Weakening of Salmonella with selected microbial metabolites of berry-derived phenolic compounds and organic acids

Hanna-Leena Alakomi (Corresponding Author), Riitta Puupponen-Pimiä, Anna-Marja Aura, Ilkka M. Helander, Liisa Nohynek, Kirsi-Marja Oksman-Caldentey, Maria Saarela

    Research output: Contribution to journalArticleScientificpeer-review

    80 Citations (Scopus)

    Abstract

    Gram-negative bacteria are important food spoilage and pathogenic bacteria. Their unique outer membrane (OM) provides them with a hydrophilic surface structure, which makes them inherently resistant to many antimicrobial agents, thus hindering their control. However, with permeabilizers, compounds that disintegrate and weaken the OM, Gram-negative cells can be sensitized to several external agents. Although antimicrobial activity of plant-derived phenolic compounds has been widely reported, their mechanisms of action have not yet been well demonstrated. The aim of our study was to elucidate the role of selected colonic microbial metabolites of berry-derived phenolic compounds in the weakening of the Gram-negative OM. The effect of the agents on the OM permeability of Salmonella was studied utilizing a fluorescence probe uptake assay, sensitization to hydrophobic antibiotics, and lipopolysaccharide (LPS) release. Our results show that 3,4-dihydroxyphenylacetic acid, 3-hydroxyphenylacetic acid, 3-(3,4-dihydroxyphenyl)propionic acid (3,4-diHPP), 3-(4-hydroxyphenyl)propionic acid, 3-phenylpropionic acid, and 3-(3-hydroxyphenyl)propionic acid efficiently destabilized the OM of Salmonella enterica subsp. enterica serovar Typhimurium and S. enterica subsp. enterica serovar Infantis as indicated by an increase in the uptake of the fluorescent probe 1-N-phenylnaphthylamine (NPN). The OM-destabilizing activity of the compounds was partially abolished by MgCl2 addition, indicating that part of their activity is based on removal of OM-stabilizing divalent cations. Furthermore, 3,4-dihydroxyphenylacetic acid, 3-hydroxyphenylacetic acid, and 3,4-diHPP increased the susceptibility of S. enterica subsp. enterica serovar Typhimurium strains for novobiocin. In addition, organic acids present in berries, such as malic acid, sorbic acid, and benzoic acid, were shown to be efficient permeabilizers of Salmonella as shown by an increase in the NPN uptake assay and by LPS release.
    Original languageEnglish
    Pages (from-to)3905 - 3912
    JournalJournal of Agricultural and Food Chemistry
    Volume55
    Issue number10
    DOIs
    Publication statusPublished - 2007
    MoE publication typeA1 Journal article-refereed

    Keywords

    • Permeability
    • Gram-negative
    • Salmonella
    • phenolic compounds
    • metabolites
    • organic acid

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