Powering Primitive Life: Emergence of Proto-bioenergetic Systems

Life can be considered an emergent phenomenon, a non-equilibrium, autopoietic (self-maintaining) state facilitated by the flow of energy and chemicals needed to fuel its own internal chemical machinery. The contemporary biochemistry which underpins all life as we know it adheres to this basic autopoietic model and at the heart of such a system of life is energy transduction; breaking down foods such as carbohydrates (eg: sugars) and locking small tranches of energy released in this process within certain molecules. Subsequently, this energy is released to drive chemical processes of value to the system. Amongst the most important and ubiquitous energy-currency molecules are activated phosphorus (P) species, adenosine triphosphate (ATP) arguably being the most important. These molecules are able to selectively discharge small packets of energy according to the mechanistic rules of chemistry (ca. 40kJmol-1 for the hydrolysis of ATP to ADP which translates to an energy capacity of a single AA battery within 250g of ATP). Various mechanisms have emerged within living systems to re-charge their supply of ATP, with mitochondrial oxidative phosphorylation and substrate-level phosphorylation during glycolysis being central.

One of the most significant problems in the field of abiogenesis concerns the emergence of P-based energy currencies, especially involving ATP. So firmly ingrained is ATP in cellular bioenergetics that it is not unreasonable to expect it to be amongst the most ancient of biochemical machinery. However, we have recently reported (Bryant et al 2010) that pyrophosphite [H2P2O52-; PPi(III)], a close molecular cousin of pyrophosphate, has both strong prebiotic provenance and the potential to drive valuable reactions such as amino acid coupling to peptides without peptidic catalysis. These observations, some as yet unpublished, suggest PPi(III) may have acted as a bridge between non-enzyme mediated energy exchange in emerging living systems and energy currencies based on the pyrophosphate linkage of contemporary biochemistry. This potential bridge will be analysed in the context of both the underlying chemistry and potential functions of value to an emerging living system. Specifically, we will consider the prebiotic plausibility of PPi(III) and provide evidence of such from a recent field expedition to the Vatnajökull glacier region of Iceland. In addition, we will outline our experiments in which PPi(III) has been shown to be capable of performing reactions to afford molecules of potential functional value to a putative living system (Scheme 1), including coupling amino acids to peptides and the possible consequences of such coupling for the emergence of activate P-based energy currency molecules.