Survival, growth, and biogenic amine production of Enterococcus faecium FC12 in response to extracts and essential oils of Rubus fruticosus and Juniperus oxycedrus

Chiara Montanari; Federica Barbieri; Silvia Lorenzini; Davide Gottardi; Vida Šimat; Fatih Özogul; Fausto Gardini; Giulia Tabanelli

doi:10.3389/fnut.2022.1092172

Survival, growth, and biogenic amine production of Enterococcus faecium FC12 in response to extracts and essential oils of Rubus fruticosus and Juniperus oxycedrus

Front Nutr. 2023 Jan 13:9:1092172. doi: 10.3389/fnut.2022.1092172. eCollection 2022.

Authors

Chiara Montanari¹, Federica Barbieri¹, Silvia Lorenzini¹, Davide Gottardi^{1

2}, Vida Šimat³, Fatih Özogul⁴, Fausto Gardini^{1

2}, Giulia Tabanelli^{2

5}

Affiliations

¹ Department of Agricultural and Food Sciences, University of Bologna, Cesena, Italy.
² Interdepartmental Center for Industrial Agri-food Research, University of Bologna, Cesena, Italy.
³ University Department of Marine Studies, University of Split, Split, Croatia.
⁴ Department of Seafood Processing Technology, Faculty of Fisheries, Cukurova University, Adana, Turkey.
⁵ Department of Agricultural and Food Sciences, University of Bologna, Bologna, Italy.

Abstract

Introduction: Enterococci are lactic acid bacteria (LAB) usually found as food contaminants in fermented products such as cheeses and fermented sausages. Due to their antibiotic resistance, the presence of virulence factors, and the ability to produce biogenic amines (BAs), the determination of these bacteria is crucial to assure food quality and safety. BAs production and consequent accumulation in foods can cause toxicological effects on human health. Plant phenolic compounds are promising alternatives to chemical preservatives and reflect consumers' demand for "green" solutions. In this study, the antimicrobial effect of blackberry (Rubus fruticosus) leaves and prickly juniper (Juniperus oxycedrus) needles, both as phenolic extracts (PE) and essential oils (EO), were evaluated against Enterococcus faecium FC12, a known tyramine-producing strain.

Methods: The growth kinetics in the presence of sub-lethal concentrations of such plant derivatives were modeled (Gompertz equation) and BA production was monitored over time by HPLC. Moreover, flow cytometry (FCM) was used to study the effects of EOs and PEs on cell viability.

Results: The EOs showed a higher antimicrobial effect (especially R. fruticosus added at 0.75 mg/ml), determining an initial decrease of culturable cells followed by a recovery, even if with lower growth rates and final cell loads. Different rates of BA formation were observed, with tyramine concentrations ranging from 120 to 160 mg/l after 96 h of incubation, and 2-phenylethylamine was produced in lower amounts, usually after reaching the peak of tyramine. FCM confirmed the higher efficacy of R. fruticosus EO that induced cell membrane injury in 93% of the total population. However, complete recovery occurred in the following incubation, demonstrating transient damage.

Discussion: Although further research is required to better investigate this recovery and to assess the suitability of this approach in a real food system, the present study showed the potential antimicrobial activity of plant derivatives, especially R. fruticosus EO, against the tyramine-producing E. faecium FC12.

Keywords: Enterococcus faecium; Juniperus oxycedrus; Rubus fruticosus; antimicrobial activity; flow cytometry; growth kinetics; tyramine production.

Grants and funding

This research was supported by the PRIMA program under BioProMedFood (Project ID 1467; CUP: J34I19004820005). The PRIMA program was supported by the European Union H2020 program.