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Food Microbiology | Spotlight

Overlap of Spoilage-Associated Microbiota between Meat and the Meat Processing Environment in Small-Scale and Large-Scale Retail Distributions

Giuseppina Stellato, Antonietta La Storia, Francesca De Filippis, Giorgia Borriello, Francesco Villani, Danilo Ercolini
C. A. Elkins, Editor
Giuseppina Stellato
aDepartment of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy
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Antonietta La Storia
aDepartment of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy
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Francesca De Filippis
aDepartment of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy
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Giorgia Borriello
bDepartment of Animal Health, Istituto Zooprofilattico Sperimentale del Mezzogiorno, Portici, Italy
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Francesco Villani
aDepartment of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy
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Danilo Ercolini
aDepartment of Agricultural Sciences, Division of Microbiology, University of Naples Federico II, Portici, Italy
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C. A. Elkins
FDA Center for Food Safety and Applied Nutrition
Roles: Editor
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DOI: 10.1128/AEM.00793-16
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  • FIG 1
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    FIG 1

    Box plots showing numbers of observed OTUs (A and B) and Chao1 diversity index values (C and D) for environmental swabs (red) and meat samples (blue) from SD (A and C) and LD (B and D) establishments. Boxes, interquartile ranges (between the first and third quartiles); lines inside boxes, medians (second quartiles); whiskers, lowest and highest values within 1.5 times the interquartile range (from the first and third quartiles, respectively); circles, outliers beyond the whiskers. *, significant difference obtained with the pairwise Wilcox test (FDR, <0.05).

  • FIG 2
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    FIG 2

    Abundance of bacterial species in meat (A and C) and environmental (B and D) samples from SD (A and B) and LD (C and D) facilities. Only OTUs showing relative abundances of ≥2% and occurring in >5 samples are reported. Other, all OTUs that failed to reach the cutoff value. Samples are coded as follows: 1, knife; 2, chopping board; 3, hand; 4, pork; 5, beef. Capital letters, different butcheries, as reported in Table S1 in the supplemental material.

  • FIG 3
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    FIG 3

    Venn diagrams showing the numbers of shared genera between groups of samples, as determined by 16S rRNA gene pyrosequencing analysis. Samples were grouped as meat versus environmental samples for the LD and SD groups (A) and for the LD and SD groups combined (B).

  • FIG 4
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    FIG 4

    Hierarchical average linkage clustering of the samples based on the Pearson's correlation coefficient for the abundance of genera present in ≥20% of the samples. The color scale indicates the scaled abundance of each variable, denoted as the Z-score; red, high abundance; blue, low abundance. Column bars are colored according to the type of sample (meat or environmental swab) and the type of retail facility (SD or LD), and the row bar is colored according to the classification at the phylum level. Samples are coded as follows: 1, knife; 2, chopping board; 3, hand; 4, pork; 5, beef. Capital letters, different butcheries, as reported in Table S1 in the supplemental material.

  • FIG 5
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    FIG 5

    Hierarchical average linkage clustering of the samples based on the Pearson's correlation coefficient for the abundance of predicted KEGG orthologs collapsed at hierarchy level 3, filtered for sample prevalence of ≥20%. The color scale indicates the scaled abundance of each variable, denoted as the Z-score; red, high abundance; blue, low abundance. Column bars are colored according to the type of sample (meat or environmental swab) and the type of retail facility (SD or LD), and the row bar is colored according to the higher hierarchy level in the KEGG classification. Only KEGG orthologs related to carbohydrate, amino acid, or lipid metabolism are reported. Samples are coded as follows: 1, knife; 2, chopping board; 3, hand; 4, pork; 5, beef. Capital letters, different butcheries, as reported in Table S1 in the supplemental material.

  • FIG 6
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    FIG 6

    Heatplot showing the correlations between Firmicutes and Proteobacteria members and predicted KEGG orthologs collapsed at hierarchy level 3, both filtered for sample prevalence of ≥20%. Rows and columns are clustered by Euclidean distance and Ward linkage hierarchical clustering. The intensity of the colors represents the degree of association between the OTUs and the KEGG orthologs, as measured by Spearman's correlations. The row bar is colored according to the OTU classification at the phylum level, and the column bar is colored according to the higher hierarchy level in the KEGG classification. Only KEGG orthologs related to carbohydrate, amino acid, or lipid metabolism are reported.

Additional Files

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    • Supplemental file 1 -

      Meat and environmental samples analyzed in this study (Table S1), aerobic plate counts (Table S2), counts of Enterobacteriaceae (Table S3), lactic acid bacteria (Table S4), Pseudomonas spp. (Table S5), and Brochothrix thermosphacta (Table S6) in meat and environmental samples, microbial counts in small- and large-scale retails (Table S7), relative abundance of the core OTUs shared by meat and surface samples (Table S8), PCA (Fig. S1 and S2), and Spearman's rank correlation matrix (Fig. S3).

      PDF, 11M

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Overlap of Spoilage-Associated Microbiota between Meat and the Meat Processing Environment in Small-Scale and Large-Scale Retail Distributions
Giuseppina Stellato, Antonietta La Storia, Francesca De Filippis, Giorgia Borriello, Francesco Villani, Danilo Ercolini
Applied and Environmental Microbiology Jun 2016, 82 (13) 4045-4054; DOI: 10.1128/AEM.00793-16

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Overlap of Spoilage-Associated Microbiota between Meat and the Meat Processing Environment in Small-Scale and Large-Scale Retail Distributions
Giuseppina Stellato, Antonietta La Storia, Francesca De Filippis, Giorgia Borriello, Francesco Villani, Danilo Ercolini
Applied and Environmental Microbiology Jun 2016, 82 (13) 4045-4054; DOI: 10.1128/AEM.00793-16
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