A low phosphorylation potential in the acetogen Acetobacterium woodii reflects its lifestyle at the thermodynamic edge of life

Spahn, Sebastian; Brandt, Karsten; Müller, Volker

doi:10.1007/s00203-015-1107-2

Cited by 22 publications

(15 citation statements)

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“…Reported values for G ADP/ATP range between 30 and 80 kJ • mol −1 (Thauer et al, 1977;Atkins and De Paula, 2011). For A. woodii, a phosphorylation potential of only 32 kJ • mol −1 has been measured (Spahn et al, 2015), but for other acetogens this value is unknown. For the calculation of the H 2 threshold of different acetogens described here, a value for G • ADP/ATP of 50 kJ • mol −1 (Poehlein et al, 2012) was used, in order not to underestimate the H 2 threshold.…”

Section: The Theoretical H 2 Threshold Of Acetogensmentioning

confidence: 99%

Extracellular Electron Uptake by Acetogenic Bacteria: Does H2 Consumption Favor the H2 Evolution Reaction on a Cathode or Metallic Iron?

Philips

2020

Front. Microbiol.

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Some acetogenic bacteria are capable of using solid electron donors, such as a cathode or metallic iron [Fe(0)]. Acetogens using a cathode as electron donor are of interest for novel applications such as microbial electrosynthesis, while microorganisms using Fe(0) as electron donor cause detrimental microbial induced corrosion. The capacity to use solid electron donors strongly differs between acetogenic strains, which likely relates to their extracellular electron transfer (EET) mechanism. Different EET mechanisms have been proposed for acetogenic bacteria, including a direct mechanism and a H 2 dependent indirect mechanism combined with extracellular hydrogenases catalyzing the H 2 evolution reaction on the cathode or Fe(0) surface. Interestingly, low H 2 partial pressures often prevail during acetogenesis with solid electron donors. Hence, an additional mechanism is here proposed: the maintenance of low H 2 partial pressures by microbial H 2 consumption, which thermodynamically favors the H 2 evolution reaction on the cathode or Fe(0) surface. This work elaborates how the H 2 partial pressure affects the H 2 evolution onset potential and the H 2 evolution rate on a cathode, as well as the free energy change of the anoxic corrosion reaction. In addition, the H 2 consumption characteristics, i.e., H 2 threshold (thermodynamic limit for H 2 consumption) and H 2 consumption kinetic parameters, of acetogenic bacteria are reviewed and evidence is discussed for strongly different H 2 consumption characteristics. Different acetogenic strains are thus expected to maintain different H 2 partial pressures on a cathode or Fe(0) surface, while those that maintain lower H 2 partial pressures (lower H 2 threshold, higher H 2 affinity) more strongly increase the H 2 evolution reaction. Consequently, I hypothesize that the different capacities of acetogenic bacteria to use solid electron donors are related to differences in their H 2 consumption characteristics. The focus of this work is on acetogenic bacteria, but similar considerations are likely also relevant for other hydrogenotrophic microorganisms.

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Section: The Theoretical H 2 Threshold Of Acetogensmentioning

confidence: 99%

Extracellular Electron Uptake by Acetogenic Bacteria: Does H2 Consumption Favor the H2 Evolution Reaction on a Cathode or Metallic Iron?

Philips

2020

Front. Microbiol.

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“…A. woodii grows heterotrophically but also autotrophically on H 2 + CO 2 [35]. The phosphorylation potential in these cells was measured to be much below the 'textbook-knowledge' value of 60 kJÁmol À1 : 37.9 AE 1.3 kJÁmol À1 for fructose, 32.1 AE 0.3 for H 2 + CO 2 , and 30.2 AE 0.9 for CO [36]. This would allow ATP synthesis with only a fraction of ions.…”

Section: Discussionmentioning

confidence: 88%

A Na⁺ A₁A_O ATP synthase with a V‐type c subunit in a mesophilic bacterium

Litty

Müller

2020

The FEBS Journal

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A 1 A O ATP synthases with a V-type c subunit have only been found in hyperthermophilic archaea which makes bioenergetic analyses impossible due to the instability of liposomes at high temperatures. A search for a potential archaeal A 1 A O ATP synthase with a V-type c subunit in a mesophilic organism revealed an A 1 A O ATP synthase cluster in the anaerobic, acetogenic bacterium Eubacterium limosum KIST612. The enzyme was purified to apparent homogeneity from cells grown on methanol to a specific activity of 1.2 UÁmg À1 with a yield of 12%. The enzyme contained subunits A, B, C, D, E, F, H, a, and c. Subunit c is predicted to be a typical V-type c subunit with only one ion (Na + )-binding site. Indeed, ATP hydrolysis was strictly Na + -dependent. N,N 0 -dicyclohexylcarbodiimide (DCCD) inhibited ATP hydrolysis, but inhibition was relieved by addition of Na + . Na + was shown directly to abolish binding of the fluorescence DCCD derivative, NCD-4, to subunit c, demonstrating a competition of Na + and DCCD/NCD-4 for a common binding site. After incorporation of the A 1 A O ATP synthase into liposomes, ATP-dependent primary transport of 22 Na + as well as DµNa + -driven ATP synthesis could be demonstrated. The Na + A 1 A O ATP synthase from E. limosum is the first ATP synthase with a V-type c subunit from a mesophilic organism. This will enable future bioenergetic analysis of these unique ATP synthases. AbbreviationsDµNa + , electrochemical sodium ion potential; DpNa, sodium ion potential; DΨ, membrane potential; DCCD, N,N 0 -dicyclohexylcarbodiimide; DDM, n-dodecyl-b-maltoside; ETH 2120, N,N,N,N 0 -tetra-cyclo-hexyl-1,2-phenylenedioxydiacetamide; MALDI, matrix-assisted laser desorption/ ionization; TCS, 3,3 0 ,4 0 ,5-tetrachlorosalicylanilide.

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“…Later, we corrected this value to −12 to −15 kJ per mol reaction, based on new insights into the stoichiometry of the ATPase reactions and considerations on the energy charge of syntrophically fermenting bacteria (Schink and Stams 2013). Energy gains in this range were reported before for syntrophic oxidation of butyrate (Adams et al 2006;Wang et al 2013), propionate (Krylova and Conrad 1998;Scholten and Conrad 2000), and acetate (Hao et al 2010;Schnürer et al 1997), as well as for homoacetogenic fermentation (Conrad and Wetter 1990;Fey and Conrad 2000;Seitz et al 1990), aceticlastic methanogenesis (Fey and Conrad 2000;Penning and Conrad 2006), and hydrogen-dependent methanogenesis (Dwyer et al 1988;Seitz (Müller 2015;Spahn et al 2015, Lim et al 2014. In any case, we have to keep in mind that measurements of bulk concentrations both in the gas phase and in the liquid phase give only a rough estimate of the actual in situ concentrations of the intermediates within the microstructure of microbial aggregates (Pauss et al 1990).…”

Section: Discussionmentioning

confidence: 99%

Biogas process parameters—energetics and kinetics of secondary fermentations in methanogenic biomass degradation

Montag

Schink

2015

Appl Microbiol Biotechnol

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Pool sizes of short-chain fatty acids (formate, acetate, propionate, and butyrate), hydrogen, and carbon monoxide were assayed in digesting sludge from four different methanogenic reactors degrading either sewage sludge or agricultural products and wastes at pH 8.0 and 40 or 47°C. Free reaction energies were calculated for the respective degradation reactions involved, indicating that acetate, propionate, and butyrate degradation all supplied sufficient energy (−10 to −30 kJ per mol reaction) to sustain the microbial communities involved in the respective processes. Pools of formate and hydrogen were energetically equivalent as electron carriers. In the sewage sludge reactor, homoacetogenic acetate formation from H 2 and CO 2 was energetically feasible whereas syntrophic acetate oxidation appeared to be possible in two biogas reactors, one operating at enhanced ammonia content (4.5 g NH 4 + -N per l) and the other one at enhanced temperature (47°C). Maximum capacities for production of methanogenic substrates did not exceed the consumption capacities by hydrogenotrophic and aceticlastic methanogens. Nonetheless, the capacity for acetate degradation appeared to be a limiting factor especially in the reactor operating at enhanced ammonia concentration.

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A low phosphorylation potential in the acetogen Acetobacterium woodii reflects its lifestyle at the thermodynamic edge of life

Cited by 22 publications

References 40 publications

Extracellular Electron Uptake by Acetogenic Bacteria: Does H2 Consumption Favor the H2 Evolution Reaction on a Cathode or Metallic Iron?

Extracellular Electron Uptake by Acetogenic Bacteria: Does H2 Consumption Favor the H2 Evolution Reaction on a Cathode or Metallic Iron?

A Na⁺ A₁A_O ATP synthase with a V‐type c subunit in a mesophilic bacterium

Biogas process parameters—energetics and kinetics of secondary fermentations in methanogenic biomass degradation

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A low phosphorylation potential in the acetogen Acetobacterium woodii reflects its lifestyle at the thermodynamic edge of life

Cited by 22 publications

References 40 publications

Extracellular Electron Uptake by Acetogenic Bacteria: Does H2 Consumption Favor the H2 Evolution Reaction on a Cathode or Metallic Iron?

Extracellular Electron Uptake by Acetogenic Bacteria: Does H2 Consumption Favor the H2 Evolution Reaction on a Cathode or Metallic Iron?

A Na+ A1AO ATP synthase with a V‐type c subunit in a mesophilic bacterium

Biogas process parameters—energetics and kinetics of secondary fermentations in methanogenic biomass degradation

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A Na⁺ A₁A_O ATP synthase with a V‐type c subunit in a mesophilic bacterium