Weather stressors correlate with Escherichia coli and Salmonella enterica persister formation rates in the phyllosphere: A mathematical modeling study

Authors: Brandl, Maria; IVANEK, RENATA - Cornell University; ZEKAJ, NERION - Cleveland State University; BELIAS, ALEXANDRA - Cornell University; WIEDMANN, MARTIN - Cornell University; SUSLOW, TREVOR - University Of California, Davis; ALLENDE, ANA - Centro De Edafologia Y Biologia Aplicada Del Segura (CEBAS); MUNTHER, DANIEL - Cleveland State University

Submitted to: ISME Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/6/2022
Publication Date: 9/27/2022
Citation: Brandl, M., Ivanek, R., Zekaj, N., Belias, A., Wiedmann, M., Suslow, T.V., Allende, A., Munther, D.S. 2022. Weather stressors correlate with Escherichia coli and Salmonella enterica persister formation rates in the phyllosphere: A mathematical modeling study. ISME Communications. 2:91. https://doi.org/10.1038/s43705-022-00170-z.
DOI: https://doi.org/10.1038/s43705-022-00170-z

Interpretive Summary: Outbreaks of produce-associated foodborne illness continue to pose a threat to human health and a challenge to the produce industry. Thus, the survival of foodborne pathogenic bacteria on plant surfaces is of great interest to public health. Enteric pathogens have the ability to enter a persister (dormant) state in which they have enhanced tolerance to physicochemical stresses. The presence of such dormant cells has been identified in E. coli O157:H7 populations on lettuce plants contaminated in the laboratory. We applied here, a mathematical model predicting the switch rate from normal to persister cell to identify weather factors associated with E. coli and Salmonella persister formation using data from published lettuce and spinach field studies in California, New York and Murcia, Spain. Results from our model study and correlation analysis indicate that high UV intensity and low air temperature, relative humidity, and dew point, therefore limited water availability on the leaves, may be significant inducers and therefore, predictors of enteric pathogen persister formation on plants in the field. These subpopulations of dormant cells may be of considerable importance to produce safety since they would act as reservoirs of contaminants from farm to table. Furthermore, their presence may lower the efficacy of produce sanitization due their known enhanced tolerance to antimicrobial, acidic pH, and oxidative stress. Hence, prediction of persister cell population sizes on crops based on environmental factors may serve as a powerful tool to improve food safety.

Technical Abstract: Outbreaks of produce-associated foodborne illness continue to pose a threat to human health and a challenge to the produce industry. Thus, the survival of foodborne pathogenic bacteria on plant surfaces is of great interest to public health. Enteric pathogens have the ability to enter a persister (dormant) state in which they have enhanced tolerance to physicochemical stresses. The presence of such dormant cells has been identified in E. coli O157:H7 populations on lettuce plants contaminated in the laboratory. We applied here, a mathematical model predicting the switch rate from normal to persister cell to identify weather factors associated with E. coli and Salmonella persister formation using data from published lettuce and spinach field studies in California, New York and Murcia, Spain. Results from our model study and correlation analysis indicate that high UV intensity and low air temperature, relative humidity, and dew point, therefore limited water availability on the leaves, may be significant inducers and therefore, predictors of enteric pathogen persister formation on plants in the field. These subpopulations of dormant cells may be of considerable importance to produce safety since they would act as reservoirs of contaminants from farm to table. Furthermore, their presence may lower the efficacy of produce sanitization due their known enhanced tolerance to antimicrobial, acidic pH, and oxidative stress. Hence, prediction of persister cell population sizes on crops based on environmental factors may serve as a powerful tool to improve food safety.