Expanding the informational chemistries of life: peptide/RNA networks

Abstract

The RNA world hypothesis simplifies the complex biopolymer networks underlining the informational and metabolic needs of living systems to a single biopolymer scaffold. This simplification requires abiotic reaction cascades for the construction of RNA, and this chemistry remains the subject of active research. Here, we explore a complementary approach involving the design of dynamic peptide networks capable of amplifying encoded chemical information and setting the stage for mutualistic associations with RNA. Peptide conformational networks are known to be capable of evolution in disease states and of co-opting metal ions, aromatic heterocycles and lipids to extend their emergent behaviours. The coexistence and association of dynamic peptide and RNA networks appear to have driven the emergence of higher-order informational systems in biology that are not available to either scaffold independently, and such mutualistic interdependence poses critical questions regarding the search for life across our Solar System and beyond.This article is part of the themed issue 'Reconceptualizing the origins of life'.

Re-conceptualizing the origins of life

“…This leads to a black-or-white distinction between life and non-life: something is alive or it is not. This provides little insight into the chemical networks of 'almost life' that span the stages of complexity between prebiotic molecules and fully functioning cellular life, such as the peptide networks discussed in [32]. We recognize abiotically produced molecules as not life, and LUCA as life, but have no capacity to characterize the things in between.…”

Prebiotic Peptides: Molecular Hubs in the Origin of Life

“…Such coevolution could have involved non-covalent interactions between the peptides and other classes of molecules as well as direct covalent linkages between peptides and their interaction partners. The possibility of coevolution between different types of macromolecules on the prebiotic Earth has been discussed previously, especially in the context of coevolution of peptides and RNA, ,,− and this review now provides a framework to ground such discussions in what has been experimentally documented about possible prebiotic interactions between peptides and other molecules.…”

“…Ongoing efforts are directed at characterizing pathways by which RNA molecules could have arisen de novo in an RNA-First World, − but it is indisputable that, in comparison with peptides, RNA is a chemically complicated, synthetically challenging, and much more kinetically fragile molecule (Chart ). Among discussions of putative earlier (pre-RNA) genetic systems that “invented” and were subsequently taken over by RNA, ,, polypeptides and peptide–nucleic acid hybrid molecules have received considerable attention. ,,,,,,− Regardless of whether polypeptides or RNA came first or (more likely) are the products of coevolution, at a minimum it seems necessary that short proto-oligopeptides and proto-nucleic acids, as well as other organic oligomers, were present simultaneously on the prebiotic Earth and interacted to drive initial selection events leading to the inception of biopolymer synthesis.…”

The Emergence of Life

“…Precursors have been shown to give rise to more complex structures through a variety of non-chemical processes (Ferris and Orgel 1966;Sanchez et al 1967Sanchez and Orgel 1970;Fuller et al 1972a,b;Orgel and Crick 1993;Ferris et al 1996;Orgel 2004;Powner et al 2009Powner et al , 2010Powner et al , 2011. Other efforts towards demonstrating the prebiotic synthesis of RNA have yielded promising results (Cafferty et al 2016;Yeates et al 2016;Costanzo et al 2017;He et al 2017;Mathis et al 2017;Szilagyi et al 2017;Taran et al 2017;Yeates et al 2017). A significant effort resulted in the robust production of enantiopure RNA precursors from racemic starting materials under potential prebiotic conditions (Hein et al 2011;Leu et al 2011;.…”