Ions in the Deep Subsurface of Earth, Mars, and Icy Moons: Their Effects in Combination with Temperature and Pressure on tRNA–Ligand Binding

Abstract

The interactions of ligands with nucleic acids are central to numerous reactions in the biological cell. How such reactions are affected by harsh environmental conditions such as low temperatures, high pressures, and high concentrations of destructive ions is still largely unknown. To elucidate the ions’ role in shaping habitability in extraterrestrial environments and the deep subsurface of Earth with respect to fundamental biochemical processes, we investigated the effect of selected salts (MgCl2, MgSO4, and Mg(ClO4)2) and high hydrostatic pressure (relevant for the subsurface of that planet) on the complex formation between tRNA and the ligand ThT. The results show that Mg2+ salts reduce the binding tendency of ThT to tRNA. This effect is largely due to the interaction of ThT with the salt anions, which leads to a strong decrease in the activity of the ligand. However, at mM concentrations, binding is still favored. The ions alter the thermodynamics of binding, rendering complex formation that is more entropy driven. Remarkably, the pressure favors ligand binding regardless of the type of salt. Although the binding constant is reduced, the harsh conditions in the subsurface of Earth, Mars, and icy moons do not necessarily preclude nucleic acid–ligand interactions of the type studied here.

Deep sea osmolytes in action: their effect on protein–ligand binding under high pressure stress

“…S3, ESI †) was estimated by determining the value of K b at three different temperatures (5, 15, and 25 1C) and applying the van't Hoff relation. 54,55 It is important to note that the same approach was used to determine the enthalpy change for the complex formation between BSA, HSA and proflavine under neat buffer conditions reported above. The value of the enthalpy change obtained is 12.9 AE 8.0 kJ mol À1 , which is about ten times lower than the value in pure buffer solution.…”

Emergent ribozyme behaviors in oxychlorine brines indicate a unique niche for molecular evolution on Mars

“…For example, perchlorate has been shown to increase the activity of α-chymotrypsin at low temperatures by lowering its activation enthalpy 51 . Additionally, pressure can reverse the deleterious effects of perchlorate on biomolecular interactions such as on liquid-liquid phase separation thought to be necessary for compartmentalization of prebiotic life 52 , and even the binding of small ligands to tRNA 53 .…”

Effects of chaotropic salts on global proteome stability in halophilic archaea: Implications for life signatures on Mars

“…Further studies could also consider other factors which may compensate effects of Martian‐relevant salts on halophilic proteomes. For example, high pressure, which reduces perchlorate enzymatic inhibition on bovine α‐chymotrypsin (Gault et al, 2020) and deleterious effects of MgCl 2 , MgSO 4 and Mg(ClO 4 ) 2 on ligand biding by tRNA (Jahmidi‐Azizi et al, 2021). Moreover, low temperatures of the surface and upper subsurface of Mars would also counteract chaotropic effects of Martian salts (Chin et al, 2010; Cray et al, 2015).…”