On the origins of life's homochirality: Inducing enantiomeric excess with spin-polarized electrons.

Life as we know it is homochiral, but the origins of biological homochirality on early Earth remain elusive. Shallow closed-basin lakes are a plausible prebiotic environment on early Earth, and most are expected to have significant sedimentary magnetite deposits. We hypothesize that ultraviolet (200- to 300-nm) irradiation of magnetite deposits could generate hydrated spin-polarized electrons sufficient to induce enantioselective prebiotic chemistry. Such electrons are potent reducing agents that drive reduction reactions where the spin polarization direction can enantioselectively alter the reaction kinetics. Our estimate of this chiral bias is based on the strong effective spin-orbit coupling observed in the chiral-induced spin selectivity (CISS) effect, as applied to energy differences in reduction reactions for different isomers. In the original CISS experiments, spin-selective electron transmission through a monolayer of double-strand DNA molecules is observed at room temperature-indicating a strong coupling between molecular chirality and electron spin. We propose that the chiral symmetry breaking due to the CISS effect, when applied to reduction chemistry, can induce enantioselective synthesis on the prebiotic Earth and thus facilitate the homochiral assembly of life's building blocks.

The central dogma of biological homochirality: How does chiral information propagate in a prebiotic network?

Biological systems are homochiral, raising the question of how a racemic mixture of prebiotically synthesized biomolecules could attain a homochiral state at the network level. Based on our recent results, we aim to address a related question of how chiral information might have flowed in a prebiotic network. Utilizing the crystallization properties of the central ribonucleic acid (RNA) precursor known as ribose-aminooxazoline (RAO), we showed that its homochiral crystals can be obtained from its fully racemic solution on a magnetic mineral surface due to the chiral-induced spin selectivity (CISS) effect [Ozturk et al., arXiv:2303.01394 (2023)]. Moreover, we uncovered a mechanism facilitated by the CISS effect through which chiral molecules, such as RAO, can uniformly magnetize such surfaces in a variety of planetary environments in a persistent manner [Ozturk et al., arXiv:2304.09095 (2023)]. All this is very tantalizing because recent experiments with tRNA analogs demonstrate high stereoselectivity in the attachment of L-amino acids to D-ribonucleotides, enabling the transfer of homochirality from RNA to peptides [Wu et al., J. Am. Chem. Soc. 143, 11836 (2021)]. Therefore, the biological homochirality problem may be reduced to ensuring that a single common RNA precursor (e.g., RAO) can be made homochiral. The emergence of homochirality at RAO then allows for the chiral information to propagate through RNA, then to peptides, and ultimately through enantioselective catalysis to metabolites. This directionality of the chiral information flow parallels that of the central dogma of molecular biology-the unidirectional transfer of genetic information from nucleic acids to proteins [F. H. Crick, in Symposia of the Society for Experimental Biology, Number XII: The Biological Replication of Macromolecules, edited by F. K. Sanders (Cambridge University Press, Cambridge, 1958), pp. 138-163; and F. Crick, Nature 227, 561 (1970)].

Growth model interpretation of planet size distribution.

The radii and orbital periods of 4,000+ confirmed/candidate exoplanets have been precisely measured by the Kepler mission. The radii show a bimodal distribution, with two peaks corresponding to smaller planets (likely rocky) and larger intermediate-size planets, respectively. While only the masses of the planets orbiting the brightest stars can be determined by ground-based spectroscopic observations, these observations allow calculation of their average densities placing constraints on the bulk compositions and internal structures. However, an important question about the composition of planets ranging from 2 to 4 Earth radii (R⊕) still remains. They may either have a rocky core enveloped in a H2-He gaseous envelope (gas dwarfs) or contain a significant amount of multicomponent, H2O-dominated ices/fluids (water worlds). Planets in the mass range of 10-15 M⊕, if half-ice and half-rock by mass, have radii of 2.5 R⊕, which exactly match the second peak of the exoplanet radius bimodal distribution. Any planet in the 2- to 4-R⊕ range requires a gas envelope of at most a few mass percentage points, regardless of the core composition. To resolve the ambiguity of internal compositions, we use a growth model and conduct Monte Carlo simulations to demonstrate that many intermediate-size planets are "water worlds."

Three regimes of extrasolar planet radius inferred from host star metallicities.

Approximately half of the extrasolar planets (exoplanets) with radii less than four Earth radii are in orbits with short periods. Despite their sheer abundance, the compositions of such planets are largely unknown. The available evidence suggests that they range in composition from small, high-density rocky planets to low-density planets consisting of rocky cores surrounded by thick hydrogen and helium gas envelopes. Here we report the metallicities (that is, the abundances of elements heavier than hydrogen and helium) of more than 400 stars hosting 600 exoplanet candidates, and find that the exoplanets can be categorized into three populations defined by statistically distinct (∼4.5σ) metallicity regions. We interpret these regions as reflecting the formation regimes of terrestrial-like planets (radii less than 1.7 Earth radii), gas dwarf planets with rocky cores and hydrogen-helium envelopes (radii between 1.7 and 3.9 Earth radii) and ice or gas giant planets (radii greater than 3.9 Earth radii). These transitions correspond well with those inferred from dynamical mass estimates, implying that host star metallicity, which is a proxy for the initial solids inventory of the protoplanetary disk, is a key ingredient regulating the structure of planetary systems.

An Earth-sized planet with an Earth-like density.

Recent analyses of data from the NASA Kepler spacecraft have established that planets with radii within 25 per cent of the Earth's (R Earth symbol) are commonplace throughout the Galaxy, orbiting at least 16.5 per cent of Sun-like stars. Because these studies were sensitive to the sizes of the planets but not their masses, the question remains whether these Earth-sized planets are indeed similar to the Earth in bulk composition. The smallest planets for which masses have been accurately determined are Kepler-10b (1.42 R Earth symbol) and Kepler-36b (1.49 R Earth symbol), which are both significantly larger than the Earth. Recently, the planet Kepler-78b was discovered and found to have a radius of only 1.16 R Earth symbol. Here we report that the mass of this planet is 1.86 Earth masses. The resulting mean density of the planet is 5.57 g cm(-3), which is similar to that of the Earth and implies a composition of iron and rock.

A closely packed system of low-mass, low-density planets transiting Kepler-11.

When an extrasolar planet passes in front of (transits) its star, its radius can be measured from the decrease in starlight and its orbital period from the time between transits. Multiple planets transiting the same star reveal much more: period ratios determine stability and dynamics, mutual gravitational interactions reflect planet masses and orbital shapes, and the fraction of transiting planets observed as multiples has implications for the planarity of planetary systems. But few stars have more than one known transiting planet, and none has more than three. Here we report Kepler spacecraft observations of a single Sun-like star, which we call Kepler-11, that reveal six transiting planets, five with orbital periods between 10 and 47 days and a sixth planet with a longer period. The five inner planets are among the smallest for which mass and size have both been measured, and these measurements imply substantial envelopes of light gases. The degree of coplanarity and proximity of the planetary orbits imply energy dissipation near the end of planet formation.

Two Earth-sized planets orbiting Kepler-20.

Since the discovery of the first extrasolar giant planets around Sun-like stars, evolving observational capabilities have brought us closer to the detection of true Earth analogues. The size of an exoplanet can be determined when it periodically passes in front of (transits) its parent star, causing a decrease in starlight proportional to its radius. The smallest exoplanet hitherto discovered has a radius 1.42 times that of the Earth's radius (R(⊕)), and hence has 2.9 times its volume. Here we report the discovery of two planets, one Earth-sized (1.03R(⊕)) and the other smaller than the Earth (0.87R(⊕)), orbiting the star Kepler-20, which is already known to host three other, larger, transiting planets. The gravitational pull of the new planets on the parent star is too small to measure with current instrumentation. We apply a statistical method to show that the likelihood of the planetary interpretation of the transit signals is more than three orders of magnitude larger than that of the alternative hypothesis that the signals result from an eclipsing binary star. Theoretical considerations imply that these planets are rocky, with a composition of iron and silicate. The outer planet could have developed a thick water vapour atmosphere.

A laser frequency comb that enables radial velocity measurements with a precision of 1 cm s(-1).

Searches for extrasolar planets using the periodic Doppler shift of stellar spectral lines have recently achieved a precision of 60 cm s(-1) (ref. 1), which is sufficient to find a 5-Earth-mass planet in a Mercury-like orbit around a Sun-like star. To find a 1-Earth-mass planet in an Earth-like orbit, a precision of approximately 5 cm s(-1) is necessary. The combination of a laser frequency comb with a Fabry-Pérot filtering cavity has been suggested as a promising approach to achieve such Doppler shift resolution via improved spectrograph wavelength calibration, with recent encouraging results. Here we report the fabrication of such a filtered laser comb with up to 40-GHz (approximately 1-A) line spacing, generated from a 1-GHz repetition-rate source, without compromising long-term stability, reproducibility or spectral resolution. This wide-line-spacing comb, or 'astro-comb', is well matched to the resolving power of high-resolution astrophysical spectrographs. The astro-comb should allow a precision as high as 1 cm s(-1) in astronomical radial velocity measurements.

UV Transmission in Prebiotic Environments on Early Earth.

Ultraviolet (UV) light is likely to have played important roles in surficial origins of life scenarios, potentially as a productive source of energy and molecular activation, as a selective means to remove unwanted side products, or as a destructive mechanism resulting in loss of molecules/biomolecules over time. The transmission of UV light through prebiotic waters depends upon the chemical constituents of such waters, but constraints on this transmission are limited. Here, we experimentally measure the molar decadic extinction coefficients for a number of small molecules used in various prebiotic synthetic schemes. We find that many small feedstock molecules absorb most at short (∼200 nm) wavelengths, with decreasing UV absorption at longer wavelengths. For comparison, we also measured the nucleobase adenine and found that adenine absorbs significantly more than the simpler molecules often invoked in prebiotic synthesis. Our results enable the calculation of UV photon penetration under varying chemical scenarios and allow further constraints on plausibility and self-consistency of such scenarios. While the precise path that prebiotic chemistry took remains elusive, improved understanding of the UV environment in prebiotically plausible waters can help constrain both the chemistry and the environmental conditions that may allow such chemistry to occur.

Iron-sulfur chemistry can explain the ultraviolet absorber in the clouds of Venus.

The clouds of Venus are believed to be composed of sulfuric acid (H2SO4) and minor constituents including iron-bearing compounds, and their respective concentrations vary with height in the thick Venusian atmosphere. This study experimentally investigates possible iron-bearing mineral phases that are stable under the unique conditions within Venusian clouds. Our results demonstrate that ferric iron can react with sulfuric acid to form two mineral phases: rhomboclase [(H5O2)Fe(SO4)2·3H2O] and acid ferric sulfate [(H3O)Fe(SO4)2]. A combination of these two mineral phases and dissolved Fe3+ in varying concentrations of sulfuric acid are shown to be good candidates for explaining the 200- to 300-nm and 300- to 500-nm features of the reported unknown UV absorber. We, therefore, hypothesize a rich and largely unexplored heterogeneous chemistry in the cloud droplets of Venus that has a large effect on the optical properties of the clouds and the behavior of trace gas species throughout Venus's atmosphere.

Photoinduced charge separation and DNA self-repair depend on sequence directionality and stacking pattern.

Charge separation is one of the most common consequences of the absorption of UV light by DNA. Recently, it has been shown that this process can enable efficient self-repair of cyclobutane pyrimidine dimers (CPDs) in specific short DNA oligomers such as the GAT[double bond, length as m-dash]T sequence. The mechanism was characterized as sequential electron transfer through the nucleobase stack which is controlled by the redox potentials of nucleobases and their sequence. Here, we demonstrate that the inverse sequence T[double bond, length as m-dash]TAG promotes self-repair with higher quantum yields (0.58 ± 0.23%) than GAT[double bond, length as m-dash]T (0.44 ± 0.18%) in a comparative study involving UV-irradiation experiments. After extended exposure to UV irradiation, a photostationary equilibrium between self-repair and damage formation is reached at 33 ± 13% for GAT[double bond, length as m-dash]T and at 40 ± 16% for T[double bond, length as m-dash]TAG, which corresponds to the maximum total yield of self-repair. Molecular dynamics and quantum mechanics/molecular mechanics (QM/MM) simulations allowed us to assign this disparity to better stacking overlap between the G and A bases, which lowers the energies of the key A-˙G+˙ charge transfer state in the dominant conformers of the T[double bond, length as m-dash]TAG tetramer. These conformational differences also hinder alternative photorelaxation pathways of the T[double bond, length as m-dash]TAG tetranucleotide, which otherwise compete with the sequential electron transfer mechanism responsible for CPD self-repair. Overall, we demonstrate that photoinduced electron transfer is strongly dependent on conformation and the availability of alternative photodeactivation mechanisms. This knowledge can be used in the identification and prediction of canonical and modified DNA sequences exhibiting efficient electron transfer. It also further contributes to our understanding of DNA self-repair and its potential role in the photochemical selection of the most photostable sequences on the early Earth.

Origin of biological homochirality by crystallization of an RNA precursor on a magnetic surface.

Homochirality is a signature of life on Earth, yet its origins remain an unsolved puzzle. Achieving homochirality is essential for a high-yielding prebiotic network capable of producing functional polymers like RNA and peptides on a persistent basis. Because of the chiral-induced spin selectivity effect, which established a strong coupling between electron spin and molecular chirality, magnetic surfaces can act as chiral agents and be templates for the enantioselective crystallization of chiral molecules. Here, we studied the spin-selective crystallization of racemic ribo-aminooxazoline (RAO), an RNA precursor, on magnetite (Fe3O4) surfaces, achieving an unprecedented enantiomeric excess (ee) of about 60%. Following the initial enrichment, we then obtained homochiral (100% ee) crystals of RAO after a subsequent crystallization. Our results demonstrate a prebiotically plausible way of achieving system-level homochirality from completely racemic starting materials, in a shallow-lake environment on early Earth where sedimentary magnetite deposits are expected to be common.

UV-driven self-repair of cyclobutane pyrimidine dimers in RNA.

Nucleic acids can be damaged by ultraviolet (UV) irradiation, forming structural photolesions such as cyclobutane-pyrimidine-dimers (CPD). In modern organisms, sophisticated enzymes repair CPD lesions in DNA, but to our knowledge, no RNA-specific enzymes exist for CPD repair. Here, we show for the first time that RNA can protect itself from photolesions by an intrinsic UV-induced self-repair mechanism. This mechanism, prior to this study, has exclusively been observed in DNA and is based on charge transfer from CPD-adjacent bases. In a comparative study, we determined the quantum yields of the self-repair of the CPD-containing RNA sequence, GAU = U to GAUU (0.23%), and DNA sequence, d(GAT = T) to d(GATT) (0.44%), upon 285 nm irradiation via UV/Vis spectroscopy and HPLC analysis. After several hours of irradiation, a maximum conversion yield of ∼16% for GAU = U and ∼33% for d(GAT = T) was reached. We examined the dynamics of the intermediate charge transfer (CT) state responsible for the self-repair with ultrafast UV pump - IR probe spectroscopy. In the dinucleotides GA and d(GA), we found comparable quantum yields of the CT state of ∼50% and lifetimes on the order of several hundred picoseconds. Charge transfer in RNA strands might lead to reactions currently not considered in RNA photochemistry and may help understanding RNA damage formation and repair in modern organisms and viruses. On the UV-rich surface of the early Earth, these self-stabilizing mechanisms likely affected the selection of the earliest nucleotide sequences from which the first organisms may have developed.

Chirality-induced avalanche magnetization of magnetite by an RNA precursor.

Homochirality is a hallmark of life on Earth. To achieve and maintain homochirality within a prebiotic network, the presence of an environmental factor acting as a chiral agent and providing a persistent chiral bias to prebiotic chemistry is highly advantageous. Magnetized surfaces are prebiotically plausible chiral agents due to the chiral-induced spin selectivity (CISS) effect, and they were utilized to attain homochiral ribose-aminooxazoline (RAO), an RNA precursor. However, natural magnetic minerals are typically weakly magnetized, necessitating mechanisms to enhance their magnetization for their use as effective chiral agents. Here, we report the magnetization of magnetic surfaces by crystallizing enantiopure RAO, whereby chiral molecules induce a uniform surface magnetization due to the CISS effect, which spreads across the magnetic surface akin to an avalanche. Chirality-induced avalanche magnetization enables a feedback between chiral molecules and magnetic surfaces, which can amplify a weak magnetization and allow for highly efficient spin-selective processes on magnetic minerals.

Calibration of an astrophysical spectrograph below 1 m/s using a laser frequency comb.

We deployed two wavelength calibrators based on laser frequency combs ("astro-combs") at an astronomical telescope. One astro-comb operated over a 100 nm band in the deep red (∼ 800 nm) and a second operated over a 20 nm band in the blue (∼ 400 nm). We used these red and blue astro-combs to calibrate a high-resolution astrophysical spectrograph integrated with a 1.5 m telescope, and demonstrated calibration precision and stability sufficient to enable detection of changes in stellar radial velocity < 1 m/s.

UV Transmission in Natural Waters on Prebiotic Earth.

Ultraviolet (UV) light plays a key role in surficial theories of the origin of life, and numerous studies have focused on constraining the atmospheric transmission of UV radiation on early Earth. However, the UV transmission of the natural waters in which origins-of-life chemistry (prebiotic chemistry) is postulated to have occurred is poorly constrained. In this work, we combine laboratory and literature-derived absorption spectra of potential aqueous-phase prebiotic UV absorbers with literature estimates of their concentrations on early Earth to constrain the prebiotic UV environment in marine and terrestrial natural waters, and we consider the implications for prebiotic chemistry. We find that prebiotic freshwaters were largely transparent in the UV, contrary to assumptions in some models of prebiotic chemistry. Some waters, such as high-salinity waters like carbonate lakes, may be deficient in shortwave (≤220 nm) UV flux. More dramatically, ferrous waters can be strongly UV-shielded, particularly if the Fe2+ forms highly UV-absorbent species such as FeCN64-. Such waters may be compelling venues for UV-averse origin-of-life scenarios but are unfavorable for some UV-dependent prebiotic chemistries. UV light can trigger photochemistry even if attenuated through photochemical transformations of the absorber (e.g., eaq- production from halide irradiation), which may have both constructive and destructive effects for prebiotic syntheses. Prebiotic chemistries that invoke waters that contain such absorbers must self-consistently account for the chemical effects of these transformations. The speciation and abundance of Fe2+ in natural waters on early Earth is a major uncertainty and should be prioritized for further investigation, as it played a major role in UV transmission in prebiotic natural waters.

Shielding from UV Photodamage: Implications for Surficial Origins of Life Chemistry on the Early Earth.

UV light has been invoked as a source of energy for driving prebiotic chemistry, but such high energy photons are also known to cause damage to biomolecules and their precursors. One potential mechanism for increasing the lifetime of UV-photounstable molecules is to invoke a protection or shielding mechanism. UV shielding could either occur by the molecule in question itself (self-shielding) or by the presence of other UV-absorbing molecules. We investigate and illustrate these two shielding mechanisms as means of increasing the lifetime of 2-aminooxazole (AO), a prebiotic precursor molecule moderately susceptible to UV photodamage, with an expected half-life of 7 h on the surface of the early Earth. AO can be protected by being present in high concentrations, such that it self-shields. AO can similarly be protected by the presence of UV-absorbing nucleosides; the degree of protection depends on the concentration and identity of the nucleoside. The purine nucleosides (A, G, and I) confer more protection than the pyrimidines (C and U). We find that 0.1 mM purine ribonucleosides affords AO about the same protection as 1 mM AO self-shielding, corresponding to a lifetime enhancement of 2-3×. This suggests that only a modest yield of nucleosides can potentially allow for protection of UV photounstable molecules, and therefore this could be a plausible mechanism for protecting sensitive molecules while prebiotic synthesis is occurring simultaneously. Our findings suggest that both synthetic and degradative reactions can proceed at the same time, given various degrees of shielding.

Prebiotic photoredox synthesis from carbon dioxide and sulfite.

Carbon dioxide (CO2) is the major carbonaceous component of many planetary atmospheres, which includes the Earth throughout its history. Carbon fixation chemistry-which reduces CO2 to organics, utilizing hydrogen as the stoichiometric reductant-usually requires high pressures and temperatures, and the yields of products of potential use to nascent biology are low. Here we demonstrate an efficient ultraviolet photoredox chemistry between CO2 and sulfite that generates organics and sulfate. The chemistry is initiated by electron photodetachment from sulfite to give sulfite radicals and hydrated electrons, which reduce CO2 to its radical anion. A network of reactions that generates citrate, malate, succinate and tartrate by irradiation of glycolate in the presence of sulfite was also revealed. The simplicity of this carboxysulfitic chemistry and the widespread occurrence and abundance of its feedstocks suggest that it could have readily taken place on the surfaces of rocky planets. The availability of the carboxylate products on early Earth could have driven the development of central carbon metabolism before the advent of biological CO2 fixation.

Ribose Alters the Photochemical Properties of the Nucleobase in Thionated Nucleosides.

Substitution of exocyclic oxygen with sulfur was shown to substantially influence the properties of RNA/DNA bases, which are crucial for prebiotic chemistry and photodynamic therapies. Upon UV irradiation, thionucleobases were shown to efficiently populate triplet excited states and can be involved in characteristic photochemistry or generation of singlet oxygen. Here, we show that the photochemistry of a thionucleobase can be considerably modified in a nucleoside, that is, by the presence of ribose. Our transient absorption spectroscopy experiments demonstrate that thiocytosine exhibits 5 times longer excited-state lifetime and different excited-state absorption features than thiocytidine. On the basis of accurate quantum chemical simulations, we assign these differences to the dominant population of a shorter-lived triplet nπ* state in the nucleoside and longer-lived triplet ππ* states in the nucleobase. This explains the distinctive photoanomerziation of thiocytidine and indicates that the nucleoside will be a less efficient phototherapeutic agent with regard to singlet oxygen generation.

In-situ determination of astro-comb calibrator lines to better than 10 cm s(-1).

Improved wavelength calibrators for high-resolution astrophysical spectrographs will be essential for precision radial velocity (RV) detection of Earth-like exoplanets and direct observation of cosmological deceleration. The astro-comb is a combination of an octave-spanning femtosecond laser frequency comb and a Fabry-Pérot cavity used to achieve calibrator line spacings that can be resolved by an astrophysical spectrograph. Systematic spectral shifts associated with the cavity can be 0.1-1 MHz, corresponding to RV errors of 10-100 cm/s, due to the dispersive properties of the cavity mirrors over broad spectral widths. Although these systematic shifts are very stable, their correction is crucial to high accuracy astrophysical spectroscopy. Here, we demonstrate an in-situ technique to determine the systematic shifts of astro-comb lines due to finite Fabry-Pérot cavity dispersion. The technique is practical for implementation at a telescope-based spectrograph to enable wavelength calibration accuracy better than 10 cm/s.