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Transcriptome Analysis of Listeria monocytogenes Exposed to Beef Fat Reveals Antimicrobial and Pathogenicity Attenuation Mechanisms.

ABSTRACT: Listeria monocytogenes is a deadly intracellular pathogen mostly associated with consumption of ready-to-eat foods. This study investigated the effectiveness of total beef fat (BF-T) from flaxseed-fed cattle and its fractions enriched with monounsaturated fatty acids (BF-MUFA) and polyunsaturated fatty acids (BF-PUFA), along with commercially available long-chain fatty acids (LC-FA), as natural antimicrobials against L. monocytogenes BF-T was ineffective at concentrations up to 6 mg/ml, while L. monocytogenes was susceptible to BF-MUFA and BF-PUFA, with MICs at pH 7 of 0.33 ± 0.21 mg/ml and 0.06 ± 0.03 mg/ml, respectively. The MIC of C14:0 was significantly lower than those of C16:0 and C18:0 (P < 0.05). Fatty acids c9-C16:1, C18:2n-6, and C18:3n-3 showed stronger inhibitory activity than c9-C18:1 and conjugated C18:2, with MICs of <1 mg/ml. Furthermore, global transcriptional analysis by transcriptome sequencing (RNA-seq) was performed to characterize the response of L. monocytogenes to selected fatty acids. Functional analysis indicated that antimicrobial LC-UFA repressed the expression of genes associated with nutrient transmembrane transport, energy generation, and oxidative stress resistance. On the other hand, upregulation of ribosome assembly and translation process is possibly associated with adaptive and repair mechanisms activated in response to LC-UFA. Virulence genes and genes involved in bile, acid, and osmotic stresses were largely downregulated, and more so for c9-C16:1, C18:2n-6, and C18:3n-3, likely through interaction with the master virulence regulator PrfA and the alternative sigma factor σ^B IMPORTANCE Listeria monocytogenes is a bacterial pathogen known for its ability to survive and thrive under adverse environments and, as such, its control poses a significant challenge, especially with the trend of minimally processed and ready-to-eat foods. This work investigated the effectiveness of fatty acids from various sources as natural antimicrobials against L. monocytogenes and evaluated their potential role in L. monocytogenes pathogenicity modulation, using the strain ATCC 19111. The findings show that long-chain unsaturated fatty acids (LC-UFA), including unsaturated beef fat fractions from flaxseed-fed cattle, could have the potential to be used as effective antimicrobials for L. monocytogenes through controlling growth as well as virulence attenuation. This not only advances our understanding of the mode of action of LC-UFA against L. monocytogenes but also suggests the potential for use of beef fat or its fractions as natural antimicrobials for controlling foodborne pathogens.

SUBMITTER: Chen YY

PROVIDER: S-EPMC8091014 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Lemon (Citrus limon) is a flowing plant belonging to the Rutaceae family. Citrus plants constitute one of the main valuable sources of essential oil used in foods and medicinal purposes.In this study, we assessed chemical composition, antioxidant and antimicrobial activities of C. limon essential oil (ClEO) with its preservative effect against Listeria monocytogenes inoculated in minced beef meat. Gas chromatography/mass spectrometry (GC-MS) was used to identify the major components of the obtained ClEO. The antioxidant activities of this ClEO were determined according to the β-carotene bleaching assay, as well as by 2.2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity. For antimicrobial activity, agar well diffusion method was used and the minimum inhibitory concentrations (MICs) as well as the minimum fungicidal concentrations (MFCs) were determined. The in situ effect of the ClEO was evaluated through physicochemical parameters (pH and thiobarbituric acid reactive substances (TBARS), as well as against L. monocytogenes in minced beef meat model.Twenty one components were identified in the ClEO and the two dominant compounds were limonene (39.74%) and β-Pinene (25.44%). This ClEO displayed an excellent DPPH scavenging ability with an extract concentration providing 50% inhibition (IC50) of 15.056 μg/ml and a strong β-carotene bleaching inhibition after 120 min of incubation with an IC50 of 40.147 μg/ml. The MICs varied from 0.039 to 1.25 mg/ml for Gram positive bacteria and from 0.25 to 2.5 mg/ml for Gram-negative bacteria. The meat preserving potential of ClEO was investigated against L. monocytogenes. ClEO successfully inhibited development of L. monocytogenes in minced beef meat. The application of ClEO at a 0.06 and 0.312 mg/g, may open new promising opportunities for the prevention of contamination from and growth of pathogenic bacteria, particularly L. monocytogenes, during minced beef meat storage at 4 °C. Additionally, during storage period, physicochemical values (pH and TBARS) were higher in control meat than treated meat with ClEO suggesting an efficient antioxidant activity of ClEO.It was suggested that the ClEO may be a new potential source as natural antimicrobial and antioxidant agents applied in food systems and pharmaceutical industry.

Project description:Listeria monocytogenes remains a significant public health threat, causing invasive listeriosis manifested as septicemia, meningitis, and abortion, with up to 30% of cases having a fatal outcome. Tracking the spread of invasive listeriosis requires an updated knowledge for virulence factors (VFs) and antimicrobial resistance features, which is an essential step toward its clinical diagnosis and treatment. Taking advantage of high-throughput genomic sequencing, we proposed that the differential genes based on the pathogenomic composition could be used to evaluate clinical observations and therapeutic options for listeriosis. Here, we performed the comparative genomic analysis of 60 strains from five continents with a diverse range of sources, representing serotypes 1/2a, 1/2b, 1/2c, and 4b, comprising lineage I and lineage II and including 13 newly contributed Chinese isolates from clinical cases. These strains were associated with globally distributed clonal groups linked with confirmed foodborne listeriosis outbreak and sporadic cases. We found that L. monocytogenes strains from clonal complex (CC) CC8, CC7, CC9, and CC415 carried most of the adherence and invasive genes. Conversely, CC1, CC2, CC4, and CC6 have the least number of adherence and invasive genes. Additionally, Listeria pathogenicity island-1 (LIPI-1), LIPI-2, intracellular survival, surface anchoring, and bile salt resistance genes were detected in all isolates. Importantly, LIPI-3 genes were harbored in CC3, CC224, and ST619 of the Chinese isolates and in CC1, CC4, and CC6 of other worldwide isolates. Notably, Chinese isolates belonging to CC14 carried antibiotic resistance genes (ARGs) against β-lactams (bla TEM-101 , bla TEM-105) and macrolide (ermC-15), whereas CC7 and CC8 isolates harbored ARGs against aminoglycoside (aadA10_2, aadA6_1), which may pose a threat to therapeutic efficacy. Phylogenomic analysis showed that CC8, CC7, and CC5 of Chinese isolates, CC8 (Swiss and Italian isolates), and CC5 and CC7 (Canadian isolates) are closely clustered together and belonged to the same CC. Additionally, CC381 and CC29 of Chinese isolates shared the same genomic pattern as CC26 of Swiss isolate and CC37 of Canadian isolate, respectively, indicating strong phylogenomic relation between these isolates. Collectively, this study highlights considerable clonal diversity with well-recognized virulence and antimicrobial-resistant determinants among Chinese and worldwide isolates that stress to design improved strategies for clinical therapies.

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Transcriptome Analysis of Listeria monocytogenes Exposed to Beef Fat Reveals Antimicrobial and Pathogenicity Attenuation Mechanisms.

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