Evolution de la bioénergétiqueEvolution of bioenergetics
What is "Free Energy"?
and what does it have to do with Life's Emergence and the Evolution of
and what does it have to do with Life's Emergence and the Evolution of Complexity?
Thermodynamic considerations allow deducing the general framework of environmental conditions permitting life to emerge and to persist. The fundamental conditio sine qua non is the existence of some kind of thermodynamic disequilibrium able to fuel local entropy decreases via disequilibria-converting mechanisms. The research field studying such mechanisms employed by life is called Bioenergetics. The comparative survey of bioenergetic principles operating in cellular life permits narrowing down the general thermodynamic requirements towards the specific conditions which likely drove the emergence of life on our planet.
(I) The nature of the driving disequilibria: The specific thermodynamic disequilibrium sustaining all non-photosynthetic life on Earth is the electrochemical tension, that is, a redox disequilibrium between reducing and oxidising environmental substrates (see Schoepp-Cothenet et al., 2013). Bioenergetic electron transfer chains convert this electrical potential into a proton (or sodium) motive force (composed of electrial field and osmotic components) which eventually is converted to a chemical disequilibrium, that is, ATP/ADP (or PPi/Pi) ratios displaced far from equilibrium.
In anoxygenic photosynthesis, the terminal environmental oxidant in the above described scheme is replaced by a light-induced positive charge while in oxygenic photosynthesis, both environmental oxidant and reductant are produced by tapping into the energy of visible-light photons (see figure below). The remaining components of the full photosynthetic electron transfer chains fully correspond to those of non-photosynthetic organisms. Phylogeny of the respective enzymes as well as the occurrence of phototrophs on the phylogenetic tree of life strongly indicate that chemotrophic life preceeded phototrophic one and that photosynthetic reaction centres were additions to pre-existing electron transfer chains collapsing environmental redox disequilibria.
In fermentation the electron sink is generated by continuously excreting partially or fully reduced metabolites (such as ethanol, aldehyde, formate, methane, acetate etc). In many of these cases, the free energy contained in the respective redox reactions is insufficient to participate in membrane-potential generation and increasing ATP-levels therefore has to proceed via substrate-level-phosphorylation.
Conclusion: The layout of extant life indicates that the fundamental source of free energy (i.e. the environmental disequilibrium) driving the entropy-decrease characterising living cells is electrochemical. We have no reason to assume that this may have been different when life emerged. However, while the proton- (sodium-) motive potential in extant cells is converted from the electrochemical potential, there is reason to believe that during life’s emergence(in specific locales, see AHV-hypothesis), a proton disequilibrium may have been constitutive and thus have served as a source of free energy in its own right next to the environmental electrochemical potential.
(II) On the importance of 2-electron electrochemistry:
A significant fraction of biologically relevant redox centres are 2-electron compounds. In aqueous solution (due to the possibility of proton-coupled electron tranfer) and under appropriate conditions (e.g. pH value), such 2-electron compounds can exhibit cooperative redox behaviour (see 2-electron webpage), in which both electrons come or go together rather than one-by-one in a consecutive manner. The existence of cooperative redox behaviour entails two corrolaries arguably crucial for life:
1. Metastable redox gradients. Cooperative 2-electron compounds react very sluggishly with 1-electron centres even if the overall electron transfer reactions are strongly exergonic. This property allows the build-up of metastable electrochemical gradients in aqueous solutions, a prerequisite for life being able to harvest the free energy inherent in these electrochemical disequilibria. Present day examples for such metastable environmental disequilibria are provided by the coexistence of molecular hydrogen or methane in the presence of oxygen. On the early Earth, ferrous iron and nitrate would have redox-equilibrated very slowly allowing for the build-up of significant concentrations of the environmental oxidant nitrate (see also Wong et al. 2017). In living cells the extremely strong redox cooperativity of the NAD(P)H/NAD(P)+ couple prevents NAD(P)H from becoming non-enzymatically oxidised in the presence of multiple 1-electron acceptors such as for example non-heme iron centres or iron-sulphur clusters.
2. Up-conversion of reducing power via electron bifurcation. As detailed on our 2-electron webpage (see also Baymann et al., 2018), 2-electron compounds featuring strong positive redox cooperativity are capable of generating 1-electron reductants more reducing than the initial 2-electron redox centre. This reaction is driven by the overall exergonic ΔG of the overall reaction (see Figure below). Prominent biological examples comprise the Qo-site reaction of Rieske/cytb complexes (Bergdoll et al. 2016) or the flavin-based electron bifurcations as reviewed in Baymann et al. 2018. We are presently exploring the possibility whether the 2-electron transition metals Molybdenum and Tungsten are able to perform electron bifurcation (Duval et al. 2016) and thereby could have performed, during life’s emergence, the redox up-converting roles played by quinones and flavins after the organic take-over.
The generation of a lower potential reductant represents a local increase of redox disequilibrium (and therefore a local decrease in entropy) and the mechanism of electron bifurcation may therefore be part of the ancestral repertoire of disquilibrium converters driving the emergence of life.
We emphasize that both metastable redox gradients and the process of electron bifurcation do only exist in protic solvents (or if the protein-environment surrounding the 2-electron centre contains deprotonatable groups with appropriate pK-values). This fact may rationalise why water appears to be an indispensable ingrediant for the emergence of life.
(III) Conversion of environmental disequilibria into the entropy-decrease characterizing life; the bioenergetics-mineral connection:
Again, general thermodynamic considerations tell us that, while environmental disequilibria (or more specifically, redox gradients, see above) are the ultimate drivers of life’s emergence, we also need to elucidate the types of mechanisms, the « engines », converting these disequilibria into the entropy decrease characterizing life. The only truly empirical way to guess which kinds of engines may have operated at life’s emergence is to retrodict from what we see in extant living organisms.Let’s face it: studying bioenergetics means working with metalloenzymes! To the sole exception of quinones and flavins, the job of converting environmental redox gradients into pmf is performed by transition metals and clusters thereof, that is, by inorganic entities. Bioenergetics therefore fundamentally is an inorganic process. Intriguingly, several of the catalytic centres found in metalloenzymes strangely resemble metal-clusters observed in certain minerals (see figures below and Nitschke et al. 2013).
While the possibility of mineral-borne reactions having preceeded truly biological mechanisms was discussed in the past by Günter Wächtershäuser as well as by Michael J. Russell, examining the inventory of catalytic centres in metalloenzymes permits to narrow down the ensemble of promising candidate minerals and relevant reaction schemes having possibly played midwife in life’s emergence. Potential roles of specific minerals are discussed on our webpage on « Inorganic engines ».
Baymann, F., Schoepp-Cothenet, B., Duval, S., Guiral, M., Brugna, M.,
Baffert, C., Russell, M.J. and Nitschke, W. (2018)
Frontiers in Microbiology 9, 1357 [pdf-file]
On the natural history of flavin-based electron bifurcation
Wong, M.L., Charnaz, B.D., Gao, P., Yung, Y.L. and Russell, M.J. (2017)
Astrobiology 17, 975-983 [pdf-file]
Nitrogen oxides in early Earth’s atmosphere
as electron acceptors for life’s emergence
Bergdoll, L., ten Brink, F., Nitschke, W., Picot, D. and Baymann, F. (2016)
Biochim. Biophys. Acta Bioenergetics 1857, 1569-1579 [pdf-file]
From low- to high-potential bioenergetic chains:
Thermodynamic constraints of Q-cycle function
Duval, S., Santini, J.M., Lemaire, D., Chaspoul, F., Russell, M.J.,
Grimaldi, S., Nitschke, W., Schoepp-Cothenet, B. (2016)
Biochim. Biophys. Acta Bioenergetics 1857, 1353-1362 [pdf-file]
The H-bond network surrounding the pyranopterins modulates redox
cooperativity in the molybdenum-bisPGD cofactor in arsenite oxidase
Schoepp-Cothenet, B., van Lis, R., Atteia, A., Baymann, F., Capowiez, L.,
Ducluzeau, A.-L., Duval, S., ten Brink, F., Russell, M.J. and Nitschke, W. (2013)
Biochim.Biophys. Acta Bioenergetics 1827, 79-93 [pdf-file]
On the universal core of bioenergetics
Nitschke, W., McGlynn, S., Milner-White, J., and Russell, M.J. (2013)
Biochim.Biophys. Acta Bioenergetics 1827, 871-881 [pdf-file]
On the antiquity of metalloenzymes and their substrates in bioenergetics