Energy conservation in chemotrophic anaerobic bacteria

Thauer, Rudolf K.; Jungermann, Kurt; Decker, Karl

doi:10.1128/br.41.1.100-180.1977

Cited by 2,315 publications

(553 citation statements)

References 687 publications

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“…Such findings are broadly consistent with the findings of Thauer et al [39] that under conditions relevant for microbes, in the reaction of H 2 with CO 2 , the equilibrium lies on the side of reduced carbon compounds, which is why acetogens can grow from the reaction…”

Section: Alkaline Hydrothermal Ventssupporting

confidence: 92%

Early bioenergetic evolution

Sousa

Thiergart

Landan

et al. 2013

Phil. Trans. R. Soc. B

233

256

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Life is the harnessing of chemical energy in such a way that the energy-harnessing device makes a copy of itself. This paper outlines an energetically feasible path from a particular inorganic setting for the origin of life to the first free-living cells. The sources of energy available to early organic synthesis, early evolving systems and early cells stand in the foreground, as do the possible mechanisms of their conversion into harnessable chemical energy for synthetic reactions. With regard to the possible temporal sequence of events, we focus on: (i) alkaline hydrothermal vents as the far-from-equilibrium setting, (ii) the Wood–Ljungdahl (acetyl-CoA) pathway as the route that could have underpinned carbon assimilation for these processes, (iii) biochemical divergence, within the naturally formed inorganic compartments at a hydrothermal mound, of geochemically confined replicating entities with a complexity below that of free-living prokaryotes, and (iv) acetogenesis and methanogenesis as the ancestral forms of carbon and energy metabolism in the first free-living ancestors of the eubacteria and archaebacteria, respectively. In terms of the main evolutionary transitions in early bioenergetic evolution, we focus on: (i) thioester-dependent substrate-level phosphorylations, (ii) harnessing of naturally existing proton gradients at the vent–ocean interface via the ATP synthase, (iii) harnessing of Na+ gradients generated by H+/Na+ antiporters, (iv) flavin-based bifurcation-dependent gradient generation, and finally (v) quinone-based (and Q-cycle-dependent) proton gradient generation. Of those five transitions, the first four are posited to have taken place at the vent. Ultimately, all of these bioenergetic processes depend, even today, upon CO2 reduction with low-potential ferredoxin (Fd), generated either chemosynthetically or photosynthetically, suggesting a reaction of the type ‘reduced iron → reduced carbon’ at the beginning of bioenergetic evolution.

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Section: Alkaline Hydrothermal Ventssupporting

confidence: 92%

Early bioenergetic evolution

Sousa

Thiergart

Landan

et al. 2013

Phil. Trans. R. Soc. B

233

256

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“…Extensive excretion of internal metabolites does occur under various nutrient limiting conditions, e.g., carbon catabolites under nitrogen limitation 38,58,59 ; but this would not benefit other organisms experiencing the same limitation. Thus, studies of mutualistic cross-feeding have mostly involved systems in which individual species cannot grow alone, such as anaerobic digesters constrained by extremely low energy influx 11,12 , and synthetic or evolved auxotrophs [17][18][19][20][21][22][23][24][25] .…”

Section: Discussionmentioning

confidence: 99%

Dynamic metabolic exchanges between complementary bacterial types provide collaborative stress resistance

Amarnath

Pontrelli

et al. 2021

Preprint

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Despite the ubiquity of microbial diversity observed across environments, mechanisms of cooperativity that enable species coexistence beyond the classical limit of one-species-per-niche have been elusive. Here we report the observation of a transient but substantial cross-feeding of internal metabolites between two marine bacterial species under acid stress, and further establish through quantitative physiological characterization of the individual strains that this cross-feeding is central to the survival and coexistence of these species in growth-dilution cycles. The coculture self-organizes into a limit cycle in which acid-stressed producers excrete various internal metabolites upon entering growth arrest, enabling the cross-feeders to grow, restore medium pH, and protect the producers from death. These results establish a rare, mechanistic example of inter-species cooperation under stress, as anticipated long ago by the stress gradient hypothesis. As the accumulation of acetate and other fermentation products occurs ubiquitously in habitats ranging from the gut to wastewater, and the excretion of internal metabolites is an obligatory physiological response by bacteria under weak acid stress, stress-induced cross-feeding provides a general physiological basis for the extensive sharing of metabolic resources to promote the coexistence of diverse species in microbial communities.

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“…Anaerobic lactate oxidation is an energetically unfavored reaction that requires bacteria to use confurcating Ldh [Ldh and electron transferring flavoprotein (EtfAB) complex] to drive the endergonic reduction of NAD (E°′ NAD/NADH = −320 mV; Thauer et al, 1977 ) with lactate (E°′ pyruvate/lactate = −190 mV) by simultaneously oxidizing Fd red ( Weghoff et al, 2015 ; Buckel and Thauer, 2018 ). Under anaerobic conditions, nZVI (E°′Fe 2+ /Fe 0 = −469 mV; Rickard and Iii, 2007 ) could transfer electrons directly to ferredoxins (E°′Fd ox /Fd red = −500 −−398 mV; Thauer et al, 1977 ; Li and Elliott, 2016 ) when ferredoxins are present extracellularly ( Marshall et al, 2017 ). Alternatively, ferredoxin can be reduced through membrane-bound or cytoplasmic reversible electron-bifurcating systems ( Buckel and Thauer, 2018 ) via direct or H 2 -mediated electron transfer.…”

Section: Discussionmentioning

confidence: 99%

nZVI Impacts Substrate Conversion and Microbiome Composition in Chain Elongation From D- and L-Lactate Substrates

Contreras-Dávila

Esveld

Buisman

et al. 2021

Front. Bioeng. Biotechnol.

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Medium-chain carboxylates (MCC) derived from biomass biorefining are attractive biochemicals to uncouple the production of a wide array of products from the use of non-renewable sources. Biological conversion of biomass-derived lactate during secondary fermentation can be steered to produce a variety of MCC through chain elongation. We explored the effects of zero-valent iron nanoparticles (nZVI) and lactate enantiomers on substrate consumption, product formation and microbiome composition in batch lactate-based chain elongation. In abiotic tests, nZVI supported chemical hydrolysis of lactate oligomers present in concentrated lactic acid. In fermentation experiments, nZVI created favorable conditions for either chain-elongating or propionate-producing microbiomes in a dose-dependent manner. Improved lactate conversion rates and n-caproate production were promoted at 0.5–2 g nZVI⋅L–1 while propionate formation became relevant at ≥ 3.5 g nZVI⋅L–1. Even-chain carboxylates (n-butyrate) were produced when using enantiopure and racemic lactate with lactate conversion rates increased in nZVI presence (1 g⋅L–1). Consumption of hydrogen and carbon dioxide was observed late in the incubations and correlated with acetate formation or substrate conversion to elongated products in the presence of nZVI. Lactate racemization was observed during chain elongation while isomerization to D-lactate was detected during propionate formation. Clostridium luticellarii, Caproiciproducens, and Ruminococcaceae related species were associated with n-valerate and n-caproate production while propionate was likely produced through the acrylate pathway by Clostridium novyi. The enrichment of different potential n-butyrate producers (Clostridium tyrobutyricum, Lachnospiraceae, Oscillibacter, Sedimentibacter) was affected by nZVI presence and concentrations. Possible theories and mechanisms underlying the effects of nZVI on substrate conversion and microbiome composition are discussed. An outlook is provided to integrate (bio)electrochemical systems to recycle (n)ZVI and provide an alternative reducing power agent as durable control method.

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Energy conservation in chemotrophic anaerobic bacteria

Cited by 2,315 publications

References 687 publications

Early bioenergetic evolution

Early bioenergetic evolution

Dynamic metabolic exchanges between complementary bacterial types provide collaborative stress resistance

nZVI Impacts Substrate Conversion and Microbiome Composition in Chain Elongation From D- and L-Lactate Substrates

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