title: Respiration of Escherichia coli in the mouse intestine.
abstract: Mammals are aerobes that harbor an intestinal ecosystem dominated by large numbers of anaerobic microorganisms. However, the role of oxygen in the intestinal ecosystem is largely unexplored. We used systematic mutational analysis to determine the role of respiratory metabolism in the streptomycin-treated mouse model of intestinal colonization. Here we provide evidence that aerobic respiration is required for commensal and pathogenic Escherichia coli to colonize mice. Our results showed that mutants lacking ATP synthase, which is required for all respiratory energy-conserving metabolism, were eliminated by competition with respiratory-competent wild-type strains. Mutants lacking the high-affinity cytochrome bd oxidase, which is used when oxygen tensions are low, also failed to colonize. However, the low-affinity cytochrome bo(3) oxidase, which is used when oxygen tension is high, was found not to be necessary for colonization. Mutants lacking either nitrate reductase or fumarate reductase also had major colonization defects. The results showed that the entire E. coli population was dependent on both microaerobic and anaerobic respiration, consistent with the hypothesis that the E. coli niche is alternately microaerobic and anaerobic, rather than static. The results indicate that success of the facultative anaerobes in the intestine depends on their respiratory flexibility. Despite competition for relatively scarce carbon sources, the energy efficiency provided by respiration may contribute to the widespread distribution (i.e., success) of E. coli strains as commensal inhabitants of the mammalian intestine.
authors: Advanced Center for Genome Technology, University of Oklahoma, Norman, Oklahoma 73019, USA.
authors: Shari A
authors: SA
authors: Jones
authors: Fatema Z
authors: FZ
authors: Chowdhury
authors: Andrew J
authors: AJ
authors: Fabich
authors: April
authors: A
authors: Anderson
authors: Darrel M
authors: DM
authors: Schreiner
authors: Anetra L
authors: AL
authors: House
authors: Steven M
authors: SM
authors: Autieri
authors: Mary P
authors: MP
authors: Leatham
authors: Jeremy J
authors: JJ
authors: Lins
authors: Mathias
authors: M
authors: Jorgensen
authors: Paul S
authors: PS
authors: Cohen
authors: Tyrrell
authors: T
authors: Conway
mesh_terms: D000332:Aerobiosis; D000693:Anaerobiosis; D000818:Animals; D025243:Bacterial Proton-Translocating ATPases / Q000235:genetics / Q000502:physiology; D015169:Colony Count, Microbial; D003573:Cytochrome b Group; D003580:Cytochromes / Q000235:genetics / Q000502:physiology; D045222:Electron Transport Chain Complex Proteins / Q000235:genetics / Q000502:physiology; D004926:Escherichia coli / Q000201:enzymology / Q000254:growth & development* / Q000378:metabolism*; D029968:Escherichia coli Proteins / Q000235:genetics / Q000502:physiology; D005243:Feces / Q000382:microbiology; D007422:Intestines / Q000382:microbiology*; D008297:Male; D051379:Mice; D008954:Models, Biological; D050901:Nitrate Reductase / Q000235:genetics / Q000502:physiology; D010088:Oxidoreductases / Q000235:genetics / Q000502:physiology; D010101:Oxygen Consumption; D013385:Succinate Dehydrogenase / Q000235:genetics / Q000502:physiology
chemical_list: D003573:Cytochrome b Group; D003580:Cytochromes; D045222:Electron Transport Chain Complex Proteins; D029968:Escherichia coli Proteins; C083850:cytochrome bo3, E coli; D010088:Oxidoreductases; D013385:Succinate Dehydrogenase; D050901:Nitrate Reductase; C040077:cytochrome bd terminal oxidase complex, E coli; D025243:Bacterial Proton-Translocating ATPases
references: J Bacteriol. 1985 Jan;161(1):123-7
references: 2981797
references: J Bacteriol. 2003 Sep;185(17):5076-85
references: 12923080
references: Infect Immun. 2005 Dec;73(12):8039-49
references: 16299298
references: J Bacteriol. 1996 Feb;178(4):1094-8
references: 8576043
references: Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15629-34
references: 16227431
references: Nature. 1961 Jul 8;191:144-8
references: 13771349
references: Biochem Soc Trans. 2006 Feb;34(Pt 1):104-7
references: 16417494
references: Annu Rev Microbiol. 1977;31:107-33
references: 334036
references: Infect Immun. 1988 May;56(5):1030-5
references: 3281898
references: J Bacteriol. 2002 Mar;184(5):1314-23
references: 11844760
references: Infect Immun. 1990 Aug;58(8):2438-45
references: 2196227
references: J Bacteriol. 1996 Aug;178(15):4515-21
references: 8755879
references: Science. 2005 Jun 10;308(5728):1635-8
references: 15831718
references: J Bacteriol. 1983 Jun;154(3):1269-75
references: 6304009
references: Mol Microbiol. 1993 Aug;9(3):425-34
references: 8412692
references: Bioessays. 2003 Oct;25(10):926-9
references: 14505359
references: Nature. 2007 Jan 4;445(7123):8-9
references: 17203031
references: Proc Natl Acad Sci U S A. 2004 May 11;101(19):7427-32
references: 15123798
references: J Bacteriol. 1982 Aug;151(2):788-99
references: 7047497
references: FEMS Microbiol Lett. 1996 Feb 1;136(1):1-11
references: 8919448
references: J Bacteriol. 2003 Jan;185(1):204-9
references: 12486057
references: Nature. 2004 Jan 29;427(6973):441-4
references: 14749831
references: Annu Rev Med. 1980;31:127-37
references: 6772089
references: Science. 2001 Jun 22;292(5525):2314-6
references: 11423658
references: Nat Rev Microbiol. 2004 Feb;2(2):123-40
references: 15040260
references: Biochem J. 1991 Dec 15;280 ( Pt 3):599-608
references: 1764023
references: J Biol Chem. 2005 Sep 16;280(37):32254-61
references: 16040611
references: FEMS Microbiol Lett. 1994 Apr 1;117(2):217-23
references: 8181727
references: Infect Immun. 2003 Apr;71(4):2142-52
references: 12654836
references: Proc Natl Acad Sci U S A. 1988 Mar;85(6):1888-92
references: 2964639
references: EcoSal Plus. 2004 Dec;1(1):
references: 26443354
references: Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4586-91
references: 10200306
references: Infect Immun. 1993 Dec;61(12):5029-34
references: 8225579
references: J Bacteriol. 1999 Sep;181(17):5303-8
references: 10464201
references: J Bacteriol. 1973 May;114(2):563-70
references: 4574693
references: J Bacteriol. 1999 Feb;181(4):1229-37
references: 9973350
references: Infect Immun. 2004 Mar;72(3):1666-76
references: 14977974
references: FEMS Microbiol Rev. 1998 Dec;22(5):341-52
references: 9990723
references: Mol Microbiol. 1999 Nov;34(4):756-66
references: 10564515
references: Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
references: 10829079
references: Science. 2005 Mar 25;307(5717):1915-20
references: 15790844
references: J Bacteriol. 2003 Oct;185(19):5862-70
references: 13129959
references: J Clin Microbiol. 1993 Oct;31(10):2799-801
references: 8253989
references: J Bacteriol. 1998 Jul;180(14):3495-502
references: 9657988
references: Biochem J. 1978 Mar 15;170(3):593-8
references: 148275