Abstract
Salmonella enterica subspecies I (ssp 1) is the leading cause of hospitalizations and deaths due to known bacterial foodborne pathogens in the United States and is frequently implicated in foodborne disease outbreaks associated with spices and nuts. However, the underlying mechanisms of this association have not been fully elucidated. In this study, we evaluated the influence of storage temperature (4 or 25°C), relative humidity (20 or 60%), and food surface characteristics on the attachment and survival of five individual strains representing S. enterica ssp 1 serovars Typhimurium, Montevideo, Braenderup, Mbandaka, and Enteritidis on raw in-shell black peppercorns, almonds, and hazelnuts. We observed a direct correlation between the food surface roughness and S. enterica ssp 1 attachment, and detected significant inter-strain difference in survival on the shell surface under various storage conditions. A combination of low relative humidity (20%) and ambient storage temperature (25°C) resulted in the most significant reduction of S. enterica on shell surfaces (p < 0.05). To identify genes potentially associated with S. enterica attachment and survival on shell surfaces, we inoculated a library of 120,000 random transposon insertion mutants of an S. Enteritidis strain on almond shells, and screened for mutant survival after 1, 3, 7, and 14 days of storage at 20% relative humidity and 25°C. Mutants in 155 S. Enteritidis genes which are involved in carbohydrate metabolic pathways, aerobic and anaerobic respiration, inner membrane transport, and glutamine synthesis displayed significant selection on almond shells (p < 0.05). Findings of this study suggest that various food attributes, environmental factors, and an unexpectedly complex metabolic and regulatory network in S. enterica ssp 1 collectively contribute to the bacterial attachment and survival on low moisture shell surface, providing new data for the future development of knowledge-based intervention strategies.
Highlights
Salmonella enterica subspecies I serovars have been implicated in a number of multi-state foodborne disease outbreaks associated with nuts and spices in recent decades in the United States
We compared the relative ability of different S. enterica ssp 1 serovars to attach to and survive on raw nuts and spices, which serves as an initial step of food contamination
After inoculation and air-drying, and prior to storage, we collected and enumerated S. enterica cells attached on black peppercorns, almonds and hazelnuts to evaluate the initial level of bacterial attachment for each strain on each type of shell surface
Summary
Salmonella enterica subspecies I serovars have been implicated in a number of multi-state foodborne disease outbreaks associated with nuts and spices in recent decades in the United States. In 2004, serovar Enteritidis was linked to raw almonds in an outbreak in 12 states, leading to 29 cases of infections (Centers for Disease Control Prevention [CDC], 2004). Montevideo linked to black pepper (Centers for Disease Control Prevention [CDC], 2010). Senftenberg infections, which sickened 11 persons in 9 states (Centers for Disease Control Prevention [CDC], 2018). Mbandaka (Scheil et al, 1998; Centers for Disease Control Prevention [CDC], 2009, 2011, 2014). These foodborne outbreaks highlight the need for a thorough examination of the mechanisms of S. enterica survival and persistence on nuts and spices
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