Absence of Thiol-Disulfide Oxidoreductase DsbA Impairs cbb3-Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus

Onder, Ozlem; Verissimo, Andreia F.; Khalfaoui-Hassani, Bahia; Peters, Annette; Koch, Hans-Georg; Daldal, Fevzi

doi:10.3389/fmicb.2017.02576

Absence of Thiol-Disulfide Oxidoreductase DsbA Impairs cbb₃-Type Cytochrome c Oxidase Biogenesis in Rhodobacter capsulatus

Journal Article · Thu Dec 21 00:00:00 EST 2017 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2017.02576· OSTI ID:1510498

Onder, Ozlem ^[1]; Verissimo, Andreia F. ^[2]; Khalfaoui-Hassani, Bahia ^[2]; Peters, Annette ^[3]; Koch, Hans-Georg ^[3]; Daldal, Fevzi ^[2]

Univ. of Pennsylvania, Philadelphia, PA (United States); Department of Biology, University of Pennsylvania, Philadelphia, PA (United States)
Univ. of Pennsylvania, Philadelphia, PA (United States)
Albert-Ludwigs-Universität Freiburg (Germany)

The thiol-disulfide oxidoreductase DsbA carries out oxidative folding of extra-cytoplasmic proteins by catalyzing the formation of intramolecular disulfide bonds. It has an important role in various cellular functions, including cell division. The purple non-sulfur bacterium Rhodobacter capsulatus mutants lacking DsbA show severe temperature-sensitive and medium-dependent respiratory growth defects. In the presence of oxygen, at normal growth temperature (35°C), DsbA^- mutants form colonies on minimal medium, but they do not grow on enriched medium where cells elongate and lyse. At lower temperatures (i.e., 25°C), cells lacking DsbA grow normally in both minimum and enriched media, however, they do not produce the cbb₃-type cytochrome c oxidase (cbb₃-Cox) on enriched medium. Availability of chemical oxidants (e.g., Cu²⁺ or a mixture of cysteine and cystine) in the medium becomes critical for growth and cbb₃-Cox production in the absence of DsbA. Indeed, addition of Cu²⁺ to the enriched medium suppresses, and conversely, omission of Cu²⁺ from the minimal medium induces, growth and cbb₃-Cox defects. Alleviation of these defects by addition of redox-active chemicals indicates that absence of DsbA perturbs cellular redox homeostasis required for the production of an active cbb₃-Cox, especially in enriched medium where bioavailable Cu²⁺ is scarce. This is the first report describing that DsbA activity is required for full respiratory capability of R. capsulatus, and in particular, for proper biogenesis of its cbb₃-Cox. We propose that absence of DsbA, besides impairing the maturation of the c-type cytochrome subunits, also affects the incorporation of Cu into the catalytic subunit of cbb₃-Cox. Defective high affinity Cu acquisition pathway, which includes the MFS-type Cu importer CcoA, and lower production of the c-type cytochrome subunits lead together to improper assembly and degradation of cbb₃-Cox.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Pennsylvania, Philadelphia, PA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: FG02-91ER20052

OSTI ID:: 1510498

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 8; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Rhodobacter capsulatus
cbb3-type cytochrome c oxidase biogenesis
copper homeostasis
disulﬁde bond formation
photosynthesis
respiration