Growth of salmonella enterica serovars typhimurium and enteritidis in iron-poor media and in meat: Role of catecholate and hydroxamate siderophore transporters

Citation

Chekabab, S.M., Rehman, M.A., Yin, X., Carrillo, C., Mondor, M., Diarra, M.S. (2019). Growth of salmonella enterica serovars typhimurium and enteritidis in iron-poor media and in meat: Role of catecholate and hydroxamate siderophore transporters, 82(4), 548-560. http://dx.doi.org/10.4315/0362-028X.JFP-18-371

Plain language summary

Iron is an essential mineral for the growth and survival of both Salmonella Enteritidis and Typhimurium which are two majors causes of salmonellosis disease in Canada. In this study, we deleted components of two iron uptake systems of both Enteritidis and Typhimurium to evaluate their impact on growth and survival in various iron-content environments. Our results showed that partial or complete deletion of the studied iron uptake systems did not abolished growth of Salmonella in an iron rich environment. However, in an iron-restricted medium similar to that found in hosts (human and chicken), the partial or complete removal of investigated iron uptake systems affected differently the growth of Enteritidis and Typhimurium with Enteritidis being the most affected by deletion. The lack of the two iron systems did not impact the susceptibility of Enteritidis or Typhimurium to antibiotic however, their ability to use specific iron scavenging agents to fulfill their iron need was significantly reduced. We demonstrated that removal of specific iron systems alone or in combination did not abolish the survival of Salmonella in chicken breast meat which is rich in iron. Thus, our data suggest that iron content of chicken meat should be taken account when developing an iron chelation-based method as a preservative method against Salmonella. This work deals with important food safety issues and underlines the importance of monitoring the survival of Salmonella in chicken meat with respect to designing effective control strategies for the food protection.

Abstract

© 2018, International Association for Food Protection. All rights reserved. Enteritidis and Typhimurium are among the top Salmonella enterica serovars implicated in human salmonellosis worldwide. This study examined the individual and combined roles of catecholate-iron and hydroxamate-iron transporters in the survival in meat of Salmonella Enteritidis and Typhimurium. Catecholate–iron-III (Fe 3þ ) and hydroxamate-Fe 3þ transporter genes fepA, iroN, and fhuACDB were deleted in isolates of these serovars to generate single, double, and triple mutants. Growth rate in high-and low-iron media was compared among mutants, complements, and their wild-type parents. Susceptibility to 14 antibiotics, the ability to produce and utilize siderophores, and survival on cooked chicken breast were evaluated. In iron-poor liquid media, differences were observed between the growth characteristics of mutant Salmonella Enteritidis and Typhimurium. The double ΔiroNΔfepA and the triple ΔfhuΔiroNΔfepA mutants of Salmonella Enteritidis exhibited prolonged lag phases (λ ¼ 9.72 and 9.53 h) and a slow growth rate (μ max ¼ 0.35 and 0.25 h 1 ) similar to that of its ΔtonB mutant (λ ¼ 10.12 h and μ max ¼ 0.30 h 1 ). In Salmonella Typhimurium, double ΔiroNΔfepA and triple ΔfhuΔiroNΔfepA mutations induced a similar growth pattern as its ΔtonB mutant. Double deletions of fepA and iroN reduced the siderophore production and the use of enterobactin as an iron source. In the ΔiroNΔfepA mutant, but not in ΔfhuΔiroNΔfepA, the ferrichrome or deferrioxamine promoted growth for both serovars, confirming the specific role of the FhuACDB system in the uptake and transport of hydroxamate Fe 3þ . Survival of the mutants was also evaluated in a meat assay, and no difference in survival was observed among the mutants compared with wild type. This study showed differences between serovars in the importance of catecholate-iron and hydroxamate-iron uptake on Salmonella growth in iron-restricted media. Data also confirmed that both Salmonella Enteritidis and Typhimurium are well equipped to survive on cooked chicken meat, offering a rich iron condition.