The Tmc Complex from<i>Desulfovibrio vulgaris</i>Hildenborough Is Involved in Transmembrane Electron Transfer from Periplasmic Hydrogen Oxidation

Pereira, Patrícia M.; Teixeira, Miguel; Xavier, António V.; Louro, Ricardo O.; Pereira, Inês

doi:10.1021/bi0610294

Cited by 46 publications

(47 citation statements)

References 36 publications

(44 reference statements)

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“…A similar function is indicated for Hmc, which is required for the reoxidation of reduced ferredoxin generated by the activity of a pyruvate-ferredoxin oxidoreductase (Por; DVU3025) (30). This activity accounts for the defective growth of the mutant in coculture on both lactate and pyruvate, along with the reduced impact on respiratory growth previously attributed to compensation by alternative transmembrane electron carriers (e.g., the Tmc and Rnf complexes) apparently specific to sulfate reduction (6,29,45).…”

Section: Discussionmentioning

confidence: 65%

The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris

et al. 2009

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Interspecies hydrogen transfer between organisms producing and consuming hydrogen promotes the decomposition of organic matter in most anoxic environments. Although syntrophic coupling between hydrogen producers and consumers is a major feature of the carbon cycle, mechanisms for energy recovery at the extremely low free energies of reactions typical of these anaerobic communities have not been established. In this study, comparative transcriptional analysis of a model sulfate-reducing microbe, Desulfovibrio vulgaris Hildenborough, suggested the use of alternative electron transfer systems dependent on growth modality. During syntrophic growth on lactate with a hydrogenotrophic methanogen, numerous genes involved in electron transfer and energy generation were upregulated in D. vulgaris compared with their expression in sulfate-limited monocultures. In particular, genes coding for the putative membrane-bound Coo hydrogenase, two periplasmic hydrogenases (Hyd and Hyn), and the well-characterized high-molecular-weight cytochrome (Hmc) were among the most highly expressed and upregulated genes. Additionally, a predicted operon containing genes involved in lactate transport and oxidation exhibited upregulation, further suggesting an alternative pathway for electrons derived from lactate oxidation during syntrophic growth. Mutations in a subset of genes coding for Coo, Hmc, Hyd, and Hyn impaired or severely limited syntrophic growth but had little effect on growth via sulfate respiration. These results demonstrate that syntrophic growth and sulfate respiration use largely independent energy generation pathways and imply that to understand microbial processes that sustain nutrient cycling, lifestyles not captured in pure culture must be considered.Nutrient cycling on earth is determined primarily by cooperative interactions among microorganisms. The sharing of available energy within communities is particularly important in anaerobic systems, where limited energy is divided among highly specialized and metabolically interdependent populations (36,37,39). In the absence of exogenous electron acceptors such as sulfate and nitrate, the mineralization of organic matter in anoxic environments yields primarily carbon dioxide and methane, and this process is controlled by the synergistic activities of multiple anaerobic microbial populations. To better understand the metabolic basis and ecological significance of these syntrophic associations, we constructed an archetypical "community of two" by pairing Desulfovibrio vulgaris Hildenborough with a hydrogenotrophic methanogen, Methanococcus maripaludis strain S2.

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Section: Discussionmentioning

confidence: 65%

The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris

et al. 2009

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“…The only BRC that has been characterized so far from D. vulgaris is the Tmc complex (17). To further investigate the respiratory chain of this model organism, membrane protein complexes were analyzed by BN-PAGE after separation on ionexchange chromatography.…”

Section: Resultsmentioning

confidence: 99%

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

Venceslau¹,

Lino

Pereira

2010

Journal of Biological Chemistry

125

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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-

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“…The alternative bc 1 complex 'Qrc' was proposed recently to function in the reverse mode as a menaquinone reductase enzyme (Venceslau et al, 2010). The quinol oxidase bd uses menaquinol as reduced substrate, and the menaquinone pool can be replenished with electrons via membrane enzymes such as type II NADH dehydrogenase, and other menaquinone-reducing enzymes present in Desulfovibrio such as the Qrc (Venceslau et al, 2010) and Tmc complexes (Pereira et al, 2006) (Fig. 8).…”

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confidence: 99%

Oxygen reduction in the strict anaerobe Desulfovibrio vulgaris Hildenborough: characterization of two membrane-bound oxygen reductases

et al. 2011

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Although Desulfovibrio vulgaris Hildenborough (DvH) is a strictly anaerobic bacterium, it is able to consume oxygen in different cellular compartments, including extensive periplasmic O 2 reduction with hydrogen as electron donor. The genome of DvH revealed the presence of cydAB and cox genes, encoding a quinol oxidase bd and a cytochrome c oxidase, respectively. In the membranes of DvH, we detected both quinol oxygen reductase [inhibited by heptyl-hydroxyquinoline-N-oxide (HQNO)] and cytochrome c oxidase activities. Spectral and HPLC data for the membrane fraction revealed the presence of o-, b-and d-type haems, in addition to a majority of c-type haems, but no a-type haem, in agreement with carbon monoxide-binding analysis. The cytochrome c oxidase is thus of the cc(o/b)o 3 type, a type not previously described. The monohaem cytochrome c 553 is an electron donor to the cytochrome c oxidase; its encoding gene is located upstream of the cox operon and is 50-fold more transcribed than coxI encoding the cytochrome c oxidase subunit I. Even when DvH is grown under anaerobic conditions in lactate/sulfate medium, the two terminal oxidase-encoding genes are expressed. Furthermore, the quinol oxidase bd-encoding genes are more highly expressed than the cox genes. The cox operon exhibits an atypical genomic organization, with the gene coxII located downstream of coxIV. The occurrence of these membrane-bound oxygen reductases in other strictly anaerobic Deltaproteobacteria is discussed.

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The Tmc Complex fromDesulfovibrio vulgarisHildenborough Is Involved in Transmembrane Electron Transfer from Periplasmic Hydrogen Oxidation

Cited by 46 publications

References 36 publications

The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris

The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris

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

Oxygen reduction in the strict anaerobe Desulfovibrio vulgaris Hildenborough: characterization of two membrane-bound oxygen reductases

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