The Grayness of the Origin of Life

Abstract

In the search for life beyond Earth, distinguishing the living from the non-living is paramount. However, this distinction is often elusive, as the origin of life is likely a stepwise evolutionary process, not a singular event. Regardless of the favored origin of life model, an inherent "grayness" blurs the theorized threshold defining life. Here, we explore the ambiguities between the biotic and the abiotic at the origin of life. The role of grayness extends into later transitions as well. By recognizing the limitations posed by grayness, life detection researchers will be better able to develop methods sensitive to prebiotic chemical systems and life with alternative biochemistries.

Keywords: agnostic biosignatures; evolutionary transitions; lipids; metalloenzymes; meteoritic organics; origin of life; pre-RNAs; prebiotic evolution; thioesters.

Figure 1

Illustration of the three macromolecules used by life on Earth, as both constituent parts (a,c,e) and larger-scale structures (b,d,f), which fulfill the roles described in the chemoton model: metabolism, compartmentalization, and information storage. (a) A polypeptide consisting of eight amino acids. (b) Spinach ferredoxin protein structure, PDB 1A70, showing alpha-helices, beta-pleated sheets and loops structures [19]. (c) A phospholipid containing fatty acid tails made of repeating 2C units. (d) A segment of a phospholipid bilayer, which forms cell membranes. (e) A short chain of DNA, illustrating the Watson–Crick nitrogenous bases. (f) An A-form double helix showing the structure of DNA storage.

Figure 2

An illustration of amino acid chirality, amino acid structural diversity, and amino acid stable isotope compositions ($\delta$D, the isotopic ratio of D/H in the sample relative to Standard Mean Ocean Water (SMOW), an isotopic standard for water, and ${\delta }^{13}$C, the isotopic ratio of ${}^{13}$C/${}^{12}$C in the sample relative to Pee Dee Belemnite (PDB) standard for carbon) across an abiotic-to-biotic spectrum. Here, the abiotic and biotic end-members are defined by the Murchison (CM2) carbonaceous chondrite (a structurally diverse and well characterized abiotic reference) and terrestrial biology, respectively. Chirality: Amino acids of abiotic origins are often racemic or near-racemic, while amino acids in terrestrial biology exhibit distinct homochirality. Structural diversity: Amino acids are categorized by the position of the amine group relative to the acid group in the chemical structure (i.e., whether the amine group is positioned at the $\alpha$, $\beta$, $\gamma$, $\delta$, or $ϵ$ carbon). For the abiotic end-member, the lengths of the bars represent the number of aliphatic amino acids identified to date in Murchison for each specific category (see Glavin et al., 2018 [23] and references therein). For the biotic end-member, the single bar represents the simple distribution of 20 proteinogenic $\alpha$-amino acids. Stable isotopes: While $\delta$D and ${\delta }^{13}$C values can vary widely depending on the source and history of the sample, meteoritic amino acids of extraterrestrial origins generally exhibit highly positive $\delta$D values and often have ${\delta }^{13}$C values above 0‰ (see Elsila et al., 2012 [36] and references therein). In contrast, amino acids of terrestrial origins generally have $\delta$D and ${\delta }^{13}$C values that fall below 0‰.

Figure 3

Proposed pre-RNA molecular information systems organized from least to most similar to RNA. From left to right: (1) HCN polymer, (2) peptide nucleic acid (PNA), using an amino acid backbone, (3) threose nucleic acid (TNA), which uses the simpler 4C sugar, and (4) p-RNA which uses the pyranose form of ribose.

Figure 4

Grayness exists in the transition from catalysis via metal sulfides and metal oxides present in the abiotic environment to the use of similar structures in the active site of modern metalloenzymes. Here, we see the structure of an abiotic iron cyanocarbonyl complex, recently identified in some carbonaceous chondrites, and compare it to the active site structure of Fe-Ni hydrogenase. Note the active site ligands CN and CO, unusual in biology. Figure adapted from Ref. [68].

Figure 5

Possible evolution of thioester and phosphate-based energy currencies. A potential progression of small, prebiotically plausible energy currencies (S-methyl thioacetate, acetyl phosphate; (left) to those used in extant biochemistry (acetyl-CoA, adenosine triphosphate; (right) is shown. Grayness exists in between these endpoints (pantetheine thioester and pyrophosphate).