A conserved histidine in cytochrome c maturation permease CcmB of Shewanella putrefaciens is required for anaerobic growth below a threshold standard redox potential.
Shewanella putrefaciens strain 200 respires a wide range of compounds as terminal electron acceptor. The respiratory versatility of Shewanella is attributed in part to a set of c-type cytochromes with widely varying midpoint redox potentials (E'(0)). A point mutant of S. putrefaciens, originally designated Urr14 and here renamed CCMB1, was found to grow at wild-type rates on electron acceptors with high E'0 [O2, NO3-, Fe(III) citrate, MnO2, and Mn(III) pyrophosphate] yet was severely impaired for growth on electron acceptors with low E'0 [NO2-, U(VI), dimethyl sulfoxide, TMAO (trimethylamine N-oxide), fumarate, gamma-FeOOH, SO3(2-), and S2O3(2-)]. Genetic complementation and nucleotide sequence analyses indicated that the CCMB1 respiratory mutant phenotype was due to mutation of a conserved histidine residue (H108Y) in a protein that displayed high homology to Escherichia coli CcmB, the permease subunit of an ABC transporter involved in cytochrome c maturation. Although CCMB1 retained the ability to grow on electron acceptors with high E'(0), the cytochrome content of CCMB1 was <10% of that of the wild-type strain. Periplasmic extracts of CCMB1 contained slightly greater concentrations of the thiol functional group (-SH) than did the wild-type strain, an indication that the E(h) of the CCMB1 periplasm was abnormally low. A ccmB deletion mutant was unable to respire anaerobically on any electron acceptor, yet retained aerobic respiratory capability. These results suggest that the mutation of a conserved histidine residue (H108) in CCMB1 alters the redox homeostasis of the periplasm during anaerobic growth on electron acceptors with low (but not high) E'0. This is the first report of the effects of Ccm deficiencies on bacterial respiration of electron acceptors whose E'0 nearly span the entire redox continuum.
Dale
Jason R
JR
School of Biology, Georgia Institute of Technology, 310 Ferst Drive, Atlanta, GA 30332-0230, USA.
Wade
Roy
R
Dichristina
Thomas J
TJ
D018528:ATP-Binding Cassette Transporters / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D000595:Amino Acid Sequence; D000693:Anaerobiosis; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D045304:Cytochromes c / Q000378:metabolism*; D017353:Gene Deletion; D005816:Genetic Complementation Test; D006639:Histidine / Q000235:genetics; D008969:Molecular Sequence Data; D009154:Mutation; D010084:Oxidation-Reduction; D016415:Sequence Alignment; D020614:Shewanella putrefaciens / Q000235:genetics / Q000378:metabolism*; D013438:Sulfhydryl Compounds / Q000378:metabolism
D018528:ATP-Binding Cassette Transporters; D001426:Bacterial Proteins; D013438:Sulfhydryl Compounds; D006639:Histidine; D045304:Cytochromes c