The alternative complex III: A different architecture using known building modules

Refojo, Patrícia N.; Sousa, Filipa L.; Teixeira, Miguel; Pereira, Manuela M.

doi:10.1016/j.bbabio.2010.04.347

Cited by 9 publications

(14 citation statements)

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“…Genomic analysis revealed the presence of the major components of electron transfer chain in strain P3M‐2 T : proton‐translocating NADH‐dehydrogenase complexes, a membrane‐bound succinate dehydrogenase/fumarate reductase, isoprenoid quinones, quinol oxidizing complex of ACIII type (Refojo et al ., ) and a F 0 F 1 ‐type bacterial ATP synthase. The components of both menaquinone and ubiquinone biosynthetic pathways were present.…”

Section: Resultsmentioning

confidence: 99%

Characterization ofMelioribacter roseusgen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the classIgnavibacteria, and a proposal of a novel bacterial phylumIgnavibacteriae

Podosokorskaya

Kadnikov

Гаврилов

et al. 2013

Environmental Microbiology

198

124

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A novel moderately thermophilic, facultatively anaerobic chemoorganotrophic bacterium strain P3M-2(T) was isolated from a microbial mat developing on the wooden surface of a chute under the flow of hot water (46°C) coming out of a 2775-m-deep oil exploration well (Tomsk region, Russia). Strain P3M-2(T) is a moderate thermophile and facultative anaerobe growing on mono-, di- or polysaccharides by aerobic respiration, fermentation or by reducing diverse electron acceptors [nitrite, Fe(III), As(V)]. Its closest cultivated relative (90.8% rRNA gene sequence identity) is Ignavibacterium album, the only chemoorganotrophic member of the phylum Chlorobi. New genus and species Melioribacter roseus are proposed for isolate P3M-2(T) . Together with I. album, the new organism represents the class Ignavibacteria assigned to the phylum Chlorobi. The revealed group includes a variety of uncultured environmental clones, the 16S rRNA gene sequences of some of which have been previously attributed to the candidate division ZB1. Phylogenetic analysis of M. roseus and I. album based on their 23S rRNA and RecA sequences confirmed that these two organisms could represent an even deeper, phylum-level lineage. Hence, we propose a new phylum Ignavibacteriae within the Bacteroidetes-Chlorobi group with a sole class Ignavibacteria, two families Ignavibacteriaceae and Melioribacteraceae and two species I. album and M. roseus. This proposal correlates with chemotaxonomic data and phenotypic differences of both organisms from other cultured representatives of Chlorobi. The most essential differences, supported by the analyses of complete genomes of both organisms, are motility, facultatively anaerobic and obligately organotrophic mode of life, the absence of chlorosomes and the apparent inability to grow phototrophically.

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Section: Resultsmentioning

confidence: 99%

Characterization ofMelioribacter roseusgen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the classIgnavibacteria, and a proposal of a novel bacterial phylumIgnavibacteriae

Podosokorskaya

Kadnikov

Гаврилов

et al. 2013

Environmental Microbiology

198

124

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“…Notably, a functional counterpart for the cyt bc 1 complex, alternative complex III (ACIII), has been identified in a wide range of bacterial taxa, and its presence usually coincides with the absence of the cyt bc 1 complex (6)(7)(8)(9)(10). This complex is structurally and compositionally unrelated to the bacterial cyt bc 1 complex, but it plays the same central role as a quinol:electron acceptor oxidoreductase in both the respiratory and photosynthetic ETCs (6,(8)(9)(10)(11)(12)(13). In the respiratory chain, ACIII is usually associated with different cyt c oxidases and functions in aerobic electron transfer (14,15).…”

Section: Introductionmentioning

confidence: 99%

Cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from Roseiflexus castenholzii

et al. 2020

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Alternative complex III (ACIII) is a multisubunit quinol:electron acceptor oxidoreductase that couples quinol oxidation with transmembrane proton translocation in both the respiratory and photosynthetic electron transport chains of bacteria. The coupling mechanism, however, is poorly understood. Here, we report the cryo-EM structures of air-oxidized and dithionite-reduced ACIII from the photosynthetic bacterium Roseiflexus castenholzii at 3.3- and 3.5-Å resolution, respectively. We identified a menaquinol binding pocket and an electron transfer wire comprising six hemes and four iron-sulfur clusters that is capable of transferring electrons to periplasmic acceptors. We detected a proton translocation passage in which three strictly conserved, mid-passage residues are likely essential for coupling the redox-driven proton translocation across the membrane. These results allow us to propose a previously unrecognized coupling mechanism that links the respiratory and photosynthetic functions of ACIII. This study provides a structural basis for further investigation of the energy transformation mechanisms in bacterial photosynthesis and respiration.

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“…RTK17.1. The strain rapidly oxidised exogenous hydrogen with this enzyme in a membrane-bound aerobic respiratory process and likely provides hydrogen-derived reducing equivalents to the quinone pool for methane monooxygenase activity and/or cytochrome reduction, via activity of a recently described alternative (ACIII) cytochrome complex (40). Our model of how methane, methanol and hydrogen oxidation are integrated into the respiratory chain of verrucomicrobial methanotrophs is shown in Figure 3.…”

Section: Discussionmentioning

confidence: 99%

“…Following CH 4 oxidation by pMMO, ensuing reactions catalysed by an XoxF type methanol dehydrogenase (MeDH) and formate dehydrogenase (FDH) contribute additional reductant (Cyt c and NADH) into the respiratory chain for ATP production and growth (11). In methane-limiting conditions, the identified Group 1d [NiFe] hydrogenase generates a small proton-motive force, oxidised reductant (Q) is maintained via type ACIII cytochrome complex (40) and sufficient ATP is generated for maintenance. Respiratory complexes I and II are not shown but are encoded in the genome of Methylacidiphilum sp.…”

Section: Discussionmentioning

confidence: 99%

Aerobic H₂respiration enhances metabolic flexibility of methanotrophic bacteria

Carere

Hards

Houghton

et al. 2016

Preprint

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26Methanotrophic bacteria are important soil biofilters for the climate-active gas 27 methane. The prevailing opinion is that these bacteria exclusively metabolise single-28 carbon, and in limited instances, short-chain hydrocarbons for growth. This specialist 29 lifestyle juxtaposes metabolic flexibility, a key strategy for environmental adaptation 30 Recent physiological and ecological studies have collectively shown hydrogen is a 88 widely utilised energy source for microbial growth and survival across a growing 89 range of taxa and soil ecosystems (17)(18)(19). The discovery that the dominant soil 90 phyla including Actinobacteria (20) and Acidobacteria (18) can switch from growing 91 on heterotrophic substrates to persisting on atmospheric hydrogen has provided a 92 new understanding of how microorganisms survive nutrient-limited conditions. Given 93 its ubiquity and diffusivity, hydrogen gas is an ideal energy source to support the 94 growth or non-replicative persistence of soil bacteria. Our recent survey of 95 hydrogenase distribution (17), metalloenzymes that catalyse the reversible oxidation 96 of hydrogen, noted that genes encoding hydrogenases were extremely widespread. 97This result led us to investigate the distribution of hydrogenases in methanotrophic 98 bacteria, and we subsequently identified genes encoding these enzymes in all 31 99 publicly available genomes ( Figure S1). This prevalence of hydrogenase genes was 100 surprising given the apparent specialist lifestyle of methanotrophic bacteria. Reports 101 of hydrogenase activity in these microorganisms are scarce. Formate-dependent 102 hydrogen production, under anoxic conditions, has been shown in cultures of 103 Methylomicrobium album BG8 and Methylosinus trichosporium OB3b (21). 104 Methylococcus capsulatus (Bath) is known to express both cytosolic and membrane-105 bound hydrogenases, though their physiological function has not been resolved (22). 106The oxidation of hydrogen in methanotrophic bacteria has been predicted to 107 contribute reducing energy for methane oxidation (22), to recycle endogenous 108 hydrogen produced during nitrogen-fixation (23), and to drive the non-productive 109 oxidation of chlorinated solvents (24). However, no studies have confirmed whether 110 hydrogen metabolism contributes to the growth and persistence of these 111 microorganisms. 112To investigate the physiological role of hydrogenases in methanotrophic bacteria, we 113 undertook a geochemical, molecular and cultivation-based survey of a geothermal 114 soil profile at Rotokawa, New Zealand with known methanotrophic activity (25). In 115 this work, we isolated a thermoacidophilic methanotroph from the genus 116 Methylacidiphilum and demonstrate that it oxidises hydrogen gas during both growth 117 and persistence. Hydrogen oxidation occurred through an aerobic respiratory 118 process mediated by a membrane-bound [NiFe]-hydrogenase. Hydrogen oxidation 119 enhanced mixotrophic growth yields during methanotrophic growth, under both 120 oxygen-replete and...

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The alternative complex III: A different architecture using known building modules

Cited by 9 publications

References 0 publications

Characterization ofMelioribacter roseusgen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the classIgnavibacteria, and a proposal of a novel bacterial phylumIgnavibacteriae

Characterization ofMelioribacter roseusgen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the classIgnavibacteria, and a proposal of a novel bacterial phylumIgnavibacteriae

Cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from Roseiflexus castenholzii

Aerobic H₂respiration enhances metabolic flexibility of methanotrophic bacteria

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The alternative complex III: A different architecture using known building modules

Cited by 9 publications

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Characterization ofMelioribacter roseusgen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the classIgnavibacteria, and a proposal of a novel bacterial phylumIgnavibacteriae

Characterization ofMelioribacter roseusgen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the classIgnavibacteria, and a proposal of a novel bacterial phylumIgnavibacteriae

Cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from Roseiflexus castenholzii

Aerobic H2respiration enhances metabolic flexibility of methanotrophic bacteria

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Aerobic H₂respiration enhances metabolic flexibility of methanotrophic bacteria