Respiration of Escherichia coli in the mouse intestine.
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.
Jones
Shari A
SA
Advanced Center for Genome Technology, University of Oklahoma, Norman, Oklahoma 73019, USA.
Chowdhury
Fatema Z
FZ
Fabich
Andrew J
AJ
Anderson
April
A
Schreiner
Darrel M
DM
House
Anetra L
AL
Autieri
Steven M
SM
Leatham
Mary P
MP
Lins
Jeremy J
JJ
Jorgensen
Mathias
M
Cohen
Paul S
PS
Conway
Tyrrell
T
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
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
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