Structure of an Ancient Respiratory System

Yu, Hongjun; Wu, Changhao; Schut, Gerrit J.; Haja, Dominik K.; Zhao, Gongpu; Peters, John W.; Adams, Michael W. W.; H, Li

doi:10.1016/j.cell.2018.03.071

Cited by 85 publications

(161 citation statements)

References 66 publications

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“…Instead, the electrons directly enter a chain of three iron-sulphur (FeS) centres in the ferredoxin (Fd)binding domain (Fig. 1d), similar to the recently characterised NDH-1L type photosynthetic complex I and membrane-bound hydrogenases [15][16][17][18] . The PQ-binding site is located ca.…”

Section: Resultsmentioning

confidence: 63%

Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I

et al. 2020

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Photosynthetic organisms capture light energy to drive their energy metabolism, and employ the chemical reducing power to convert carbon dioxide (CO 2 ) into organic molecules. Photorespiration, however, significantly reduces the photosynthetic yields. To survive under low CO 2 concentrations, cyanobacteria evolved unique carbon-concentration mechanisms that enhance the efficiency of photosynthetic CO 2 fixation, for which the molecular principles have remained unknown. We show here how modular adaptations enabled the cyanobacterial photosynthetic complex I to concentrate CO 2 using a redox-driven proton-pumping machinery. Our cryo-electron microscopy structure at 3.2 Å resolution shows a catalytic carbonic anhydrase module that harbours a Zn 2+ active site, with connectivity to protonpumping subunits that are activated by electron transfer from photosystem I. Our findings illustrate molecular principles in the photosynthetic complex I machinery that enabled cyanobacteria to survive in drastically changing CO 2 conditions.

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Section: Resultsmentioning

confidence: 63%

Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I

et al. 2020

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“…The secondary Na + gradient then drives ATP synthesis via a Na + A 1 A O ATP synthase (37). This idea is supported by the recent highresolution structure of the 14-subunit Mbh from P. furiosus (25). The membrane arm can be divided into a H + and a Na + translocation unit, the latter resembles an Mrp-type Na + /H + antiporter.…”

Section: Discussionmentioning

confidence: 90%

Energy conservation by a hydrogenase-dependent chemiosmotic mechanism in an ancient metabolic pathway

Schoelmerich

Müller

2019

Proc. Natl. Acad. Sci. U.S.A.

115

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The ancient reductive acetyl-CoA pathway is employed by acetogenic bacteria to form acetate from inorganic energy sources. Since the central pathway does not gain net ATP by substrate-level phosphorylation, chemolithoautotrophic growth relies on the additional formation of ATP via a chemiosmotic mechanism. Genome analyses indicated that some acetogens only have an energy-converting, ion-translocating hydrogenase (Ech) as a potential respiratory enzyme. Although the Ech-encoding genes are widely distributed in nature, the proposed function of Ech as an ion-translocating chemiosmotic coupling site has neither been demonstrated in bacteria nor has it been demonstrated that it can be the only energetic coupling sites in microorganisms that depend on a chemiosmotic mechanism for energy conservation. Here, we show that the Ech complex of the thermophilic acetogenic bacteriumThermoanaerobacter kivuiis indeed a respiratory enzyme. Experiments with resting cells prepared fromT. kivuicultures grown on carbon monoxide (CO) revealed CO oxidation coupled to H2formation and the generation of a transmembrane electrochemical ion gradient (Δµ∼ion). Inverted membrane vesicles (IMVs) prepared from CO-grown cells also produced H2and ATP from CO (via a loosely attached CO dehydrogenase) or a chemical reductant. Finally, we show that Ech activity led to the translocation of both H+and Na+across the membrane of the IMVs. The H+gradient was then used by the ATP synthase for energy conservation. These data demonstrate that the energy-converting hydrogenase in concert with an ATP synthase may be the simplest form of respiration; it combines carbon dioxide fixation with the synthesis of ATP in an ancient pathway.

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“…In P. atrospeticum these are HyfD and HyfF, which are related to HycC/HyfB, and the HyfE protein. Together, all five proteins are expected to form a stable complex in the membrane, as in the structure of the Group 4 [Ni-Fe]-hydrogenase from Pyrococcus furiosus (Yu et al, 2018). Indeed, this large membrane domain is thought to be the ancient progenitor to the ionpumping membrane domain of respiratory Complex I (Yu et al, 2018, Batista et al, 2013.…”

Section: Key Differences Between Fhl-2 and Fhl-1mentioning

confidence: 99%

“…Together, all five proteins are expected to form a stable complex in the membrane, as in the structure of the Group 4 [Ni-Fe]-hydrogenase from Pyrococcus furiosus (Yu et al, 2018). Indeed, this large membrane domain is thought to be the ancient progenitor to the ionpumping membrane domain of respiratory Complex I (Yu et al, 2018, Batista et al, 2013. Given the conservation of these genes, it was surprising that removal of all of the extra membrane proteins from FHL-2 had no discernible effect on the physiological activity of the P. atrosepticum system (Figure 5A).…”

Section: Key Differences Between Fhl-2 and Fhl-1mentioning

confidence: 99%

The plant pathogenPectobacterium atrosepticumcontains a functional formate hydrogenlyase-2 complex

Lowden

Fleszar

Albareda

et al. 2019

Preprint

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Pectobacterium atrosepticum SCRI1043 is a phytopathogenic gram-negative enterobacterium. Genomic analysis has identified that genes required for both respiration and fermentation are expressed under anaerobic conditions. One set of anaerobically expressed genes is predicted to encode an important but poorly-understood membrane-bound enzyme termed formate hydrogenlyase-2 (FHL-2), which has fascinating evolutionary links to the mitochondrial NADH dehydrogenase (Complex I). In this work, molecular genetic and biochemical approaches were taken to establish that FHL-2 is fully functional in P. atrosepticum and is the major source of molecular hydrogen gas generated by this bacterium. The FHL-2 complex was shown to comprise a rare example of an active [NiFe]-hydrogenase-4 (Hyd-4) isoenzyme, itself linked to an unusual selenium-free formate dehydrogenase in the final complex. In addition, further genetic dissection of the genes encoding the predicted membrane domain of FHL-2 established surprisingly that the majority of genes encoding this domain are not required for physiological hydrogen production activity. Overall, this study presents P. atrosepticum as a new model bacterial system for understanding anaerobic formate and hydrogen metabolism in general, and FHL-2 function and structure in particular. Significance StatementPectobacterium atrospecticum contains the genes for the formate hydrogenlyase-2 enzyme, considered the ancient progenitor of mitochondrial respiratory Complex I. In this study, the harnessing of P. atrosepticum as a new model system for understanding bacterial hydrogen metabolism has accelerated new knowledge in FHL-2 and its component parts. Importantly, those component parts include an unusual selenium-free formate dehydrogenase and a complicated [NiFe]-hydrogenase-4 with a large membrane domain. FHL-2 is established as the major source of molecular hydrogen produced under anaerobic conditions by P. atrospectium, however surprisingly some components of the membrane domain were not essential for this activity.

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Structure of an Ancient Respiratory System

Cited by 85 publications

References 66 publications

Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I

Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I

Energy conservation by a hydrogenase-dependent chemiosmotic mechanism in an ancient metabolic pathway

The plant pathogenPectobacterium atrosepticumcontains a functional formate hydrogenlyase-2 complex

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