The Qrc Membrane Complex, Related to the Alternative Complex III, Is a Menaquinone Reductase Involved in Sulfate Respiration

Abstract

Biological sulfate reduction is a process with high environmental significance due to its major contribution to the carbon and sulfur cycles in anaerobic environments. However, the respiratory chain of sulfate-reducing bacteria is still poorly understood. Here we describe a new respiratory complex that was isolated as a major protein present in the membranes of Desulfovibrio vulgaris Hildenborough. The complex, which was named Qrc, is the first representative of a new family of redox complexes. It has three subunits related to the complex iron-sulfur molybdoenzyme family and a multiheme cytochrome c and binds six hemes c, one Respiratory chains rely on membrane-bound protein complexes to perform a stepwise transduction of the free energy of redox reactions into an electrochemical potential difference across the membrane that drives the synthesis of ATP. In aerobic eukaryotic organisms, a fixed and mostly linear respiratory chain is present, in contrast to bacteria and archaea whose flexible and usually highly branched respiratory chains reflect their ability to use an array of different electrons donors and acceptors (1). This flexibility enables prokaryotes to explore virtually every possible energy source and oxidant pairs that can provide energy to sustain life and, thus, colonize multiple habitats on earth, including the most extreme environments. In addition, the recycling of elements provided by bacterial energy metabolism is a crucial component for the maintenance of life in our planet (2). The study of bacterial respiratory complexes (BRCs) 3 has highlighted the diversity of mechanisms by which energy conservation can be achieved (3, 4). BRCs usually have simpler compositions than their eukaryotic counterparts and are, therefore, useful models to understand the molecular mechanisms involved in those processes. Furthermore, bacteria contain many unique BRCs whose architectures have highly modular characters, with dif-

Metabolism of H2 by Desulfovibrio alaskensis G20 during syntrophic growth on lactate

“…The purified Qrc was shown to be reduced by H 2 (or formate) in the presence of the TpIc 3 and hydrogenase (or formate dehydrogenase). The purified complex also served to transfer electrons from the TpIc 3 to menaquinone, of which the latter was suggested to provide electrons to another membrane complex (perhaps Qmo), which would then transfer the electrons to a cytoplasmic protein for reduction of sulfate (Venceslau et al, 2010). Ultimately, the cycling of menaquinone provides this system with the capability to generate a PMF.…”

“…The reasons are not clear, although that insertion may be less stable than those described here. The orthologue of the G20 Qrc was recently purified from D. vulgaris Hildenborough and was shown to be composed of four subunits present at a 1 : 1 : 1 : 1 ratio, forming a transmembrane complex with periplasmic components (Venceslau et al, 2010). The purified Qrc was shown to be reduced by H 2 (or formate) in the presence of the TpIc 3 and hydrogenase (or formate dehydrogenase).…”

“…cycA encodes the TpIc 3 , which has been suggested to act as electron acceptor for periplasmic hydrogenases and formate dehydrogenases in Desulfovibrio (Heidelberg et al, 2004;LeGall & Fauque, 1988;Matias et al, 2005) and to interact with and mediate electron transfer from the Fe hydrogenase to a transmembrane high-molecular-mass cytochrome c (Hmc) (Pereira et al, 1998). Based on pureculture experiments, TpIc 3 and QrcABCD were proposed to interact to shuttle electrons from H 2 oxidation in the periplasm to the menaquinone pool in the inner membrane, after which electrons are ultimately used for sulfate reduction in the cytoplasm (Li et al, 2009;Venceslau et al, 2010). Another group has generated a mutation in the same cycA gene by plasmid insertion.…”

“…These genes encode a periplasm-facing integral membrane protein with clear homology to alternative complex III (Li et al, 2009;Venceslau et al, 2010). This complex was described as Mop in a previous publication (Li et al, 2009), but the complex has been recently characterized biochemically from D. vulgaris and renamed Qrc (Venceslau et al, 2010).…”

“…This complex was described as Mop in a previous publication (Li et al, 2009), but the complex has been recently characterized biochemically from D. vulgaris and renamed Qrc (Venceslau et al, 2010). The other mutant had a lesion in Dde_3182 (cycA), predicted to encode the TpIc 3 (Table 1), a single-subunit protein.…”