. Olivera1
1Centro Nacional Patagónico (CENPAT-CONICET), Puerto Madryn, Argentina
2Cátedra de Biología Celular y Molecular, Facultad de Ciencias Naturales (FCN) Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB), Trelew, Argentina

Tóm tắt

Bacteriocin-producing Lactococcus lactis TW34 was isolated from marine fish. TW34 bacteriocin inhibited the growth of the fish pathogen Lactococcus garvieae at 5 AU/ml (minimum inhibitory concentration), whereas the minimum bactericidal concentration was 10 AU/ml. Addition of TW34 bacteriocin to L. garvieae cultures resulted in a decrease of six orders of magnitude of viable cells counts demonstrating a bactericidal mode of action. The direct detection of the bacteriocin activity by Tricine-SDS-PAGE showed an active peptide with a molecular mass ca. 4.5 kDa. The analysis by MALDI-TOF-MS detected a strong signal at m/z 2,351.2 that corresponded to the nisin leader peptide mass without the initiating methionine, whose sequence STKDFNLDLVSVSKKDSGASPR was confirmed by MS/MS. Sequence analysis of nisin structural gene confirmed that L. lactis TW34 was a nisin Z producer. This nisin Z-producing strain with probiotic properties might be considered as an alternative in the prevention of lactococcosis, a global disease in aquaculture systems.

Tài liệu tham khảo

Abee T, Krockel L, Hill C (1995) Bacteriocins: modes of action and potentials in food preservation and control of food poisoning. Int J Food Microbiol 28:169–185 Aguado-Urda M, López-Campos GH, Gibello A, Cutuli MT, López-Alonso V, Fernández-Garayzábal JF, Blanco MM (2011) Genome sequence of Lactococcus garvieae 8831, isolated from rainbow trout lactococcosis outbreaks in Spain. J Bacteriol 193:4263–4264 Altschul SF, Gish W, Miller M, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410 Andrews JM (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48:5–16 Avella MA, Place A, Du SJ, Williams E, Silvi S, Zohar Y, Carnevali O (2012) Lactobacillus rhamnosus accelerates zebrafish backbone calcification and gonadal differentiation through effects on the GnRH and IGF systems. PLoS One 7:e45572 Balcázar JL, de Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Múzquiz JL (2006) The role of probiotics in aquaculture. Vet Microbiol 114:173–186 Balcázar JL, de Blas I, Ruiz-Zarzuela I, Vendrell D, Gironés O, Muzquiz JL (2007a) Sequencing of variable regions of the 16S rRNA gene for identification of lactic acid bacteria isolated from the intestinal microbiota of healthy salmonids. Comp Immunol Microbiol 30:111–118 Balcázar JL, Vendrell D, de Blas I, Ruiz-Zarzuela I, Gironés O, Múzquiz JL (2007b) In vitro competitive adhesion and production of antagonistic compounds by lactic acid bacteria against fish pathogens. Vet Microbiol 122:373–380 Balciunas EM, Castillo Martinez FA, Todorov SD, Franco BDGDM, Converti A, Oliveira RPDS (2013) Novel biotechnological applications of bacteriocins: a review. Food Control 32:134–142 Bhunia AK, Johnson MC, Ray B (1987) Direct detection of an antimicrobial peptide of Pediococcus acidilactici in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J Ind Microbiol 2:319–322 Breukink E, van Kraaij C, Demel RA, Siezen RJ, Kuipers OP, de Kruijff B (1997) The C-terminal region of nisin is responsible for the initial interaction of nisin with the target membrane. Biochemistry 36:6968–6976 Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8:1137–1144 Carnevali O, Zamponi MC, Sulpizio R, Rollo A, Nardi M, Orpianesi C, Silvi S, Caggiano M, Polzonetti AM, Cresci A (2004) Administration of probiotic strain to improve sea bream wellness during development. Aquac Int 12:377–386 Chan JFW, Woo PCY, Teng JLL, Lau SKP, Leung SSM, Tam FCC, Yuen KY (2011) Primary infective spondylodiscitis caused by Lactococcus garvieae and a review of human L. garvieae infections. Infection 39:259–264 Chatterjee C, Patton GC, Cooper L, Paul M, van der Donk WA (2006) Engineering dehydro amino acids and thioethers into peptides using lacticin 481 synthetase. Chem Biol 13:1109–1117 Chu W, Lu F, Zhu W, Kang C (2011) Isolation and characterization of new potential probiotic bacteria based on quorum-sensing system. J Appl Microbiol 110:202–208 Cleveland J, Montville TJ, Nes IF, Chikindas ML (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71:1–20 de Vuyst L, Vandamme E (1994) Nisin, a lantibiotic produced by Lactococcus lactis subsp. lactis: properties, biosynthesis, fermentation and applications. In: de Vuyst L, Vandamme E (eds) Bacteriocins of lactic acid bacteria. Microbiology, genetics and applications. Chapman & Hall, London, pp 151–221 Defoirdt T, Boon N, Bossier P, Verstraete W (2004) Disruption of bacterial quorum sensing: an unexplored strategy to fight infections in aquaculture. Aquaculture 240:69–88 Defoirdt T, Sorgeloos P, Bossier P (2011) Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr Opin Microbiol 14:251–258 Desriac F, Defer D, Bourgougnon N, Brillet B, Le Chevalier P, Fleury Y (2010) Bacteriocin as weapons in the marine animal-associated bacteria warfare: inventory and potential applications as an aquaculture probiotic. Mar drugs 8:1153–1177 Dimitroglou A, Merrifield DL, Carnevali O, Picchietti S, Avella M, Daniels C, Güroy D, Davies SJ (2011) Microbial manipulations to improve fish health and production—a Mediterranean perspective. Fish Shellfish Immun 30:1–16 Eyngor M, Zlotkin A, Ghittino C, Prearo M, Douet DG, Chilmonczyk S, Eldar A (2004) Clonality and diversity of the fish pathogen Lactococcus garvieae in Mediterranean countries. Appl Environ Microb 70:5132–5137 Ferguson RMW, Merrifield DL, Harper GM, Rawling MD, Mustafa S, Picchietti S et al (2010) The effect of Pediococcus acidilactici on the gut microbiota and immune status of on growing red tilapia (Oreochromis niloticus). J Appl Microbiol 109:851–862 Gatesoupe FJ (2008) Updating the importance of lactic acid bacteria in fish farming: natural occurrence and probiotic treatments. J Mol Microbiol Biotechnol 14:107–114 Gillor O, Etzion A, Riley MA (2008) The dual role of bacteriocins as anti-and probiotics. App Microbiol Biot 81:591–606 Heo WS, Kim EY, Kim YR, Hossain MT, Kong IS (2012) Salt effect of nisin Z isolated from a marine fish on the growth inhibition of Streptococcus iniae, a pathogen of streptococcosis. Biotechnol Lett 34:315–320 Irianto A, Austin B (2002) Probiotics in aquaculture. J Fish Dis 25:633–642 Ivanova I, Kabadjova P, Pantev A, Danova S, Dousset X (2000) Detection, purification, and partial characterization of a novel bacteriocin substance produced by Lactococcus lactis subsp. lactis B14 isolated from boza-Bulgarian traditional cereal beverage. Biocatal—Vest Moskov Univ Kimia 41:47–53 Kuipers A (2010) Microbial production of thioether-stabilized peptides. Dissertation, University of Groningen, NL http://dissertations.ub.rug.nl/faculties/science/2010/a.kuipers/. Accessed 25 March 2014 Lin YH, Chen YS, Wu HC, Pan SF, Yu B, Chiang CM, Chiu CM, Yanagida F (2013) Screening and characterization of LAB produced bacteriocin like substances from the intestine of grey mullet (Mugil cephalus L.) as potential biocontrol agents in aquaculture. J Appl Microbiol 114:299–307 Lubelski J, Rink R, Khusainov R, Moll GN, Kuipers OP (2008) Biosynthesis, immunity, regulation, mode of action and engineering of the model lantibiotic nisin. Cell Mol Life Sci 65:455–476 Martínez MI, Rodríguez E, Medina M, Hernández PE, Rodríguez JM (1998) Detection of specific bacteriocin-producing producing lactic acid bacteria by colony hybridization. J Appl Microbiol 84:1099–1103 Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker R, Bøgwald J, Castex M, Ringø E (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302:1–18 Moll GN, Konings WN, Driessen AJ (1999) Bacteriocins: mechanism of membrane insertion and pore formation. Antonie van Leeuwenhoek 76:185–198 Nhan DT, Cam DTV, Wille M, Defoirdt T, Bossier P, Sorgeloos P (2010) Quorum quenching bacteria protect Macrobrachium rosenbergii larvae from Vibrio harveyi infection. J Appl Microbiol 109:1007–1016 Pardo MF, Natalucci CL (2002) Electrophoretic analysis (Tricine SDS-PAGE) of bovine caseins. Acta Farm Bonaer 21:57–60 Pérez T, Balcázar JL, Ruiz-Zarzuela I, Halaihel N, Vendrell D, de Blas I, Múzquiz JL (2010) Host-microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol 3:355–360 Pérez-Sánchez T, Balcázar JL, Merrifield DL, Carnevali O, Gioacchini G, de Blas I, Ruiz-Zarzuela I (2011a) Expression of immune–related genes in rainbow trout (Oncorhynchus mykiss) induced by probiotic bacteria during Lactococcus garvieae infection. Fish Shellfish Immun 31:196–201 Pérez-Sánchez T, Balcázar JL, García Y, Halaihel N, Vendrell D, De Blas I, Merrifield DL, Ruiz-Zarzuela I (2011b) Identification and characterization of lactic acid bacteria isolated from rainbow trout, Oncorhynchus mykiss (Walbaum), with inhibitory activity against Lactococcus garvieae. J Fish Dis 34:499–507 Pérez-Sánchez T, Ruiz-Zarzuela I, Blas I, Balcázar JL (2014) Probiotics in aquaculture: a current assessment. Rev Aquac 6:133–146 Pinto AL, Fernandes M, Pinto C, Albano H, Castilho F, Teixeira P, Gibbs PA (2009) Characterization of anti- Listeria bacteriocins isolated from shellfish: potential antimicrobials to control non-fermented seafood. Int J Food Microbiol 129:50–58 Reimundo P, Pignatelli M, Alcaraz LD, D’Auria G, Moya A, Guijarro JA (2011) Genome sequence of Lactococcus garvieae UNIUD074, isolated in Italy from a lactococcosis outbreak. J Bacteriol 193:3684–3685 Rodriguez JM, Cintas LM, Casaus P, Horn N, Dodd HM, Hernández PE, Gasson MJ (1995) Isolation of nisin-producing Lactococcus lactis strains from dry fermented sausages. J Appl Bacteriol 78:109–115 Rodriguez E, González B, Gaya P, Nuñez M, Medina M (2000) Diversity of bacteriocins produced by lactic acid bacteria isolated from raw milk. Int Dairy J 10:7–15 Romero J, Feijoó CG, Navarrete P (2012) Antibiotics in aquaculture–use, abuse and alternatives. In: Carvalho E (ed) Health and environment in aquaculture, Rijeka, pp 159–198 Salminen S, von Wright A, Morelli L, Marteau P, Brassart D, de Vos WM, Fondén R, Saxelin M, Collins K, Mogensen G, Birkeland SE, Mattila-Sandholm T (1998) Demonstration of safety of probiotics–a review. Int J Food Microbiol 44:93–106 Sequeiros C, Vallejo M, Marguet ER, Olivera NL (2010) Inhibitory activity against the fish pathogen Lactococcus garvieae produced by Lactococcus lactis TW34, a lactic acid bacterium isolated from the intestinal tract of a Patagonian fish. Arch Microbiol 192:237–245 van den Berg, van Saparoea HB, Bakkes PJ, Moll GN, Driessen AJ (2008) Distinct contributions of the nisin biosynthesis enzymes NisB and NisC and transporter NisT to prenisin production by Lactococcus lactis. Appl Environ Microb 74:5541–5548 van der Meer JR, Rollema HS, Siezen RJ, Beerthuyzen MM, Kuipers OP, De Vos WM (1994) Influence of amino acid substitutions in the nisin leader peptide on biosynthesis and secretion of nisin by Lactococcus lactis. J Biol Chem 269:3555–3562 Vela AI, Vázquez J, Gibello A, Blanco MM, Moreno MA, Liébana P, Albendea C, Alcalá B, Mendez A, Domínguez L, Fernández-Garayzábal JF (2000) Phenotypic and genetic characterization of Lactococcus garvieae isolated in Spain from lactococcosis outbreaks and comparison with isolates of other Countries and sources. J Clin Microbiol 38:3791–3795 Vendrell D, Balcázar JL, Ruiz-Zarzuela I, de Blas I, Gironés O, Múzquiz JL (2006) Lactococcus garvieae in fish: a review. Comp Immunol Microbiol 29:177–198 Vendrell D, Balcázar JL, de Blas I, Ruiz-Zarzuela I, Gironés O, Múzquiz JL (2008) Protection of rainbow trout (Oncorhynchus mykiss) from lactococcosis by probiotic bacteria. Comp Immunol Microb 31:337–345 Verschuere L, Rombaut G, Sorgeloos P, Veratraete W (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 64:655–671 Yang R, Johnson MC, Ray B (1992) Novel method to extract large amounts of bacteriocins from lactic acid bacteria. App Environ Microbiol 58:3355–3359