Shewanella oneidensis cytochrome c maturation component CcmI is essential for heme attachment at the non-canonical motif of nitrite reductase NrfA.
Shewanella oneidensis is renowned for its respiratory versatility, which is largely due to abundant c-type cytochromes. Maturation of these proteins depends on a Ccm system encoded by genes in an unusual chromosomal arrangement, but the detailed mechanism is not understood. In this study, we identify SO0265 as CcmI, an apocytochrome c chaperone that is important and essential for maturation of c-type cytochromes with the canonical heme binding motif(s) (HBM; CX(2)CH) and nitrite reductase NrfA carrying a non-canonical CX(2)CK motif respectively. We show that the N-terminal transmembrane segment of CcmI, CcmI-1, is sufficient for maturation of the former but the entire protein is required for maturation of the latter. Although S. oneidensis possesses a heme lyase, SirEFG, dedicated for non-canonical HBMs, it is specific for SirA, a sulfite reductase with a CX(15)CH motif. By presenting evidence that the periplasmic portion of CcmI, CcmI-2, interacts with NrfA, we suggest that CcmI also takes the role of Escherichia coli NrfG for chaperoning apo-NrfA for maturation at CX(2)CK. Moreover, intact CcmI is required for maturation of NrfA, presumably by ensuring that heme attachment at canonical HBMs occurs before apoprotein degradation.
Institute of Microbiology and College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, 310058, China.
Huihui
H
Fu
Miao
M
Jin
Fen
F
Wan
Haichun
H
Gao
D020816:Amino Acid Motifs; D003574:Cytochrome c Group / Q000378:metabolism; D045304:Cytochromes c / Q000378:metabolism*; D004926:Escherichia coli / Q000235:genetics / Q000378:metabolism; D029968:Escherichia coli Proteins / Q000378:metabolism; D006418:Heme / Q000378:metabolism*; D008190:Lyases / Q000378:metabolism; D018832:Molecular Chaperones / Q000378:metabolism; D009572:Nitrite Reductases / Q000737:chemistry / Q000378:metabolism*; D050862:Oxidoreductases Acting on Sulfur Group Donors / Q000378:metabolism; D019897:Periplasm / Q000378:metabolism; D017434:Protein Structure, Tertiary; D020592:Shewanella / Q000235:genetics / Q000378:metabolism*
D003574:Cytochrome c Group; D029968:Escherichia coli Proteins; D018832:Molecular Chaperones; C528085:NrfG protein, E coli; D006418:Heme; D045304:Cytochromes c; D009572:Nitrite Reductases; D050862:Oxidoreductases Acting on Sulfur Group Donors; D008190:Lyases