In search of the RNA world on Mars

Abstract

Advances in origins of life research and prebiotic chemistry suggest that life as we know it may have emerged from an earlier RNA World. However, it has been difficult to reconcile the conditions used in laboratory experiments with real-world geochemical environments that may have existed on the early Earth and hosted the origin(s) of life. This challenge is due to geologic resurfacing and recycling that have erased the overwhelming majority of the Earth's prebiotic history. We therefore propose that Mars, a planet frozen in time, comprised of many surfaces that have remained relatively unchanged since their formation > 4 Gya, is the best alternative to search for environments consistent with geochemical requirements imposed by the RNA world. In this study, we synthesize in situ and orbital observations of Mars and modeling of its early atmosphere into solutions containing a range of pHs and concentrations of prebiotically relevant metals (Fe²⁺ , Mg²⁺ , and Mn²⁺ ) spanning various candidate aqueous environments. We then experimentally determine RNA degradation kinetics due to metal-catalyzed hydrolysis (cleavage) and evaluate whether early Mars could have been permissive toward the accumulation of long-lived RNA polymers. Our results indicate that a Mg²⁺ -rich basalt sourcing metals to a slightly acidic (pH 5.4) environment mediates the slowest rates of RNA cleavage, though geologic evidence and basalt weathering models suggest aquifers on Mars would be near neutral (pH ~ 7). Moreover, the early onset of oxidizing conditions on Mars has major consequences regarding the availability of oxygen-sensitive metals (i.e., Fe²⁺ and Mn²⁺ ) due to increased RNA degradation rates and precipitation. Overall, (a) low pH decreases RNA cleavage at high metal concentrations; (b) acidic to neutral pH environments with Fe²⁺ or Mn²⁺ cleave more RNA than Mg²⁺ ; and (c) alkaline environments with Mg²⁺ dramatically cleaves more RNA while precipitates were observed for Fe²⁺ and Mn²⁺ .

Keywords: Mars; RNA world; origins of life.

Figure 1

RNA‐containing oligonucleotide cleavage assay. A hybrid RNA–DNA oligomer, 5’‐Cy3‐TTT‐TTTrCTT‐TTT‐TTT‐3’, was designed to contain a single ribonucleotide (r) in between a chain of deoxyribonucleotides which could allow us to quantify cleavage at a single site. Representative gel scan displays two fluorescent bands belonging to either the intact 15‐mer (Band 1) or the residual 7‐mer (Band 2) cleaved at the single ribonucleotide site

Figure 2

Relevant observations of Earth and Mars. Geologic resurfacing and recycling have erased the overwhelming majority of the Earth's prebiotic history during the Hadean when life may have originated. We propose that Mars, a planet comprised of surfaces that have remained relatively unchanged since their formation, is the best alternative to search for environments consistent with geochemical requirements imposed by the RNA world. *uncertain timing, ¹Monteux et al. 2016, ²Pearce et al. 2018, ³Mojzsis et al. 2001, ⁴Wilde et al. 2001, ⁵Gomes et al. 2005, ⁶Boehnke & Harrison, 2016, ⁷Boussau et al. 2008, ⁸Gladman et al. 1996, ⁹Hassenkam et al. 2017, ¹⁰Tashiro et al. 2017, ¹¹Allwood et al. 2006, ¹²Allwood et al. 2009, ¹³Andrews‐Hanna et al. 2010, Lillis et al. 2013, ¹⁵Fassett & Head, 2011, ¹⁶Cabrol et al. 2003, ¹⁷Fassett & Head, 2008a, ¹⁸Goudge et al. 2018, ¹⁹Grotzinger et al. 2014, ²⁰Jakosky et al. 2017, ²¹Ehlmann & Edwards, 2014, ²²Grotzinger et al. 2014, ²³Hurowitz et al. 2017, ²⁴Squyres et al. 2006, ²⁵Ming et al. 2008

Figure 3

Metal ion catalysis of RNA degradation. Plot of oligonucleotide strand cleavage at the single ribonucleotide site as measured by urea polyacrylamide gel electrophoresis with 50 mM Fe2+ (●), 50 mM Mg2+ (■), and 50 mM Mn2+ (▲) at pH 6.7. (a) The natural logarithm of the fraction of un‐cleaved (e.g., intact) RNA‐containing oligomer with time (h) was fit to a linear regression ln[pt] = ‐kt + ln[po] and (b) the slope yielded our pseudofirst‐order rate constants (kobs(h‐1). [Fe2+]: ln(p/po) = −0.117h, R2 = 0.997; [Mg2+]: ln(p/po) = −0.038h, R2 = 0.989; [Mn2+]: ln(p/po) = −0.135h, R2 = 0.999

Figure 5

Characterization of RNA degradation kinetics. Saturation curves of Fe2 + and Mg2+ cleavage fitted to the one‐site binding model. Within the range tested, we observe greater RNA stability at pH 5.4 where the maximum rate of catalysis (Bmax) with Mg2+ is lower than with Fe2+. Experiments with Fe2+ at pH 6.7 did not reach saturation. Error bars represent SEM (n = 2)

Figure 4

RNA degradation. Incubations of the RNA‐containing oligonucleotide at pH 3.2–9 and 0–50 mM of prebiotically relevant metal. Enhanced RNA hydrolysis occurs in nearly all pH conditions. At pH 3.2, increasing concentrations of metals decrease the rate of RNA degradation. Between pH 5.4 and 8, RNA incubations containing Mg2+ are generally more stable than those containing Fe2+ or Mn2+. At pH 9, we record the most rapid metal‐catalyzed hydrolysis rates in our experiments. Precipitates were observed for both Fe2+ and Mn2+ incubations likely resulting in artificially decreased catalysis rates relative to Mg2+. Error bars represent SEM (n = 2)

Figure 6

RNA degradation by metal mixtures. Results for the basalt analog solutions tend towards less overall cleavage in Mg2+‐rich solutions (e.g., forsteritic) over Fe2+‐rich solutions (e.g., fayalitic). Degradation at pH 9 for all basalt analogs is inferred to be primarily Mg2+‐catalyzed as Fe2+ was observed to precipitate out of solution. Error bars represent SEM (n = 2)