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Energy Conservation by a Hydrogenase-Dependent Chemiosmotic Mechanism in an Ancient Metabolic Pathway

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Energy Conservation by a Hydrogenase-Dependent Chemiosmotic Mechanism in an Ancient Metabolic Pathway Energy conservation by a hydrogenase-dependent chemiosmotic mechanism in an ancient metabolic pathway Marie Charlotte Schoelmericha,1 and Volker Müllera,2 aMolecular Microbiology & Bioenergetics, Institute of Molecular Biosciences, Johann Wolfgang Goethe University Frankfurt/Main, 60438 Frankfurt, Germany Edited by Caroline S. Harwood, University of Washington, Seattle, WA, and approved February 12, 2019 (received for review October 29, 2018) The ancient reductive acetyl-CoA pathway is employed by aceto- (THF), followed by a reduction of the formyl group to a meth- genic bacteria to form acetate from inorganic energy sources. enyl group via methenyl-THF and methylene-THF (12–15). A Since the central pathway does not gain net ATP by substrate-level second molecule of CO2 is reduced by the CO dehydrogenase/ phosphorylation, chemolithoautotrophic growth relies on the addi- acetyl CoA synthase (CODH/Acs) to enzyme-bound CO that tional formation of ATP via a chemiosmotic mechanism. Genome combines with the methyl group and CoA on the CODH/Acs analyses indicated that some acetogens only have an energy-converting, to acetyl-CoA (12, 16). Acetyl-CoA is then converted via acetyl ion-translocating hydrogenase (Ech) as a potential respiratory enzyme. phosphate to acetate and ATP. Although the Ech-encoding genes are widely distributed in nature, CO metabolism follows the same principle but involves oxi- the proposed function of Ech as an ion-translocating chemiosmotic dation of CO to CO2 according to: coupling site has neither been demonstrated in bacteria nor has it been demonstrated that it can be the only energetic coupling sites 4CO + 4H2O → 4CO2 + 4H2ðΔG0′ = −20 kJ=molÞ. [2] in microorganisms that depend on a chemiosmotic mechanism for energy conservation. Here, we show that the Ech complex of the In sum, CO is oxidized to acetate according to: thermophilic acetogenic bacterium Thermoanaerobacter kivui is MICROBIOLOGY indeed a respiratory enzyme. Experiments with resting cells prepared 4CO + 2H2O → 1CH3COOH + 2CO2ðΔG0′ = −165.6 kJ=molÞ. from T. kivui cultures grown on carbon monoxide (CO) revealed CO [3] oxidation coupled to H2 formation and the generation of a trans- membrane electrochemical ion gradient (Δμ~ion). Inverted membrane The net yield of ATP by substrate level phosphorylation (SLP) is vesicles (IMVs) prepared from CO-grown cells also produced H2 and zero, but since the bacteria do grow under lithotrophic condi- ATP from CO (via a loosely attached CO dehydrogenase) or a chemical tions, additional ATP synthesis must occur by a chemiosmotic reductant. Finally, we show that Ech activity led to the translocation mechanism (11). of both H+ and Na+ across the membrane of the IMVs. The H+ gradient How the WLP can be coupled to the synthesis of ATP has was then used by the ATP synthase for energy conservation. These been solved only recently for a mesophilic acetogen. Aceto- data demonstrate that the energy-converting hydrogenase in concert bacterium woodii, which grows optimally at 30 °C, has a simple with an ATP synthase may be the simplest form of respiration; it com- respiratory chain consisting of a ferredoxin-oxidizing, NAD- bines carbon dioxide fixation with the synthesis of ATP in an ancient reducing respiratory enzyme encoded by the rnf genes and an pathway. ATP synthase that are connected by a sodium ion circuit across acetogenesis | bioenergetics | energy-converting hydrogenase | respiratory Significance mechanism | chemiosmosis Acetogenic bacteria are the most primordial living organisms. he pioneer organism in a primordial world was probably a They can live solely on inorganic compounds by using carbon Tchemolithoautotrophic thermophilic anaerobe that employed monoxide or molecular hydrogen as energy sources to fix the reductive acetyl-CoA pathway (1, 2). This pathway is also carbon dioxide to acetate and rely on a chemiosmotic mecha- called Wood–Ljungdahl pathway (WLP), in dedication to its nism for energy conservation. Most microorganisms possess a discoverers, and encompasses CO2 fixation to acetyl CoA, CO2 complex respiratory chain that is composed of many different assimilation into biomass, and energy conservation (3, 4). The components to establish the chemiosmotic gradient. Here, we WLP has prevailed in three groups of strictly anaerobic organ- dissect the bioenergetics in a chemolithoautotrophic thermo- isms: methanogenic archaea, sulfate reducing bacteria, and philic acetogenic bacterium. This living fossil uses a simple acetogenic bacteria. respiration comprising only a hydrogenase and an ATP syn- Acetogenic bacteria are ubiquitous in nature and occupy an in- thase for energy conservation. This two-module respiration system is sufficient to sustain primordial microbial life. creasingly important role in biotechnological and industrial applica- – tions (5 8). They can grow heterotrophically on, for example, sugars, Author contributions: M.C.S. and V.M. designed research; M.C.S. performed research; alcohols, and aldehydes but also chemolithoautotrophically on M.C.S. and V.M. analyzed data; and M.C.S. and V.M. wrote the paper. hydrogen plus carbon dioxide or on carbon monoxide (3, 9–11). The authors declare no conflict of interest. Lithotrophic metabolism involves reduction of two mol CO2 to This article is a PNAS Direct Submission. acetate with electrons derived from H2 according to: Published under the PNAS license. 1Present address: Microbiology & Biotechnology, Institute of Plant Sciences and Microbi- 4H2 + 2CO2 → 1CH3COOH + 2H2O ðΔG0′ = −95 kJ=molÞ. ology, Universität Hamburg, 22609 Hamburg, Germany. [1] 2To whom correspondence should be addressed. Email: [email protected]. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. One molecule of CO2 is reduced to formate, the formate is then 1073/pnas.1818580116/-/DCSupplemental. bound in an ATP-dependent reaction to formyl-tetrahydrofolate www.pnas.org/cgi/doi/10.1073/pnas.1818580116 PNAS Latest Articles | 1of6 Downloaded by guest on October 3, 2021 the cytoplasmic membrane (17, 18): The Rnf complex uses redox grown on CO or glucose, and resting cells were prepared. After + energy to generate a transmembrane electrochemical Na gra- addition of CO, glucose-grown cells produced only little H2,whereas −1 −1 dient across the cytoplasmic membrane that then drives ATP CO-grown cells produced H2 at a rate of 584 ± 3nmol·min ·mg + synthesis by a Na F1FO ATP synthase. rnf genes are not present protein (n = 2, SD) (Fig. 1A), indicating that the ability to oxidize in every acetogen and, thus, a second mode of energy conser- CO was induced during growth on CO. Concomitant with H2 vation must exist in acetogenic bacteria. Interestingly, inspection formation, the intracellular ATP content increased (Fig. 1B). ATP of genome sequences led to the detection of genes encoding synthesis depended on an energized membrane as evident from the energy-converting, possibly ion-translocating, membrane-bound inhibition by the protonophore 3,3′,4′,5-tetrachlorosalicylanilide hydrogenases (Ech) in Rnf-free acetogens, leading to the pos- (TCS) or sodium ionophore N,N,N′,N′-tetracyclohexyl-1,2- tulate that in these acetogens Rnf is replaced by Ech (15). phenylenedioxydiacetamide (ETH2120) and NaCl (SI Appendix, Ech belongs to the group 4 [NiFe] hydrogenases (respiratory Fig. S1). To address whether CO oxidation is coupled to the hydrogenases), which comprise a very diverse and still largely generation of an electrical field across the membrane (due to ion enigmatic group of H2-evolving, possibly ion-translocating, translocation), we tested the effect of ionophores on electron energy-conserving membrane-associated hydrogenases (19, 20). transport (H2 formation). The protonophore TCS or the sodium The first described complex of this kind was the formate- ionophore ETH2120 and NaCl (Fig. 1C) both stimulated H2 hydrogen lyase (FHL), discovered in the most common micro- formation [84 ± 30% or 69 ± 2% (n = 2, SD), respectively]. This bial model organism Escherichia coli (21). To date, however, is reminiscent of “respiratory control” as observed in mitochon- FHL complexes have never been demonstrated to translocate dria: Charge translocation leads to the build-up of an electrical ions across the cytoplasmic membrane in bacteria. More complex field that slows down further electron transport; disruption of the Ech complexes with 6 to 14 subunits are present in archaea, and electrical field then stimulates electron transport. Thus, the ex- evidence has been presented for ion transport for the enzymes periments described above are consistent with the hypothesis that – from Methanosarcina, Pyrococcus, and Thermococcus (22 24). H2 formation from CO in T. kivui is coupled to the generation of a The six-subunit complex as found in the methanogen Meth- transmembrane electrochemical ion gradient. + + anosarcina mazei is H -translocating and the first enzyme in a To investigate whether Na might be the chemiosmotic coupling + chain of respiratory enzymes. The 14-subunit complex of Pyro- ion, we analyzed the effect of Na on H2 evolution from CO. H2 coccus was described as proton translocating, but the recent formation from CO was already quite high at the lowest (con- + high-resolution cryo-EM structure revealed a row of potential taminating) Na concentration (90 μM), and addition of NaCl + + Na /H antiporter modules leading to the assumption that the (0.25–10 mM) only slightly increased H2 formation (SI Appendix, + + + enzyme translocates both H and Na
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