Biogenesis of Cytochrome c Complexes: From Insertion of Redox Cofactors to Assembly of Different Subunits

  • Bahia Khalfaoui-Hassani
  • Andreia F. Verissimo
  • Namita P. Shroff
  • Seda Ekici
  • Petru-Iulian Trasnea
  • Marcel Utz
  • Hans-Georg Koch
  • Fevzi DaldalEmail author
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 41)


Cytochromes (cyts) are ubiquitous heme containing proteins that are key components of energy transduction pathways. They participate in a wide variety of electron transfer reactions, which are essential for cellular processes responsible for chemical energy (ATP) production. The cbb3-type cyt c oxidase (cbb3-Cox) provides an excellent model to study biogenesis of membrane-integral, oligomeric cyt c complexes. Its subunits contain three hemes c, two hemes b and a copper (CuB) atom as cofactors that use distinct insertion processes. In cyts c, heme b is covalently ligated (referred to as heme c) via a complex maturation process that involves in some species up to nine components (Ccm-System I). In addition to the cyts c, many cyt c containing complexes carry other cofactors, and insertion of these cofactors requires additional biogenesis components besides the Ccm-system I. In the case of cbb3-Cox, the mechanisms underlying incorporation of hemes b into the catalytic subunit are not well understood. However, remarkable progress was achieved recently on how the single CuB atom at the catalytic heart of this heme-copper oxidase is acquired. Finally, insertion of the cofactors must be temporally and spatially coordinated with the assembly of the subunits in order to yield a functional cbb3-Cox enzyme. In this chapter, we discuss the biogenesis of cbb3-Cox from the insertion of its catalytic heme-copper (CuB) center and maturation of its c-type cyts to the assembly of its mature subunits, mainly focusing on studies carried out with the anoxygenic phototrophic bacterium Rhodobacter capsulatus.


Cytochrome c cbb3 cytochrome c oxidase Cytochrome c biogenesis Copper biogenesis Rhodobacter capsulatus 



Cytochrome c maturation system I


Cytochrome c oxidase




Heme-copper terminal oxidase


Heme handling protein


Heavy metal binding domain


Major facilitator superfamily




Quinol (hydroquinone) oxidase





This work is supported by grants from the NIH GM 38237 and DOE, Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences DE-FG02-91ER20052 to FD, and by grants from the Deutsche Forschungs Gemeinschaft (GRK1487) and the German-French PhD College (Membrane Proteins and Biological Membranes) to HGK.


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Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Bahia Khalfaoui-Hassani
    • 1
  • Andreia F. Verissimo
    • 1
  • Namita P. Shroff
    • 1
  • Seda Ekici
    • 1
  • Petru-Iulian Trasnea
    • 2
  • Marcel Utz
    • 2
  • Hans-Georg Koch
    • 2
  • Fevzi Daldal
    • 1
    Email author
  1. 1.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA
  2. 2.Institut für Biochemie und MolekularbiologieAlbert-Ludwigs Universität FreiburgFreiburgGermany

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