Iron-Uptake Systems of Chicken-Associated Salmonella Serovars and Their Role in Colonizing the Avian Host
Abstract
:1. Introduction
1.1. Iron Homeostasis by Salmonella in a Nutshell: Regulation and Iron-Uptake Systems
1.2. Ferric Uptake Regulator (Fur)-Mediated Regulation of Iron Uptake, Storage and Utilization
1.3. Uptake of Ferric (Fe3+) Iron via Siderophores
1.4. Uptake of Ferrous Iron (Fe2+) via FeoABC, SitABCD and MntH
2. Emergence of Chicken-Associated Invasive NTS: The Iron Link
3. Iron Uptake in NTS Virulence: Chicken vs. Mammalian Models
3.1. Feo-Mediated Fe2+ Uptake Involved in Rapid Colonization of the Gut and Systemic Spread
- (i)
- Feo-mediated ferrous iron uptake is important for rapid colonization by and systemic spread of Salmonella Typhimurium in NRAMP+/+ mice. We predict the same in chicken–NTS interaction.
- (ii)
- Feo may not be essential for persistent infection in mouse models due to redundancy of various iron-uptake systems. This includes Mn2+ uptake via SitABCD and MntH, and uptake of siderophores.
- (iii)
- NTS predilects to iron-rich hemophagocytes during systemic infection.
3.2. Siderophore Synthesis Is Important During Persistent Infection and Bacteremia
- (i)
- Ferric iron uptake mechanisms are important for persistent infection.We predict similar results for chicken as those found in mouse models because bioavailability of iron is expected to be low in most compartments of the host.
- (ii)
- Aerobactin, salmochelin and yersiniabactin provide a serum resistance during bacteremia and systemic infection. This may explain the siderophore link towards chicken-associated virulent NTS serovars.
- (iii)
- The role of stealth siderophores of NTS in adult chickens during colonization may be nonessential due to tolerogenic response.
4. Opening the Pandora’s Box of Gallus-Iron-Salmonella Interaction
4.1. Nutritional Immunity Status in Chicken during Salmonella Infection
4.2. Non-Canonical Function of Siderophores: Defense against Respiratory Burst and Immunomodulatory Function
5. Concluding Remarks
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Serotype | Source | Year(s) | Geographical Region | No of Cases a | References |
---|---|---|---|---|---|
Enteritidis | Chicken (shell eggs) | 2010 | USA | 1939 b | CDC 2020 d |
Enteritidis Virchow | Chicken | 2010 (from 2007) | Brazil | >260 | [11] |
Enteritidis Virchow | Chicken | 2010 | Taiwan | >1000 | [12] |
Stanley | Turkey (meat) | 2011–2013 | EU | 710 | [13] |
Heidelberg | Chicken (meat) | 2011 | USA | 190 | CDC 2020 d |
Infantis Newport Lille | Chicks, ducklings (live) | 2012 | USA | 195 | CDC 2020 d |
Heidelberg | Chicken (meat) | 2013 | USA | 634 | CDC 2020 d |
Typhimurium | Chicks, ducklings (live) | 2013 | USA | 356 | CDC 2020 d |
Enteritidis | Chicken (eggs) | 2014 | EU | >400 | [14] |
Multiple NTS c | Chicks, ducklings (live) | 2014 | USA | 363 | CDC 2020 d |
Multiple NTS | Chicks, ducklings (live) | 2015 | USA | 252 | CDC 2020 d |
Multiple NTS | Chicks, ducklings (live) | 2016 | USA | 895 | CDC 2020 d |
Typhimurium | Chicken (egg) | 2015–2016 | Australia | 272 | [15] |
Enteritidis | Chicken (eggs) | 2016–present | EU | 1656 | ECDC 2020 e |
Multiple NTS | Chicks, ducklings (live) | 2017 | USA | 1120 | CDC 2020 d |
Typhimurium | Chicken (salad) | 2018 | USA | 265 | CDC 2020 d |
Reading | Turkey | 2018 | USA | 358 | CDC 2020 d |
Enteritidis | Chicken (processed meat) | 2017–2019 | Canada | 584 | Public Health Service 2020 f |
Enteritidis | Chicks, ducklings (live) | 2019 | USA | 1134 | CDC 2020 d |
Salmonella Serovar | Genetic/Phenotypic Signatures | Role Related to Virulence in Chicken or Human | References |
---|---|---|---|
Kentucky (SKn) | (1) Colicin production (pColV) (2) Salmonella genomic island 1 (SGI1) (3) RpoS regulated gene cluster: csg (curli), prpBCDE (propionate catabolism) (4) Lack of Saf and Sef fimbria (5) Additional iron uptake carried in pColV; siderophores- aerobactin & salmochelin, sit operon (Mn2+, Fe2+ uptake) | (1) Increased colonization in chicken gut (2) Multidrug resistant (MDR) including 3rd generation cephalosporin, ciprofloxacin resistant *, (3) Upregulated in chicken cecal explants (4) Decreased invasiveness in humans compared to other NTS (5) NDA (no data available) | [54,55,56] |
Heidelberg (SHb) | (6) Type IV secretion (T4SS) (7) SopE (T3SS1 effector) duplication in the chromosome (8) Salmonella atypical fimbria (safABCD) (9) Additional iron uptake carried in pColV; siderophore-aerobactin | (6) Dissemination of antibiotics resistance and efficient survival in macrophages (7) Invasion into epithelial cells and induce inflammation (8) Only presented in the outbreak strain linked to human salmonellosis. (9) NDA | [55,57,58] |
Typhimurium (STm) | (10) Salmonella genomic island 1 (SGI1) (11) Salmonella genomic island 4 (SGI4) (12) Plasmid encoded factors; mig-5, rck, spv (Salmonella plasmid virulence), pef , (13) Additional iron uptake in pColV; aerobactin, salmochelin sit operon (Mn2+, Fe2+) | (10) Sequence type DT104 showed Increased egg contamination compared to SEn phage type 4, contains ACSSuT # drug-resistant phenotype (11) Heavy metal resistant in DT104 (12) colonization in chicken gut, systemic spread (13) NDA | [59,60,61,62] |
Typhimurium mono phasic variant (STmv) (DT193/DT120) | (14) Phase 2 flagellin not expressed (fljBA operon) (15) SGI-4 (16) Lack of Salmonella plasmid virulence locus, (17) Lack of Gifsy prophages | (14) Predicted to be an adaptation related to the expansion of reservoir host (15) resistant to heavy metals copper and zinc (16) less invasive in humans (17) NDA | [59,63,64] |
Enteritidis (SEn) | (18) pSLA5 plasmid (19) Plasmid encoded factors; mig-5, rck, spv (Salmonella plasmid virulence), pef (20) Peg fimbria | (18) Associated with recent outbreaks in the EU. (19) Colonization in chicken gut, systemic spread (20) Generally unique to Enteritidis. Facilitates cecal colonization in chickens | [65,66,67,68] |
Virchow (SVr) | (21) Salmonella Typhi colonization factor: TcfA (22) Novel SopE effector | (21) TcfA fimbriae provides tissue tropism in invasion into human cells. Role in chickens unknown (22) Associated with invasive nature of SVQ1 strain linked to outbreaks in Australia | [53,69] |
Montevideo (SMv) | (23) Typhoid-associated virulence factors; TcfA fimbria, cytolethal toxin B etc. | (23) Predicted to increase tissue tropism and invasions in humans. Role in chickens unknown | [53,70] |
Infantis (SIn) | (24) Plasmid-encoded factors;(pESI like);
| (24) Associated in human outbreaks. Also, plasmid-encoded fimbria were contributed a colonization in the gastrointestinal tract of chicks | [71,72,73,74] |
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Wellawa, D.H.; Allan, B.; White, A.P.; Köster, W. Iron-Uptake Systems of Chicken-Associated Salmonella Serovars and Their Role in Colonizing the Avian Host. Microorganisms 2020, 8, 1203. https://doi.org/10.3390/microorganisms8081203
Wellawa DH, Allan B, White AP, Köster W. Iron-Uptake Systems of Chicken-Associated Salmonella Serovars and Their Role in Colonizing the Avian Host. Microorganisms. 2020; 8(8):1203. https://doi.org/10.3390/microorganisms8081203
Chicago/Turabian StyleWellawa, Dinesh H., Brenda Allan, Aaron P. White, and Wolfgang Köster. 2020. "Iron-Uptake Systems of Chicken-Associated Salmonella Serovars and Their Role in Colonizing the Avian Host" Microorganisms 8, no. 8: 1203. https://doi.org/10.3390/microorganisms8081203
APA StyleWellawa, D. H., Allan, B., White, A. P., & Köster, W. (2020). Iron-Uptake Systems of Chicken-Associated Salmonella Serovars and Their Role in Colonizing the Avian Host. Microorganisms, 8(8), 1203. https://doi.org/10.3390/microorganisms8081203