On the universal core of bioenergetics

Abstract

Living cells are able to harvest energy by coupling exergonic electron transfer between reducing and oxidising substrates to the generation of chemiosmotic potential. Whereas a wide variety of redox substrates is exploited by prokaryotes resulting in very diverse layouts of electron transfer chains, the ensemble of molecular architectures of enzymes and redox cofactors employed to construct these systems is stunningly small and uniform. An overview of prominent types of electron transfer chains and of their characteristic electrochemical parameters is presented. We propose that basic thermodynamic considerations are able to rationalise the global molecular make-up and functioning of these chemiosmotic systems. Arguments from palaeogeochemistry and molecular phylogeny are employed to discuss the evolutionary history leading from putative energy metabolisms in early life to the chemiosmotic diversity of extant organisms. Following the Occam's razor principle, we only considered for this purpose origin of life scenarios which are contiguous with extant life. This article is part of a Special Issue entitled: The evolutionary aspects of bioenergetic systems.

Beating the acetyl coenzyme A-pathway to the origin of life

“…Distribution of free-energy-conserving metabolisms relevant to this article within the prokaryotes. The topology of this schematic phylogenetic tree has been argued previously [16]. Differently coloured regions refer to the presence of different chemical (and electrochemical) types of quinones (or complete absence thereof for the cases of the grey regions).…”

“…WL pathways are characterized by the fact that, rather than consuming free energy for biomass production, they participate in chemiosmotic potential generation and thus are also free-energy-harvesting processes. In aceto-and methanogens, the WL-type metabolism thus is at the same time a bioenergetic and a carbon-fixing system, whereas in almost all other species, carbon fixation and free energy harvesting occur in distinct pathways and the coupling is ensured by ATP and NAD(P)H. Free energy harvesting in these latter species quasi-exclusively exploits quinone-based electron transfer chains which, through mechanisms of 'free energy conversion' [8] couple the dissipation of the electrochemical disequilibria of various exogenous redox substrates [16] to the production of useful downstream disequilibria (such as the transmembrane proton gradient). The aceto-and methanogenic WL systems considered to be archetypal, by contrast, are devoid of quinone-based membrane-crossing electron transfer.…”

The evolution of Earth's biogeochemical nitrogen cycle

“…First, it is an abundant element in the cosmos and in Earth"s atmosphere (Henry et al, 2000;Marty, 2012); second, it forms versatile covalent bonds with carbon that are integral to the functioning of organic biomolecules; and third, nitrogen is redox-active in the stability field of liquid water and is thus a potent source of electrochemical energy for biological metabolism (Schoepp-Cothenet et al, 2012). A better understanding of what constrained the evolution of life on Earth therefore demands a reconstruction of the biogeochemical nitrogen cycle over time; in particular its role as a limiting nutrient affecting biological evolution and ecology (Anbar and Knoll, 2002).…”

Bioenergetic Constraints on the Evolution of Complex Life

“…First, chemiosmotic coupling is extremely versatile, because it allows almost any combination of electron donor and acceptor to be plugged into a basic electrical circuit. The proteins required form a limited "redox protein construction kit" (Baymann et al 2003;Schoepp-Cothenet et al 2013), which is easily passed around by lateral gene transfer, enabling swift adaptation to new niches. Second, by decoupling an exergonic reaction from ATP synthesis, growth can be sustained using many redox couples, which in terms of stoichiometric chemistry should not support life.…”