title: Salmonella uses energy taxis to benefit from intestinal inflammation.
abstract: Chemotaxis enhances the fitness of Salmonella enterica serotype Typhimurium (S. Typhimurium) during colitis. However, the chemotaxis receptors conferring this fitness advantage and their cognate signals generated during inflammation remain unknown. Here we identify respiratory electron acceptors that are generated in the intestinal lumen as by-products of the host inflammatory response as in vivo signals for methyl-accepting chemotaxis proteins (MCPs). Three MCPs, including Trg, Tsr and Aer, enhanced the fitness of S. Typhimurium in a mouse colitis model. Aer mediated chemotaxis towards electron acceptors (energy taxis) in vitro and required tetrathionate respiration to confer a fitness advantage in vivo. Tsr mediated energy taxis towards nitrate but not towards tetrathionate in vitro and required nitrate respiration to confer a fitness advantage in vivo. These data suggest that the energy taxis receptors Tsr and Aer respond to distinct in vivo signals to confer a fitness advantage upon S. Typhimurium during inflammation by enabling this facultative anaerobic pathogen to seek out favorable spatial niches containing host-derived electron acceptors that boost its luminal growth.
authors: Department of Medical Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, California, United States of America.
authors: Fabian
authors: F
authors: Rivera-Chávez
authors: Sebastian E
authors: SE
authors: Winter
authors: Christopher A
authors: CA
authors: Lopez
authors: Mariana N
authors: MN
authors: Xavier
authors: Maria G
authors: MG
authors: Winter
authors: Sean-Paul
authors: SP
authors: Nuccio
authors: Joseph M
authors: JM
authors: Russell
authors: Richard C
authors: RC
authors: Laughlin
authors: Sara D
authors: SD
authors: Lawhon
authors: Torsten
authors: T
authors: Sterzenbach
authors: Charles L
authors: CL
authors: Bevins
authors: Renée M
authors: RM
authors: Tsolis
authors: Rasika
authors: R
authors: Harshey
authors: L Garry
authors: LG
authors: Adams
authors: Andreas J
authors: AJ
authors: Bäumler
mesh_terms: D000818:Animals; D001426:Bacterial Proteins / Q000378:metabolism*; D002352:Carrier Proteins / Q000378:metabolism; D002633:Chemotaxis; D003092:Colitis / Q000276:immunology / Q000382:microbiology*; D004579:Electron Transport; D004734:Energy Metabolism; D005260:Female; D007249:Inflammation; D007413:Intestinal Mucosa / Q000378:metabolism; D007422:Intestines / Q000382:microbiology; D008565:Membrane Proteins / Q000378:metabolism*; D000072236:Methyl-Accepting Chemotaxis Proteins; D051379:Mice; D008810:Mice, Inbred C57BL; D008808:Mice, Inbred CBA; D009504:Neutrophils / Q000276:immunology; D009566:Nitrates / Q000378:metabolism; D017382:Reactive Oxygen Species / Q000378:metabolism; D011956:Receptors, Cell Surface / Q000378:metabolism; D012481:Salmonella Infections, Animal / Q000276:immunology / Q000382:microbiology*; D012486:Salmonella typhimurium / Q000276:immunology / Q000472:pathogenicity* / Q000502:physiology; D013776:Tetrathionic Acid / Q000378:metabolism
chemical_list: D001426:Bacterial Proteins; D002352:Carrier Proteins; D008565:Membrane Proteins; D000072236:Methyl-Accepting Chemotaxis Proteins; D009566:Nitrates; D017382:Reactive Oxygen Species; D011956:Receptors, Cell Surface; C057635:Tsr protein, Bacteria; D013776:Tetrathionic Acid
references: Cell Host Microbe. 2009 May 8;5(5):476-86
references: 19454351
references: Infect Immun. 2001 Jul;69(7):4610-7
references: 11402005
references: Nature. 2010 Sep 23;467(7314):426-9
references: 20864996
references: Infect Immun. 2011 May;79(5):1806-14
references: 21343352
references: Mol Cell. 2002 Nov;10(5):1033-43
references: 12453412
references: Science. 2013 Feb 8;339(6120):708-11
references: 23393266
references: J Biosci Bioeng. 2004;97(3):184-90
references: 16233612
references: Gut Microbes. 2010 Jan;1(1):30-41
references: 21327114
references: Proc Natl Acad Sci U S A. 2000 May 23;97(11):5830-5
references: 10811894
references: Cell Microbiol. 2008 May;10(5):1166-80
references: 18241212
references: Antonie Van Leeuwenhoek. 2009 Feb;95(2):149-58
references: 19130287
references: Infect Immun. 2008 Mar;76(3):907-15
references: 18160481
references: Infect Immun. 1999 Sep;67(9):4879-85
references: 10456944
references: J Clin Invest. 1999 Oct;104(8):1107-14
references: 10525049
references: Methods Enzymol. 1993;217:270-9
references: 8474334
references: Antibiot Chemother (1971). 1974;19:12-20
references: 4618737
references: Proc Natl Acad Sci U S A. 1990 Jun;87(12):4645-9
references: 2162051
references: Gene. 1993 Dec 22;136(1-2):271-5
references: 8294016
references: FEMS Microbiol Lett. 2007 Nov;276(2):193-201
references: 17956426
references: Proc Natl Acad Sci U S A. 1979 Jan;76(1):260-4
references: 370826
references: PLoS Biol. 2007 Oct;5(10):2177-89
references: 17760501
references: Infect Immun. 2009 May;77(5):1904-16
references: 19237529
references: Cell. 1979 Mar;16(3):617-25
references: 378395
references: Microbiology (Reading). 2003 Sep;149(Pt 9):2661-2667
references: 12949190
references: Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
references: 10829079
references: Biotechniques. 1995 Aug;19(2):186-8
references: 8527132
references: Mol Gen Genet. 1979 Mar 20;171(2):193-203
references: 375029
references: Infect Immun. 2004 Jul;72(7):4138-50
references: 15213159
references: Gene. 1991 Apr;100:195-9
references: 2055470
references: Infect Immun. 2003 May;71(5):2839-58
references: 12704158
references: Proc Natl Acad Sci U S A. 2006 Feb 7;103(6):1834-9
references: 16446425
references: J Gen Microbiol. 1972 Jun;71(1):133-9
references: 5039254
references: Infect Immun. 2003 Feb;71(2):629-40
references: 12540539
references: Mol Microbiol. 2006 Jun;60(6):1590-602
references: 16796690
references: Arch Microbiol. 2010 Jul;192(7):507-20
references: 20411245
references: Proc Natl Acad Sci U S A. 2011 Oct 18;108(42):17480-5
references: 21969563
references: Mol Microbiol. 2006 Nov;62(3):823-37
references: 16995896
references: Nature. 2004 Dec 16;432(7019):917-21
references: 15531878
references: J Bacteriol. 1995 Mar;177(5):1383-7
references: 7868615
references: J Bacteriol. 1995 Mar;177(5):1357-66
references: 7868611
references: Infect Immun. 2008 Jan;76(1):403-16
references: 17967858
references: J Bacteriol. 2006 Nov;188(22):7981-4
references: 16980469
references: Mol Microbiol. 2001 Apr;40(1):214-24
references: 11298288
references: mBio. 2012 Jun 12;3(3):
references: 22691391
references: Bacteriol Rev. 1977 Mar;41(1):100-80
references: 860983
references: Mol Microbiol. 1999 Apr;32(2):275-87
references: 10231485
references: Biochem Pharmacol. 2001 Jul 15;62(2):255-9
references: 11389886
references: J Bacteriol. 2006 Mar;188(6):2233-43
references: 16513753