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Complementary Antibacterial Effects of Bacteriocins and Organic Acids as Revealed by Comparative Analysis of Carnobacterium spp. from Meat

The results of this study demonstrated that both bacteriocins and organic acids are important factors contributing to the antibacterial activities of Carnobacterium from vacuum-packaged (VP) meats. This study demonstrated that formate and acetate are the key organic acids produced by Carnobacterium and demonstrated their association with the inhibitory activity of carnobacteria under VP meat-relevant storage conditions. The role of lactate, on the other hand, may not be as important as previously believed in the antimicrobial activities of Carnobacterium spp. on chilled VP meats. These findings advance our understanding of the physiology of Carnobacterium spp. to better explore their biopreservative properties for chilled VP meats. ABSTRACT Carnobacterium maltaromaticum and Carnobacterium divergens are often predominant in the microbiota of vacuum-packaged (VP) meats after prolonged storage at chiller temperatures, and more so in recent studies. We investigated the antibacterial activities of C. maltaromaticum and C. divergens (n = 31) from VP meats by phenotypic characterization and genomic analysis. Five strains showed antibacterial activities against Gram-positive bacteria in a spot-lawn assay, with C. maltaromaticum strains having an intergeneric and C. divergens strains an intrageneric inhibition spectrum. This inhibitory activity is correlated with the production of predicted bacteriocins, including carnobacteriocin B2 and carnolysin for C. maltaromaticum and divergicin A for C. divergens. The supernatants of both species cultured in meat juice medium under anaerobic conditions retarded the growth of most Gram-positive and Gram-negative bacteria in broth assay in a strain-dependent manner. C. maltaromaticum and C. divergens produced formate and acetate but not lactate under VP meat-relevant conditions. The relative inhibitory activity by Carnobacterium strains was significantly correlated (P < 0.05) to the production of both acids. Genomic analysis revealed the presence of genes required for respiration in both species. In addition, two clusters of C. divergens have an average nucleotide identity below the cutoff value for species delineation and thus should be considered to be two subspecies. In conclusion, both bacteriocins and organic acids are factors contributing significantly to the antibacterial activity of C. maltaromaticum and C. divergens under VP meat-relevant conditions. A few Carnobacterium strains can be explored as protective cultures to extend the shelf life and improve the safety of VP meats. IMPORTANCE The results of this study demonstrated that both bacteriocins and organic acids are important factors contributing to the antibacterial activities of Carnobacterium from vacuum-packaged (VP) meats. This study demonstrated that formate and acetate are the key organic acids produced by Carnobacterium and demonstrated their association with the inhibitory activity of carnobacteria under VP meat-relevant storage conditions. The role of lactate, on the other hand, may not be as important as previously believed in the antimicrobial activities of Carnobacterium spp. on chilled VP meats. These findings advance our understanding of the physiology of Carnobacterium spp. to better explore their biopreservative properties for chilled VP meats.