Curli fimbriae confer shiga toxin-producing Escherichia coli a competitive trait in mixed biofilms

Authors: Carter, Michelle; Feng, Doris; Li, Hui Hong

Submitted to: Food Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/19/2019
Publication Date: 3/22/2019
Citation: Carter, M.Q., Feng, D., Li, H. 2019. Curli fimbriae confer shiga toxin-producing Escherichia coli a competitive trait in mixed biofilms. Food Microbiology. 82:482-488. https://doi.org/10.1016/j.fm.2019.03.024.
DOI: https://doi.org/10.1016/j.fm.2019.03.024

Interpretive Summary: Biofilm is a ubiquitous lifestyle of bacteria associated with a surface. Many bacteria including enteric pathogens produce diverse fimbriae and adhesins such as curli that promote bacterial surface attachment and biofilm formation. Biofilm-associated cells are more resistant to toxic substances including antibiotics, chlorine, and detergents, thus they are generally more resistant to antimicrobial washes used in the produce industry. In this study, we investigated both environmental and bacterial factors that may contribute to the biofilm formation of enteric pathogen E. coli O157:H7 on surfaces of stainless steel, a common material used in food industry. We first examined survival of E. coli O157:H7 in spinach leaf wash water and observed a growth of this pathogen at 4'C, 10'C, and 26'C, implying a potential amplification of the pathogen even at cold storage conditions. We next examined the biofilm population of E. coli O157:H7 on stainless steel surfaces in the presence and absence of spinach-associated microorganisms, and discovered a distinct difference in biofilm population between the E. coli O157:H7 curli-expressing and curli-deficient strains. Curli-deficient strain was impaired in formation of the mixed biofilm by E. coli O157:H7 and spinach-associated microorganisms; however this deficiency was rescued when curli biogenesis was restored. Our data suggest that curli fimbriae not only promote the direct contact of pathogen cells with surfaces of stainless steel, but also mediate the interaction of pathogen cells with spinach-associated microorganisms. Such interactions expanded the ecological niches of E. coli O157:H7 and enhance the persistence of this pathogen in produce-processing environments.

Technical Abstract: Shiga toxin-producing Escherichia coli (STEC) is one of the most important causal agents of foodborne illness linked to fresh leafy vegetables. Here, we investigated the impact of spinach-associated microorganisms on survival and biofilm formation of STEC O157:H7 on stainless steel surfaces at temperatures related to produce production and postharvest produce-processing environments. The impact of spinach-associated microorganisms on the survival of E. coli O157:H7 was observed at 10'C and 26'C, but not at 4'C. The inhibition of E. coli O157:H7 growth by spinach-associated microorganisms indicated a competition between E. coli O157:H7 and spinach indigenous microflora. The impact of spinach-associated microorganisms on biofilm of E. coli O157:H7 was temperature and strain dependent. A significant decrease of pathogen population in mixed biofilm was observed only at 26'C for curli-deficient strain MQC43, but not for curli-producing strain MQC57. Deletion of curli genes in MQC57 led to a significant decease of pathogen population in mixed biofilm; whereas expression of curli genes in mutant restored pathogen population in mixed biofilm to a level similar to that of MQC57. Our data support that curli confer E. coli O157:H7 a competitive trait in mixed biofilm, presumably through the interaction between STEC and the biofilm-proficient microorganisms associated with spinach leaves such as Pseudomonas spp.