The Microbial Lipopeptide Paenibacterin Disrupts Desiccation Resistance in Salmonella enterica Serovars Tennessee and Eimsbuettel

Abstract

Salmonella enterica is increasingly linked to disease outbreaks associated with consumption of low-water-activity (low-a w ) foods. Persistence of the pathogen in these foods was attributed to its ability to implement desiccation resistance mechanisms. Published knowledge about methods that disrupt desiccation resistance in S. enterica is lacking. We hypothesize that strong membrane-active compounds disrupt the desiccation resistance that S. enterica may acquire in low-a w foods or environments. The newly discovered antimicrobial lipopeptide paenibacterin was the membrane-active agent investigated in this study. Strains of S. enterica serovars Tennessee and Eimsbuettel, with a history of association with low-moisture foods, were investigated. The viability of these strains did not decrease significantly during dehydration and subsequent storage in the dehydrated state. Considering that the paenibacterin MIC against S. enterica strains was 8 g/ml, concentrations of 4 to 16 g/ml paenibacterin were tested. Within this range, desiccation-adapted S. Eimsbuettel was much more tolerant to the antimicrobial agent than the desiccation-adapted S. Tennessee. Pretreatment with 8 g/ml paenibacterin increased inactivation of S. enterica during desiccation. The use of paenibacterin at 16 g/ml or higher concentrations resulted in leakage of intracellular potassium ions from desiccation-adapted cells. Paenibacterin significantly decreased the biosynthesis of the intracellular osmoprotectant solute, trehalose, in a concentrationdependent manner. Treatment with 64 g/ml paenibacterin increased the permeability of the cytoplasmic membranes of desiccation-adapted cells. Transcription of the desiccation-related genes proV, STM1494, kdpA, and otsB in response to paenibacterin treatment was investigated using reverse transcription-quantitative PCR. Transcription of some of these genes was downregulated in a concentration-and strain-dependent manner. IMPORTANCE Salmonella enterica adapts effectively and persists for a long time in low-a w foods or environments through resistance mechanisms to desiccation stress. Desiccation-resistant cells compromise food safety and constitute a serious health hazard. Strategies to combat desiccation resistance in S. enterica are needed to sensitize the pathogen to lethal processes used in food preservation. The study proved that the membrane-active lipopeptide paenibacterin disrupts the resistance in desiccation-adapted S. enterica, as measured by phenotypic, biochemical, and genetic analyses. This study highlighted the role of the lipopeptide paenibacterin in disrupting mechanisms employed by S. enterica to resist desiccation. This knowledge may lead to the design of novel control measures to improve the safety of low-a w foods.

Persistence of Pathogens on Inanimate Surfaces: A Narrative Review

“…The longest survival of all three species were detected at 5 °C, where the bacteria were not inactivated after 300 days and showed a maximum reduction of 4 logs [ 135 ]. Other serotypes, S. Tennessee and S. Eimsbuettel were detectable after 72 h on plastic at 22 °C and 40% RH according to a study by Abdelhamid et al [ 149 ]. The titer reduction was 1-log after 72 h [ 149 ].…”

“…Other serotypes, S. Tennessee and S. Eimsbuettel were detectable after 72 h on plastic at 22 °C and 40% RH according to a study by Abdelhamid et al [ 149 ]. The titer reduction was 1-log after 72 h [ 149 ].…”

Natural Antimicrobials Suitable for Combating Desiccation-Resistant Salmonella enterica in Milk Powder

“…Hence, our goal was to explore methods to overcome desiccation-resistant Salmonella without excessive processing. In a previous study, we found that a newly discovered microbial lipopeptide, paenibacterin, disrupted the desiccation resistance in S. enterica and rendered the pathogen sensitive to desiccation [ 8 ]. Paenibacterin caused intracellular potassium leakage, increased the cytoplasmic membrane permeability, decreased the biosynthesis of the osmoprotectant trehalose, and downregulated the expression of desiccation-related genes in desiccation-adapted S. enterica .…”

Controlling foodborne pathogens with natural antimicrobials by biological control and antivirulence strategies

“…Such synergistic interaction, also known as hurdle approach, aims to get maximum lethality against foodborne pathogens ( Leistner, 2000 ). For example, sequential application of the lipopeptide paenibacterin and desiccation stress resulted in significant population reduction (1.5–1.9 log CFU/ml) of S. enterica serovars compared to desiccation stress alone (<0.1 log CFU/ml) ( Abdelhamid and Yousef, 2019 ). Another example was that three antimicrobials, nisin A, lactoperoxidase, and reuterin, synergized to control L. monocytogenes and S. aureus in a dairy product with 4-log reduction after incubation at 10 °C for 12 days, compared to that reduction by any of the two antimicrobials ( Arqués et al., 2008 ).…”