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NASA NTRS2012

Processes that Drove the Transition from Chemistry to Biology: Concepts and Evidence

Two properties are particularly germane to the transition from chemistry to biology. One is the emergence of complex molecules (polymers) capable of performing non-trivial functions, such as catalysis, energy transduction or transport across cell walls. The other is the ability of several functions to work in concert to provide reproductive advantage to systems hosting these functions. Biological systems exhibit these properties at remarkable levels of efficiency and accuracy in a way that appears effortless. However, dissection of these properties reveals great complexities that are involved. This opens a question: how a simple, ancestral system could have acquired the required properties? Other questions follow. What are the chances that a functional polymer emerges at random? What is the minimum structural complexity of a polymer to carry out a function at a reasonable level of efficiency? Can we identify concrete, protobiologically plausible mechanisms that yield advantageous coupling between different functions? These and similar questions are at the core of the main topic of this session: how soulless chemistry became life? Clearly, we do not have complete answers to any of these questions. However, in recent years a number of new and sometimes unexpected clues have been brought to light. Of particular interest are proteins because they are the main functional polymers in contemporary cells. The emergence of protein functions is a puzzle. It is widely accepted that a well ]defined, compact structure (fold) is a prerequisite for function. It is equally widely accepted that compact folds are rare among random amino acid polymers. Then, how did protein functionality start? According to one hypothesis well folded were preceded by their poorly folded, yet still functional ancestors. Only recently, however, experimental evidence supporting this hypothesis has been presented. In particular, a small enzyme capable of ligating two RNA fragments with the rate of 106 above background was evolved in vitro. This enzyme does not look like any contemporary protein. It is very flexible and its structure is kept together just by a single salt bridge between a charged residue and a coordinating zinc. A similar picture emerges from studies of simple transmembrane channels that mimic those in ancestral cells. Again, they are extremely flexible and do not form a conventional pore. Yet, they efficiently mediate ion transport. Studies on simple proteins that are on-going in several laboratories hold promise of revealing crucial links between chemical and biological catalysis and other ubiquitous cell functions. Interaction between composition, growth and division of protobiologically relevant vesicles and metabolic reactions that they encapsulate is an example of coupling between simple functions that promotes reproduction and evolution. Recent studies have demonstrated possible mechanisms by which vesicles might have evolved their composition from fatty acids to phospholipids, thus facilitating a number of new cellular functions. Conversely, it has been also demonstrated that an encapsulated metabolism might drive vesicle division. These are, again, examples of processes that might have driven the transition from chemistry to biology.

Pohorille, Andrew↗

NASA NTRS2012

Microbial Lipid and C Isotopic Biosignatures of a Unique Community at Grand Prismatic Spring, Yellowstone National Park

The microbial communities found in modern hot springs are considered analogs to ones that may have existed in hydrothermal systems on the early Earth and possibly Mars. Our goal was to characterize the microbial biosignatures and to assess the preservation of organic matter in the silica-depositing Grand Prismatic Spring in Yellowstone National Park. This study combines 16S rRNA surveys, lipid biomarkers, and C isotopes to query, "Who's there and what are they doing?" On the edge of the approximately 90 m diameter blue vent pool (56.1 C, pH 8.5), a floating green streamer community grew over a benthic pink community. The membrane lipids in the green streamers and pink mat were composed of unusual ester-linked fatty acids, indicating the presence of novel bacterial groups. In particular, we discovered a series of 2-methyl and 2,X-dimethyl phospholipid fatty acids (C18-22). We are attempting to use the 16S rRNA surveys to link these compounds to source organisms. Wax esters, biomarkers for Chloroflexi, were present in both communities, but displayed different profiles. A higher proportion of branched wax esters were found in the green streamers, and were associated with a relatively high concentration of long-chain di- and trienes (C29-31). This suggests that Chloroflexus primarily grew in the green streamers, while a pink mat of Roseiflexus grew on the sinter substrate underneath. Cyanobacterial alkanes were found in the green streamers (n-C17, 7-, 6- and 5-monomethyl-C17, 7,11-dimethyl-C17, n-C19, n-C19:1). We also detected a series of monoalkylglycerylethers and geologically relevant hopanoids in both communities. Carbon isotope analyses indicated that Chloroflexus was growing photoheterotrophically using cyanobacterial photosynthate. Roseiflexus also traditionally grows photoheterotrophically, but the C isotopic signatures of the lipids in the pink mat were approximately 10 %0 lighter than the cyanobacterial and Chloroflexus lipids, indicating a potentially novel metabolic mechanism or prior secondary reworking of substrates before reaching Roseiflexus. This arrangement of Synechococcus-Chloroflexus green streamers floating over a benthic pink community of Roseiflexus is different from the classical laminated Synechococcus-Chloroflexi mats at Octopus Hot Spring.

Jahnke, Linda↗

NASA NTRS2016

Microorganisms, Organic Carbon, and Their Relationship with Oxidant Activity in Hyper-Arid Mars-Like Soils: Implications for Soil Habitability

Soil samples from the hyper-arid region in the Atacama 23 Desert in Southern Peru (La Joya Desert) were analyzed for total and labile organic carbon (TOC & LOC), phospholipid fatty acids analysis (PLFA), quantitative real time polymerase chain reaction (qRT-PCR), 4',6- diamidino-2-phenylindole (DAPI)-fluorescent microscopy, culturable microorganisms, and oxidant activity, in order to understand the relationship between the presence of organic matter and microorganisms in these types of soils. TOC content levels were similar to the labile pool of carbon suggesting the absence of recalcitrant carbon in these soils. The range of LOC was from 2 to 60 micro-g/g of soil. PLFA analysis indicated a maximum of 2.3 x 10(exp 5) cell equivalents/g. Culturing of soil extracts yielded 1.1 x 10(exp 2)-3.7 x 10(exp 3) CFU/g. qRT-PCR showed between 1.0 x 10(exp 2) and 8 x 10(exp 3) cells/g; and DAPI fluorescent staining indicated bacteria counts up to 5 x 104 cells/g. Arid and semiarid samples (controls) showed values between 10(exp 7) and 10(exp 11) cells/g with all of the methods used. Importantly, the concentration of microorganisms in hyper-arid soils did not show any correlation with the organic carbon content; however, there was a significant dependence on the oxidant activity present in these soil samples evaluated as the capacity to decompose sodium formate in 10 hours. We suggest that the analysis of oxidant activity could be a useful indicator of the microbial habitability in hyper-arid soils, obviating the need to measure water activity over time. This approach could be useful in astrobiological studies on other worlds.

Mars-like soils↗

NASA NTRS2018

Simple Ion Channels: From Structure to Electrophysiology and Back

A reliable way to establish whether our understanding of a channel is satisfactory is to reproduce its measured ionic conductance over a broad range of applied voltages in computer simulations. In molecular dynamics (MD), this can be done by way of applying an external electric field to the system and counting the number of ions that traverse the channel per unit time. Since this approach is computationally very expensive, we have developed a markedly more efficient alternative in which MD is combined with the electrodiffusion (ED) equation. In this approach, the assumptions of the ED equation can be rigorously tested, and the precision and consistency of the calculated conductance can be determined. We have demonstrated that the full current/voltage dependence and the underlying free energy profile for a simple channel can be reliably calculated from equilibrium or non-equilibrium MD simulations at a single voltage. To carry out MD simulations, a structural model of a channel has to be assumed, which is an important constraint, considering that high-resolution structures are available for only very few simple channels. If the comparison of calculated ionic conductance with electrophysiological data is satisfactory, it greatly increases our confidence that the structure and the function are described sufficiently accurately. We examined the validity of the ED for several channels embedded in phospholipid membranes - four naturally occurring channels: trichotoxin, alamethicin, p7 from hepatitis C virus (HCV) and Vpu from the HIV-1 virus, and a synthetic, hexameric channel, formed by a 21-residue peptide that contains only leucine and serine. All these channels mediate transport of potassium and chloride ions. It was found that the ED equation is satisfactory for these systems. In some of them experimental and calculated electrophysiological properties are in good agreement, whereas in others there are strong indications that the structural models are incorrect.

molecular dynamics (MD↗

NASA NTRS2018

Transitory Microbial Habitat in the Hyperarid Atacama Desert

Traces of life are nearly ubiquitous on Earth. However, a central unresolved question is whether these traces always indicate an active microbial community or whether, in extreme environments, such as hyperarid deserts, they instead reflect just dormant or dead cells. Although microbial biomass and diversity decrease with increasing aridity in the Atacama Desert, we provide multiple lines of evidence for the presence of an at times metabolically active, microbial community in one of the driest places on Earth. We base this observation on four major lines of evidence: (i) a physico-chemical characterization of the soil habitability after an exceptional rain event, (ii) identified biomolecules indicative of potentially active cells [e.g., presence of ATP, phospholipid fatty acids (PLFAs), metabolites, and enzymatic activity], (iii) measurements of in situ replication rates of genomes of uncultivated bacteria reconstructed from selected samples, and (iv) microbial community patterns specific to soil parameters and depths. We infer that the microbial populations have undergone selection and adaptation in response to their specific soil microenvironment and in particular to the degree of aridity. Collectively, our results highlight that even the hyperarid Atacama Desert can provide a habitable environment for microorganisms that allows them to become metabolically active following an episodic increase in moisture and that once it decreases, so does the activity of the microbiota. These results have implications for the prospect of life on other planets such as Mars, which has transitioned from an earlier wetter environment to today’s extreme hyperaridity.

Schulze-Makuch, Dirk↗

NASA NTRS2019

Emergence of Simple Ion Channels by Self-Assembly of Short Peptides

As protocells transitioned from structures bound by membranes made of simple amphiphiles, such as fatty acids, to structures containing phospholipid membranes, they became nearly impermeable to charged species. Yet, the ability to transport ions across membranes was vital to regulating cellular volume, pH homeostasis, generating energy and sensing the environment. For this reason, life evolved ion channels, protein structures surrounding water-filled pores in the membrane that facilitated ion transport. In contemporary cells, ion channels are complex protein assemblies. Could the same function be carried out, even if less efficiently and selectively, by much simpler peptides at the origins of life? To answer this question, we turned to trichogen (GAIV), an 11-residue peptide that was found to permeabilize membrane, causing leakage of the vesicle content including ions. Since GAIV is synthesized non-gnomically, it represents as excellent model for the earliest, poorly optimized channels. Understanding the mechanism by which short peptides, such as GAIV, mediate ion transport across membranes provides crucial information on the emergence, structure and the mechanism of action of the earliest ion channels. In this study, we used extensive molecular dynamics (MD) simulations to investigate directly spontaneous assembly of GAIV peptide and its structural dynamics, the formation of an induced water pore across the membrane and consequently ion conduction through the membrane.

Wei, Chenyu↗

NASA NTRS2020

Ion Channels – From Structure to Electrophysiology and Back

A reliable way to establish whether our understanding of a channel is satisfactory is to reproduce its measured ionic conductance over a broad range of applied voltages in computer simulations. In molecular dynamics (MD), this can be done by way of applying an external electric field to the system and counting the number of ions that traverse the channel per unit time. Since this approach is computationally very expensive, we have developed a markedly more efficient alternative in which MD is combined with the electrodiffusion (ED) equation. In this approach, the assumptions of the ED equation can be rigorously tested, and the precision and consistency of the calculated conductance can be determined. We have demonstrated that the full current/voltage dependence and the underlying free energy profile for a simple channel can be reliably calculated from equilibrium or non-equilibrium MD simulations at a single voltage. Free energy profiles can be obtained from non-equilibrium simulations without a loss of accuracy even without the knowledge of diffusion coefficient. To carry out MD simulations, a structural model of a channel has to be assumed, which is an important constraint, considering that high-resolution structures are available for only very few simple channels. If the comparison of calculated ionic conductance with electrophysiological data is satisfactory, it greatly increases our confidence that the structure and the function are described sufficiently accurately. We examined the validity of the ED for several channels embedded in phospholipid membranes - four naturally occurring channels: trichotoxin, alamethicin, p7 from hepatitis C virus (HCV) and Vpu from the HIV-1 virus, a synthetic, hexameric channel, formed by a 21-residue peptide that contains only leucine and serine and a bacterial pentameric ligand-gated ion channel, GLIC. All these channels mediate transport of potassium and chloride ions. It was found that the ED equation is satisfactory for these systems. In some of them, experimental and calculated electrophysiological properties are in good agreement, whereas in others there are strong indications that the structural models are incorrect.

Pohorille, Andrew↗

NASA NTRS1992

Permeability of lipid bilayers to amino acids and phosphate

Permeability coefficients for amino acid classes, including neutral, polar, hydrophobic, and charged species, were measured and compared with values for other ionic solutes such as phosphate. The rates of efflux of glycine, lysine, phenylalanine, serine and tryptophan were determined after they were passively entrapped in large unilamellar vesicles (LUVs) composed of egg phosphatidylcholine (EPC) or dimyristoylphosphatidylcholine (DMPC). The following permeability coefficients were obtained for: glycine, 5.7 x 10(-12) cm s-1 (EPC), 2.0 x 10(-11) cm s-1 (DMPC); serine, 5.5 x 10(-12) cm s-1 (EPC), 1.6 x 10(-11) cm s-1 (DMPC); lysine, 5.1 x 10(-12) cm s-1 (EPC), 1.9 x 10(-11) cm s-1 (DMPC); tryptophan, 4.1 x 10(-10) cm s-1 (EPC); and phenylalanine, 2.5 x 10(-10) cm s-1 (EPC). Decreasing lipid chain length increased permeability slightly, while variations in pH had only minor effects on the permeability coefficients of the amino acids tested. Phosphate permeability was in the range of 10(-12)-10(-13) cm s-1 depending on the pH of the medium. The values for the polar and charged amino acids were surprisingly similar to those previously measured for monovalent cations such as sodium and potassium, which are in the range of 10(-12)-10(-13) cm s-1, depending on conditions and the lipid species used. This observation suggests that the permeation rates for the neutral, polar and charged amino acids are controlled by bilayer fluctuations and transient defects, rather than partition coefficients and Born energy barriers. The results are relevant to the permeation of certain peptides into lipid bilayers during protein translocation and membrane biogenesis.

NASA Discipline Exobiology↗