Quantifying the bioprotective effect of Lactobacillus sakei CTC494 against Listeria monocytogenes on vacuum packaged hot-smoked sea bream
Introduction
Smoked fish products are sold as ready-to-eat (RTE) foods characterized by a relatively long refrigerated shelf-life when packaged under vacuum (Hwang, 2007). These seafood commodities are popular, but they are also considered among the top risk foodstuffs since they can be contaminated with foodborne pathogens and no cooking is applied before consumption (Ghanbari et al., 2013). At present, the microbiological concerns in the EU associated with extended shelf-life refrigerated RTE foods are focused on psychrotrophic foodborne pathogens such as Listeria monocytogenes (EFSA BIOHAZ, 2018).
Biopreservation, also called bioprotection, is a biocontrol approach to enhance product safety and shelf-life using microorganisms selected for their antimicrobial properties, so called protective cultures (Leroi et al., 2015). Lactic-acid bacteria (LAB) are considered a new generation of food additives and the basis of food biopreservation (Said et al., 2019). Protective cultures are considered by the regulatory agencies as ‘new’ food additives, meaning that they require market authorization for their technological use in foods. However, most LAB are Generally Recognized as Safe (GRAS) and many LAB species (including Lactobacillus sakei) have been granted by EFSA with the Qualified Presumption of Safety (QPS) status (EFSA (European Food Safety Authority), 2018). In the EU, microorganisms with the latter food-grade standard do not need to undergo a further safety assessment other than to provide evidence of efficacy and to satisfy the specified qualifications, if applicable, for its market approval. Two recent studies have proved that the antilisterial sakacin K-producing Lactobacillus sakei strain CTC494 (from meat origin) is effective to inhibit L. monocytogenes in filleted sea bream and cold-smoked salmon under refrigerated storage (Aymerich et al., 2019; Costa et al., 2019). Nevertheless, the inhibitory capacity of this bioprotective LAB strain has not been tested in other fish products where the differences in product's characteristics and formulations might either favor its inhibition thanks to the antimicrobial hurdle combinations (Leistner, 2000) or hinder the ability of the strain to inhibit L. monocytogenes (Tahiri et al., 2009; Vasilopoulos et al., 2010).
Quantifying microbial interaction in food can be highly complex and often overlooked in predictive microbiology studies (Powell et al., 2004). Most of the competitive growth models available in literature are based on two approaches: one based on the Jameson effect phenomenon (i.e. nutrient competition) (Jameson, 1962) and the other using the general Lotka-Volterra competition model (i.e. predator-prey model) (Powell et al., 2004; Valenti et al., 2013). Both mathematical models represent a simultaneous deceleration of bacterial populations. The inhibition of L. monocytogenes by endogenous LAB usually responsible for spoilage has been studied and modelled in minimally processed fish products (Mejlholm et al., 2015; Mejlholm and Dalgaard, 2015, 2007). In this regard, most of the published microbial interaction models aim at describing competition between background microbiota and microbial pathogens, rather than to characterize the performance of bioprotective bacteria with specific antagonistic activities, that are normally added at higher levels than the natural background (spoilage) microbiota (Cornu et al., 2011). To the best author's knowledge, studies having quantified the bioprotective effect of bacteriocin-producing LAB cultures through the development and implementation of predictive models are scarce. The first attempt to model the inhibitory effect of a bacteriocinogenic LAB strain against Listeria in fish was made by Costa et al. (2019), in which model parameters were derived from experiments in a fish-based broth and then validated on fresh filleted sea bream.
The objective of this study was (i) to evaluate the bioprotective potential of L. sakei CTC494 against L. monocytogenes on hot-smoked sea bream under constant and dynamic storage temperature conditions and (ii) to evaluate the capacity of three microbial interaction models based on the Jameson effect and Lotka-Volterra approaches to describe the inhibitory effect of L. sakei CTC494 on L. monocytogenes.
Section snippets
Bacterial strains
The selected bacterial strains used in this work were the bioprotective culture L. sakei CTC494 and the target pathogen L. monocytogenes CTC1034. This pathogenic strain was used in a previous work as a reference strain to study the antagonism of bacteriocin-producing LAB, including L. sakei CTC494 (Garriga et al., 2002). Both microorganisms were stored at −80 °C in the appropriate culture broth with 20% (v/v) glycerol. Before inoculation, a fresh culture was prepared for each strain and a
Sensory evaluation of the bioprotective L. sakei CTC494 on smoked sea bream
The average sensory scores and sensory deterioration rates obtained for the three evaluated attributes during storage at 5 °C for non-inoculated (control) and inoculated samples are showed in Fig. 1 and Table 1, respectively. Overall, no significant differences (p > 0.05) were found between the spoilage rates obtained for control and inoculated samples with 2 and 4 log CFU/g of L. sakei CTC494 throughout the storage period, with sensory scores denoting, in general, “very good” or “good” quality
Conclusions
The results from this study contribute to extend the application of the bacteriocinogenic strain L. sakei CTC494 for controlling growth of L. monocytogenes in hot-smoked fish products from Mediterranean aquaculture during refrigerated storage. Results from the challenge tests demonstrated the potential of L. sakei CTC494 applied at a dose of 4 log CFU/g to limit or inhibit the growth of L. monocytogenes on hot-smoked sea bream under different storage temperatures. Nevertheless, further research
Author contributions
Araceli Bolívar: Methodology, Investigation, Writing - Original Draft preparation, Visualization. Jean Carlos Correia Peres Costa: Validation, Writing - Review and Editing. Guiomar D. Posada-Izquierdo: Writing - Review and Editing. Sara Bover-Cid: Writing - Review and Editing. Gonzalo Zurera: Validation, Project administration, Funding acquisition. Fernando Pérez-Rodríguez: Conceptualization, Writing - Review and Editing, Supervision.
Declarations of interest
None.
Acknowledgements
This work was supported by the Projects P12-AGR-1906 and 1261329-R (AquaSafeFish) from the Andalusian Government (Spain) and the Research Group AGR-170 HIBRO. Author Araceli Bolívar was supported by the Spanish Ministry of Education under a FPU grant (FPU16/01452).
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