Bacterial Biofilms and Their Implications in Pathogenesis and Food Safety

Abstract

Biofilm formation is an integral part of the microbial life cycle in nature. In food processing environments, bacterial transmissions occur primarily through raw or undercooked foods and by cross-contamination during unsanitary food preparation practices. Foodborne pathogens form biofilms as a survival strategy in various unfavorable environments, which also become a frequent source of recurrent contamination and outbreaks of foodborne illness. Instead of focusing on bacterial biofilm formation and their pathogenicity individually, this review discusses on a molecular level how these two physiological processes are connected in several common foodborne pathogens such as Listeria monocytogenes, Staphylococcus aureus, Salmonella enterica and Escherichia coli. In addition, biofilm formation by Pseudomonas aeruginosa is discussed because it aids the persistence of many foodborne pathogens forming polymicrobial biofilms on food contact surfaces, thus significantly elevating food safety and public health concerns. Furthermore, in-depth analyses of several bacterial molecules with dual functions in biofilm formation and pathogenicity are highlighted.

Keywords: E. coli; Listeria; Pseudomonas; Salmonella; Staphylococcus; biofilm; food safety; pathogenesis.

Figure 1

Schematic showing the different stages of biofilm formation (i) attachment, (ii) microcolony formation, (iii) maturation with cellular differentiation, and (iv) detachment or dispersion, and participation of bacterial virulence factors in each step. Abbreviations: ActA, actin polymerization protein; Bap, biofilm-associated protein; bcsA, bacterial cellulose synthesis; CidA, cell death effector protein; csg, curli synthesis gene; EPS, extracellular polymeric substance; eDNA, extracellular DNA; FnBP, fibronectin-binding proteins; icaA, intercellular adhesion; LAP, Listeria adhesion protein; PIA, polysaccharide intercellular adhesin; SasG, S. aureus surface protein G; SpA, S. aureus protein A. Figure adapted with permission from Ray and Bhunia 2014 [15].

Figure 2

Listeria monocytogenes translocation pathways from lumen to lamina propria in the intestine. Figure adapted with permission from Drolia and Bhunia 2019 [47]. Copyright, Elsevier.

Figure 3

Biofilms formed (above) by recombinant Lactobacillus casei (Lbc) expressing Listeria Adhesion Protein (LAP) from L. monocytogenes (LbcLAP^Lm) or nonpathogenic L. innocua (LbcLAP^Lin) on mouse colonic villi after feeding for ten days (arrows). The wild-type Lactobacillus casei (LbcWT) did not show any biofilm formation (left panel). Bar, 25 µm. The figure was adapted with permission from Drolia et al. 2020 [51].

Figure 4

Tunicamycin-mediated inhibition of teichoic acids also suppresses S. aureus biofilm formation in a dose-dependent manner. Upper panels (A–C) show a quantitative assessment of biofilm formation (colony counts, crystal violet staining, and eDNA amounts), and lower panel (D) shows crystal violet-stained S. aureus cells in biofilms in the presence of variable concentrations of tunicamycin. The figure was adapted with permission from Zhu et al. 2018 [77]. ****, p < 0.0001; ***, p < 0.001; **, p < 0.01.