Special Issue "Origin of Life - Feature Papers"

Abstract: There are several ways that our species might try to send a message to another species separated from us by space and/or time. Synthetic biology might be used to write an epitaph to our species, or simply “Kilroy was here”, in the genome of a bacterium via the patterns of either (1) the codons to exploit Life's non-equilibrium character or (2) the bases themselves to exploit Life's quasi-equilibrium character. We suggest here how DNA movies might be designed using such patterns. We also suggest that a search for mechanisms to create and preserve such patterns might lead to a better understanding of modern cells. Finally, we argue that the cutting-edge microbiology and synthetic biology needed for the Kilroy project would put origin-of-life studies in the vanguard of research.

Abstract: On Earth, marine anaerobic methane oxidation (AOM) can be driven by the microbial reduction of sulfate, iron, and manganese. Here, we have further characterized marine sediment incubations to determine if the mineral dependent methane oxidation involves similar microorganisms to those found for sulfate-dependent methane oxidation. Through FISH and FISH-SIMS analyses using ¹³C and ¹⁵N labeled substrates, we find that the most active cells during manganese dependent AOM are primarily mixed and mixed-cluster aggregates of archaea and bacteria. Overall, our control experiment using sulfate showed two active bacterial clusters, two active shell aggregates, one active mixed aggregate, and an active archaeal sarcina, the last of which appeared to take up methane in the absence of a closely-associated bacterial partner. A single example of a shell aggregate appeared to be active in the manganese incubation, along with three mixed aggregates and an archaeal sarcina. These results suggest that the microorganisms (e.g., ANME-2) found active in the manganese-dependent incubations are likely capable of sulfate-dependent AOM. Similar metabolic flexibility for Martian methanotrophs would mean that the same microbial groups could inhabit a diverse set of Martian mineralogical crustal environments. The recently discovered seasonal Martian plumes of methane outgassing could be coupled to the reduction of abundant surface sulfates and extensive metal oxides, providing a feasible metabolism for present and past Mars. In an optimistic scenario Martian methanotrophy consumes much of the periodic methane released supporting on the order of 10,000 microbial cells per cm² of Martian surface. Alternatively, most of the methane released each year could be oxidized through an abiotic process requiring biological methane oxidation to be more limited. If under this scenario, 1% of this methane flux were oxidized by biology in surface soils or in subsurface aquifers (prior to release), a total of about 10²⁰ microbial cells could be supported through methanotrophy with the cells concentrated in regions of methane release.

Abstract: I discuss briefly the history of the origin of life field, focusing on the “Miller” era of prebiotic synthesis, through the “Orgel” era seeking enzyme free template replication of single stranded RNA or similar polynucleotides, to the RNA world era with one of its foci on a ribozyme with the capacity to act as a polymerase able to copy itself. I give the history of the independent invention in 1971 by T. Ganti, M. Eigen and myself of three alternative theories of the origin of molecular replication: the Chemotron, the Hypercycle, and Collectively Autocatalytic Sets, CAS, respectively. To date, only collectively autocatalytic DNA, RNA, and peptide sets have achieved molecular reproduction of polymers. Theoretical work and experimental work on CAS both support their plausibility as models of openly evolvable protocells, if housed in dividing compartments such as dividing liposomes. My own further hypothesis beyond that of CAS in themselves, of their formation as a phase transition in complex chemical reaction systems of substrates, reactions and products, where the molecules in the system are candidates to catalyze the very same reactions, now firmly established as theorems, awaits experimental proof using combinatorial chemistry to make libraries of stochastic DNA, RNA and/or polypeptides, or other classes of molecules to test the hypothesis that molecular polymer reproduction has emerged as a true phase transition in complex chemical reaction systems. I remark that my colleague Marc Ballivet of the University of Geneva and I, may have issued the first publications discussing what became combinatorial chemistry, in published issued patents in 1987, 1989 and later, in this field.

Abstract: Life is an inordinately complex unsolved puzzle. Despite significant theoretical progress, experimental anomalies, paradoxes, and enigmas have revealed paradigmatic limitations. Thus, the advancement of scientific understanding requires new models that resolve fundamental problems. Here, I present a theoretical framework that economically fits evidence accumulated from examinations of life. This theory is based upon a straightforward and non-mathematical core model and proposes unique yet empirically consistent explanations for major phenomena including, but not limited to, quantum gravity, phase transitions of water, why living systems are predominantly CHNOPS (carbon, hydrogen, nitrogen, oxygen, phosphorus, and sulfur), homochirality of sugars and amino acids, homeoviscous adaptation, triplet code, and DNA mutations. The theoretical framework unifies the macrocosmic and microcosmic realms, validates predicted laws of nature, and solves the puzzle of the origin and evolution of cellular life in the universe.

Abstract: The paper develops the Life Origination Hydrate Hypothesis (LOH-hypothesis), according to which living-matter simplest elements (LMSEs, which are N-bases, riboses, nucleosides, nucleotides), DNA- and RNA-like molecules, amino-acids, and proto-cells repeatedly originated on the basis of thermodynamically controlled, natural, and inevitable processes governed by universal physical and chemical laws from CH₄, niters, and phosphates under the Earth's surface or seabed within the crystal cavities of the honeycomb methane-hydrate structure at low temperatures; the chemical processes passed slowly through all successive chemical steps in the direction that is determined by a gradual decrease in the Gibbs free energy of reacting systems. The hypothesis formulation method is based on the thermodynamic directedness of natural movement and consists ofan attempt to mentally backtrack on the progression of nature and thus reveal principal milestones alongits route. The changes in Gibbs free energy are estimated for different steps of the living-matter origination process; special attention is paid to the processes of proto-cell formation. Just the occurrence of the gas-hydrate periodic honeycomb matrix filled with LMSEs almost completely in its final state accounts for size limitation in the DNA functional groups and the nonrandom location of N-bases in the DNA chains. The slowness of the low-temperature chemical transformations and their “thermodynamic front” guide the gross process of living matter origination and its successive steps. It is shown that the hypothesis is thermodynamically justified and testable and that many observed natural phenomena count in its favor.

Abstract: This problem-oriented, exploratory and hypothesis-driven discourse toward the unknown combines several basic tenets: (i) a photo-active metal sulfide scenario of primal biogenesis in the porespace of shallow sedimentary flats, in contrast to hot deep-sea hydrothermal vent conditions; (ii) an inherently complex communal system at the common root of present life forms; (iii) a high degree of internal compartmentalization at this communal root, progressively resembling coenocytic (syncytial) super-cells; (iv) a direct connection from such communal super-cells to proto-eukaryotic macro-cell organization; and (v) multiple rounds of micro-cellular escape with streamlined reductive evolution—leading to the major prokaryotic cell lines, as well as to megaviruses and other viral lineages. Hopefully, such nontraditional concepts and approaches will contribute to coherent and plausible views about the origins and early life on Earth. In particular, the coevolutionary emergence from a communal system at the common root can most naturally explain the vast discrepancy in subcellular organization between modern eukaryotes on the one hand and both archaea and bacteria on the other.

Abstract: The invariance principle of enzyme enantioselectivity must be absolute because it is absolutely essential to the homochiral biological world. Most enzymes are strictly enantioselective, and tryptophanase is one of the enzymes with extreme absolute enantioselectivity for L-tryptophan. Contrary to conventional knowledge about the principle, tryptophanase becomes flexible to catalyze D-tryptophan in the presence of diammonium hydrogenphosphate. Since D-amino acids are ordinarily inert or function as inhibitors even though they are bound to the active site, the inhibition behavior of D-tryptophan and several inhibitors involved in this process was examined in terms of kinetics to explain the reason for this flexible enantioselectivity in the presence of diammonium hydrogenphosphate. Diammonium hydrogenphosphate gave tryptophanase a small conformational change so that D-tryptophan could work as a substrate. As opposed to other D-amino acids, D-tryptophan is a very bulky amino acid with a benzene ring in its heterocyclic moiety, and so we suggest that this structural feature makes the catalysis of D-tryptophan degradation possible, consequently leading to the flexible enantioselectivity. The present results not only help to understand the mechanism of enzyme enantioselectivity, but also shed light on the origin of homochirality.