Early bioenergetic evolution

Abstract

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.

Early Microbial Evolution: The Age of Anaerobes

“…The acetyl-CoA pathway is regarded as the most ancient of the six pathways of CO 2 fixation known (Fuchs 2011) and in contrast to earlier views; it is the only one that occurs in both archaea and bacteria (Berg et al 2010). The source of electrons for CO 2 fixation is geological H 2 (Martin and Russell 2007), the same electron donor that modern microbes using the acetyl-CoA harness, and the source of energy is the exergonic reduction of CO 2 to acetate in the case of acetogens or methane in the case of methanogens (Sousa et al 2013b). The H 2 required to push the equilibrium toward the accumulation of reduced organic compounds comes from a geochemical process called serpentinization (Martin and Russell 2007;Russell et al 2010), which has been going on as long as there has been water on Earth (Sleep et al 2004).…”

“…There is also the problem that concatenation entails an assumption that the concatenated genes in question all share the same evolutionary history, which is actually very hard to show for real data spanning the bacterial -archaeal divide. Charlebois and Doolittle (2004) called this rescuing the core, James McInerney called it a tree of tips (Creevey et al 2004), and we called it the disappearing tree effect (Sousa et al 2013b). There can be no question that there are tree-like components to some segments of prokaryote evolution (Daubin et al 2003), but the question of how far back any tree-like component of prokaryote evolution goes is very difficult to answer (Doolittle and Bapteste 2007;Dagan et al 2008).…”

“…Amino acids, the main constituents of cells comprising 60% of a cell's mass by weight (Neidhardt et al 1990) are quite stable (Amend and McCollom 2009); an organic soup type mixture is at or very close to equilibrium. Life is not just a process of reorganizing existing components that are close to equilibrium into something that looks like a cell, life is an exergonic chemical reaction, a continuous far from equilibrium process (Sousa et al 2013b). Second, the kind of substrates that heterotrophic origins supporters have in mind, namely organics from space delivered to earth by comets or meteorites (Chyba et al 1990), tend to show what is called complete structural diversity (Sephton 2002), meaning that for a given chemical formula detected, a very large number of isomers are found, all in very minute quantities (Sephton 2002).…”

Fluid mixing and the deep biosphere of a fossil Lost City-type hydrothermal system at the Iberia Margin

“…Serpentinization systems have existed throughout most of Earth's history, and it has been suggested that mixing of serpentinization fluids with Archean seawater produced conditions conducive to abiotic synthesis and the emergence of life on Earth (1). The Lost City hydrothermal field, located ∼15 km off the Mid-Atlantic Ridge axis at 30°N (2)(3)(4), represents the archetype of low-temperature seafloor serpentinization systems at slow-spreading midocean ridges and serves as an excellent present-day analog to fossil serpentinitehosted hydrothermal systems in such environments.…”

The Hormesis of Thinking: A Deeper Quantum Thermodynamic Perspective?

“…Although the mitochondrion is not the only eukaryotic sensor system, it can rapidly detect environmental change and induce adaptation to enhance information capture. Its major role is perhaps inferred if life was initiated in a thermal vent [79] and then evolved the ability to use electron gradients to generate its own proton gradient; perturbation of these gradients would provide a selective pressure to capture information to improve efficiency.…”