Salmonella "sops" up a preferred electron receptor in the inflamed intestine - PubMed (original) (raw)
Salmonella "sops" up a preferred electron receptor in the inflamed intestine
James B Bliska et al. mBio. 2012.
Abstract
The microbiota of the mammalian intestinal tract represents a formidable barrier to colonization by pathogens. To overcome this resistance to colonization, bacterial pathogens use virulence factors to induce intestinal inflammation, which liberates nutrients for selective use by the infecting microbe. Studies of Salmonella enterica serovar Typhimurium (S. Typhimurium) infection in a streptomycin-treated mouse colitis model show how virulence factor-induced inflammation can produce nutrients used selectively by the pathogen. Type III secreted effectors of invading S. Typhimurium induce inflammation in the intestine (epithelial cells and lamina propria macrophages) that causes changes in the composition of the lumen. For example, neutrophils entering the intestine produce superoxide, resulting in production of tetrathionate, which S. Typhimurium in the lumen uses as an electron acceptor for anaerobic respiration. In their recent study, Lopez et al. demonstrate that S. Typhimurium strains that are lysogenized with a phage encoding type III effector SopE induce the host to produce nitric oxide synthetase (iNOS) in the intestine (C. A. Lopez et al., mBio 3:e00143-12, 2012). Nitric oxide is converted to a highly favorable electron acceptor, nitrate. As a result, growth of sopE(+) S. Typhimurium in the intestine lumen is boosted by nitrate respiration. This is a striking example of how acquisition of a virulence factor by horizontal gene transfer can increase the metabolic fitness of a pathogen. Interestingly, survival of the invading bacteria is probably decreased as a result of the SopE-induced immune response, and yet the S. Typhimurium bacteria that multiply in the lumen of the intestine can efficiently disseminate to another host, ensuring success for the pathogen.
Similar articles
- Phage-mediated acquisition of a type III secreted effector protein boosts growth of salmonella by nitrate respiration.
Lopez CA, Winter SE, Rivera-Chávez F, Xavier MN, Poon V, Nuccio SP, Tsolis RM, Bäumler AJ. Lopez CA, et al. mBio. 2012 Jun 12;3(3):e00143-12. doi: 10.1128/mBio.00143-12. Print 2012. mBio. 2012. PMID: 22691391 Free PMC article. - Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota.
Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, Sterzenbach T, Tsolis RM, Roth JR, Bäumler AJ. Thiennimitr P, et al. Proc Natl Acad Sci U S A. 2011 Oct 18;108(42):17480-5. doi: 10.1073/pnas.1107857108. Epub 2011 Oct 3. Proc Natl Acad Sci U S A. 2011. PMID: 21969563 Free PMC article. - Respiration of Microbiota-Derived 1,2-propanediol Drives Salmonella Expansion during Colitis.
Faber F, Thiennimitr P, Spiga L, Byndloss MX, Litvak Y, Lawhon S, Andrews-Polymenis HL, Winter SE, Bäumler AJ. Faber F, et al. PLoS Pathog. 2017 Jan 5;13(1):e1006129. doi: 10.1371/journal.ppat.1006129. eCollection 2017 Jan. PLoS Pathog. 2017. PMID: 28056091 Free PMC article. - Salmonella Typhimurium metabolism affects virulence in the host - A mini-review.
Herrero-Fresno A, Olsen JE. Herrero-Fresno A, et al. Food Microbiol. 2018 May;71:98-110. doi: 10.1016/j.fm.2017.04.016. Epub 2017 Apr 28. Food Microbiol. 2018. PMID: 29366476 Review. - Basic Processes in _Salmonella_-Host Interactions: Within-Host Evolution and the Transmission of the Virulent Genotype.
Diard M, Hardt WD. Diard M, et al. Microbiol Spectr. 2017 Sep;5(5):10.1128/microbiolspec.mtbp-0012-2016. doi: 10.1128/microbiolspec.MTBP-0012-2016. Microbiol Spectr. 2017. PMID: 28884670 Free PMC article. Review.
Cited by
- Multi-omics analysis reveals regime shifts in the gastrointestinal ecosystem in chickens following anticoccidial vaccination and Eimeria tenella challenge.
Liu P-Y, Liaw J, Soutter F, Ortiz JJ, Tomley FM, Werling D, Gundogdu O, Blake DP, Xia D. Liu P-Y, et al. mSystems. 2024 Oct 22;9(10):e0094724. doi: 10.1128/msystems.00947-24. Epub 2024 Sep 17. mSystems. 2024. PMID: 39287379 Free PMC article. - Salmonella Pathogenicity Island 1 (SPI-1) and Its Complex Regulatory Network.
Lou L, Zhang P, Piao R, Wang Y. Lou L, et al. Front Cell Infect Microbiol. 2019 Jul 31;9:270. doi: 10.3389/fcimb.2019.00270. eCollection 2019. Front Cell Infect Microbiol. 2019. PMID: 31428589 Free PMC article. Review. - A tale of two sites: how inflammation can reshape the microbiomes of the gut and lungs.
Scales BS, Dickson RP, Huffnagle GB. Scales BS, et al. J Leukoc Biol. 2016 Nov;100(5):943-950. doi: 10.1189/jlb.3MR0316-106R. Epub 2016 Jun 30. J Leukoc Biol. 2016. PMID: 27365534 Free PMC article. Review. - A Novel, Molybdenum-Containing Methionine Sulfoxide Reductase Supports Survival of Haemophilus influenzae in an In vivo Model of Infection.
Dhouib R, Othman DS, Lin V, Lai XJ, Wijesinghe HG, Essilfie AT, Davis A, Nasreen M, Bernhardt PV, Hansbro PM, McEwan AG, Kappler U. Dhouib R, et al. Front Microbiol. 2016 Nov 14;7:1743. doi: 10.3389/fmicb.2016.01743. eCollection 2016. Front Microbiol. 2016. PMID: 27933034 Free PMC article. - The respiratory tract microbiome and lung inflammation: a two-way street.
Huffnagle GB, Dickson RP, Lukacs NW. Huffnagle GB, et al. Mucosal Immunol. 2017 Mar;10(2):299-306. doi: 10.1038/mi.2016.108. Epub 2016 Dec 14. Mucosal Immunol. 2017. PMID: 27966551 Free PMC article. Review.
References
- Stecher B, et al. 2008. The role of microbiota in infectious disease. Trends Microbiol. 16:107–114 - PubMed
- Lupp C, et al. 2007. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2:119–129 - PubMed
- Ackermann M, et al. 2008. Self-destructive cooperation mediated by phenotypic noise. Nature 454:987–990 - PubMed
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Research Materials