On the inevitable journey to being
Dr Michael Russell, JPL, California Institute of Technology
Life is the evolutionary culmination of emergent symmetry-breaking, macroscopically organized dynamic structures in the universe. Members of this cascading series of autocatalytic energy converting systems, or engines in Cottrell’s terminology, become ever more complex—more chemical and less physical—as each engine extracts, exploits and generates ever lower grades of energy and resources in the service of entropy generation. Each one of these engines emerges spontaneously from order created by a particular mother engine or engines as the disequilibrated potential daughter is driven beyond a critical point, as in e.g., the transition to thermonuclear reactions during gravitationally-driven star formation; the transition to convective flow in systems driven beyond the Rayleigh limit by thermal gradients (such as those responsible for the tectonic dynamics of our planet); and the onset of Mohr-Coulomb failure and fracture propagation due to differential mechanical stress exceeding rock strength (as occurs in the planet's tectonically-strained ocean floor rock). Importantly, it is these fractures in the ocean floor, acting themselves as engines of dissipation, that allow ocean water access to the crust which in turn drives the onset of exothermic serpentinization, alkaline hydrothermal convection and thereby the spontaneous production of precipitated submarine hydrothermal mounds. It is at such mounds finally that, we argue, the two chemical disequilibria directly causative in the emergence of life spontaneously arose across the mineral precipitate membranes separating the acidulous, nitrate-bearing CO2-rich, Hadean sea from the alkaline and CH4/H2-rich serpentine-generated effluents. The first and foremost of these great geochemical gifts was the imposition of essential redox gradients involving hydrothermal CH4 and H2 as electron donors, and CO2 and nitrate, nitrite, and ferric iron from the ambient ocean as acceptors; which gradients, we propose, functioned as the original “carbon-fixing engine”. The second gift, also imposed across the inorganic membrane, was a post-critical-point (milli)voltage pH potential (proton concentration gradient) that, we hypothesize, drove the condensation of orthophosphate to produce a high energy currency:- “the pyrophosphatase engine”. Notably, of course, this specific ionic gradient, there available for the taking, is one upon which all extant cellular systems now depend even though they must constantly recreate it on their own through the harnessing of redox gradients, or the catabolism of biomolecules such as glucose, to recondense ADP to ATP. Once metabolizing cells emerged and evolved in this submarine mound, the call for constant and far-from-equilibrium free energy sources presumably diminished somewhat due to the relative stability, and “templating effect” of the relatively stable organized states of matter mediating the key steps of proto-life free energy conversion. Thus the metabolic engines could sustain themselves by merely “ticking over” during times of deprivation and in this way more robustly survive for the long periods that life occupied the ocean floor and deep biosphere before its escape to the wider and more free-energy rich world and, ultimately, its “discovery” of photosynthesis.
The energetics of organic synthesis inside and outside the cell
Professor Jan Amend, University of Southern California
Thermodynamic modeling of organic synthesis has largely been focused on deep-sea hydrothermal systems. When seawater mixes with hydrothermal fluids, redox gradients are established that serve as potential energy sources for the formation of organic compounds and biomolecules from inorganic starting materials. This energetic drive, which varies substantially depending on the type of host rock, is present and available both for abiotic (outside the cell) and biotic (inside the cell) processes. Here, we review and synthesize a library of theoretical studies that target organic synthesis energetics. The biogeochemical scenarios evaluated include those in present-day hydrothermal systems and in putative early Earth environments. It is consistently and repeatedly shown in these studies that the formation of relatively simple organic compounds and biomolecules can be energy-yielding (exergonic) at conditions that occur in hydrothermal systems. Expanding on our ability to calculate biomass synthesis energetics, we also present here a new approach for estimating the energetics of polymerization reactions, specifically those associated with polypeptide formation from the requisite amino acids.
The early evolution of biological energy conservation: hydrogen, metals, gradients and electron bifurcation
Professor William Martin, Heinrich Heine University, Germany
In very early chemical evolution, the forerunners of carbon and energy metabolism were the processes of generating reduced carbon compounds from carbon dioxide and the mechanisms of harnessing energy as compounds capable of doing some chemical work. New insights into energy conservation in methanogens and acetogens — cells that fuel both their carbon and energy metabolism through the CO2/H2 redox couple — suggest that reduced ferredoxin is the most ancient biological energy currency. Those anaerobic autotrophs generate reduced ferredoxin from H2 via a mechanism called electron bifurcation, a process that in turn links ferredoxin reduction to exergonic reactions and the generation of transmembrane ion gradients. Overall carbon and energy metabolsm in methanogens and acetogens that lack cytochromes and quinones (or the quinone analogue methanophenazine) involves Ech and Rnf complexes that pump ions while reducing protons and NAD+, respectively, with electrons from ferredoxin. This has some similarity to serpentinization, a geochemical process in which electons from Fe2+ generate H2 and reduced carbon compounds such as methane. The new findings from microbial physiology are remarkably congruent with the independently derived idea that life evolved in submarine alkaline hydrothermal vents and underscore evolutionarily significant similarities as well as differences in acetogen and methanogen physiology.
A reassessment of autotrophy at the emergence of life
Professor Wolfgang Nitschke, CNRS Marseilles
An empirical way to study the origin of life is through extrapolating the evolutionary history of extant life back towards its very beginning while respecting geochemical boundary conditions and fundamental physical laws. This approach has in the past identified the Wood-Ljungdahl (WL) pathway of aceto- and methanogens as a promising candidate for primordial energy and carbon metabolism. However, a number of problems with this scenario have recently been pointed out (Schoepp et al., 2012, Biochim.Biophys.Acta, doi: 10.1016/j.bbabio.2012.09.005) suggesting that the original model may require amendments and reinterpretations. Here we present a scenario which stipulates that methane and nitrogen oxyanions ought to be considered in addition to the canonical WL-substrates, H2 and CO2. The recently described denitrifying methanotrophs represent an extant example for a corresponding metabolism. We will present arguments suggesting that denitrifying methanotrophy may pre-date aceto- and methanogenesis. Extant methanotrophic pathways suggest that the earliest carbon-fixing and energy harvesting metabolism may have condensed CO (delivered by the Ni/Fe-catalysed reduction of CO2) and a second C1-body represented by formaldehyde (or a sulphur-associated methyl group) produced by monooxygenation of methane to methanol (at a diiron centre) followed by further oxidation to formaldehyde (possibly catalysed by a molybdenum/tungsten-sulphide). In both half-reactions, redox bifurcations play crucial roles.