Multiple prebiotic metals mediate translation

Abstract

SignificanceRibosomes are found in every living organism, where they are responsible for the translation of messenger RNA into protein. The ribosome’s centrality to cell function is underscored by its evolutionary conservation; the core structure has changed little since its inception ∼4 billion years ago when ecosystems were anoxic and metal-rich. The ribosome is a model system for the study of bioinorganic chemistry, owing to the many highly coordinated divalent metal cations that are essential to its function. We studied the structure, function, and cation content of the ribosome under early Earth conditions (low O2, high Fe2+, and high Mn2+). Our results expand the roles of Fe2+ and Mn2+ in ancient and extant biochemistry as cofactors for ribosomal structure and function.

The Future of Origin of Life Research: Bridging Decades-Old Divisions

“…Experimentation with origins in hydrothermal vents [147][148][149] and geothermal fields [150][151][152] have taken into consideration geological insights in their OoL scenarios. In particular, the importance of relevant metals and metal clusters in the Hadean has settled in experimental work that recreates the origin of biochemistry in vitro, including carbon cycling [98,103,153], nitrogen fixation [154], ribosomal translation [155], and even the generation of pH gradients [156]. Simulated hydrothermal conditions, in particular pores, select for the replication of longer oligonucleotides [157].…”

Iron-mediated degradation of ribosomes under oxidative stress is attenuated by manganese

“…How other ions with different properties are able to promote RNA folding is not well understood (26). Ribosomal Mg 2+ can be substituted with other divalent cations, including Fe 2+ or Mn 2+ (27)(28)(29)(30) and the ribosome can competently mediate translation in this state (30).…”

“…Recent work has drawn on the interesting observation that while evolution has conserved the ribosomal core through billions of years, the earth environment has changed dramatically over this time, and with it the bioavailability of the metals on which the ribosome structure depends. Metal levels in the aqueous environment prior to abiogenesis included high concentrations of Fe 2+ (36), while Mg 2+ was less abundant than today (30,37). With the evolution of photosynthesis and the increase in molecular oxygen, much of the iron was lost from the aqueous environment through precipitation (38).…”

“…The proclivity for Fe 2+ to participate in the Fenton reaction with H2O2 (which produces hydroxyl radicals and Fe 3+ ) is of consequence in cells under oxidative stress conditions as it can enhance oxidant-induced damage to biomolecules. In an increasingly oxygen-rich environment, continuous close associations with Fe 2+ would have become a dangerous proposition (30). Conversely, the higher reduction potential of manganese prevents its participation in Fenton chemistry (40).…”

Replacing Mg2+ by Fe2+ for RNA‐Cleaving DNAzymes

“…They found that Mg 2+ can replace Fe 2+ at neutral pH but not at low pH. Fe 2+ was also able to substitute for Mg 2+ in DNA polymerases, RNA polymerases, DNA ligases, and in protein translation …”