The recent research activities performed under the umbrella of the Minerva Center for Life Under Extreme Planetary Conditions follows planetary and astrobiological themes, also outlined in the original center proposal. We organize the summary here around these four themes that serve to unify our research interests: Planetary Formation and Evolution, Early Life, Origin of Life, and Extremophiles.

Planetary Formation and Evolution

Under this broad topic of planetary evolution and habitability, we have studied aspects of the early conditions on planetary bodies in the solar system, and specifically the role of impacts in their early evolution. We have continued our investigation in the formation of Earth’s Moon by multiple impacts, and evaluated the dynamical paths followed by multi-moon systems. This theory has implications not only for the ancient Moon, but also for the early thermal state of Earth itself. In a related idea, we published a study on the possible origin of a class of asteroids from Mars as a result of a planet-scale impact. This study examined the spectral signature of these objects which points to a planetary origin, as well as the dynamics governing their capture. If correct, this would be the first identification of an asteroidal body from a planetary origin, and would offer direct access to a sample from the deep mantle material of Mars (without the need for drilling). The planetary-scale impacts implicated govern the early conditions on the young planets, and their timing determine the timing the transition to habitability.

The state and distribution of water and water ice on various bodies is central to the question of life in the past, as well as resource utilization in the future. Several recent studies addressed this question in the context of the lunar high-latitudes, where water ice deposits have been first speculated and later measured to exist. Our work focused on modeling the thermal state of the lunar regolith, whose temperature variations govern the stability and present distribution of ice on the Moon. On Mars, the water ice harbors a record of past climate, and it an ongoing study, we published results on the expected vertical distribution of hydrogen isotopes that may be used to probe past climate oscillations that are not recorded in the physical stratigraphy.

Exoplanets continue to provide new discoveries that stimulate theories on planet formation and evolution. In studies led by the Minerva Center postdoc Dr. Aviv Ofir, we published a new technique designed to detect the gravitational perturbations of exoplanet on each other; this technique is more sensitive than its predecessors, and using it we were able to detect > 100 new signals due to potential exoplanets, many unseen directly. These measurements enable place constraints on the mass, and hence density and composition not otherwise possible. We also take part in the international CARMENES project, which has provided some of the most exciting recent discoveries of neighboring planets, such as our nearest neighbor Proxima b – an Earthlike planet in the habitable zone, and Bernard Star b – a super-Earth near the snowline of an M-Dwarf (depicted here). Both of these, as well as other results from this collaboration, were highly reported in the media.

Early Life

Over the past two years we continued to study the long time scale evolution of habitability on Earth and Mars. In several studies, we combined laboratory experiments and numerical models to constrain the chemistry of the early oceans, the mineralogy of primary marine precipitates, and the implications for the early biosphere and biogeochemical cycles. Using a coupled model of the biogeochemical cycles of the major elements in seawater, we constrained the long-term evolution of seawater chemistry and pH, providing the first systematic estimate of pH over Earth history. We performed a series of experiments to constrain the iron-bearing precipitates from early iron-rich seawater, and incorporated the findings into a model of the iron cycle to constrain the concentrations of iron in early seawater, with implications for early metabolic activity. In ongoing work, we are experimentally exploring the implications of our findings for the budgets of several bio-essential nutrients and metals. We were involved in an experimental investigation of the kinetics of the reaction of cyanide (HCN) with various sulfur-bearing compounds, and the degradation of the thiocyanate (SCN-) product under anoxic conditions. We find that HCN concentrations were likely much lower in the early ocean than previously estimated, with implications for the involvement of this molecule in prebiotic organic synthesis. In addition to experiments and numerical models, we employed the study of modern analogues for ancient environments to provide insight into these environments. Specifically, we were involved in the development and exploration of an alpine spring as an analogue to interfaces between anoxic-ferruginous (O₂-poor, Fe-rich), anoxic-sulfidic (O₂-poor, H₂S-rich) and oxic (O₂-rich) water masses, which are thought to have existed early in Earth’s history. Especially the sulfidic environments pose a challenge to most lifeforms, due to the toxicity of H₂S.

In another line of investigation, we explored the consequences of disequilibrium chemistry on the isotopic composition of sulfur, carbon and oxygen in common minerals in sedimentary rocks. The isotopic composition of such minerals are valuable sources of information on ancient environments and biological activity in them. In a series of theoretical and experimental studies, we developed a conceptual and practical framework with which to understand disequilibrium isotopic compositions in carbonate minerals, which are some of the most widely used proxies for climate and for biological activity in the ocean. We are continuing to perform experiments and develop models in an attempt to provide a complete set of internally consistent isotopic fractionation factors for the dissolved inorganic carbon system. In a second line of investigation, we combined culture experiments and models of isotopic fractionation during microbial sulfate reduction to understand the controls on the isotopic composition of sulfur in marine sedimentary rocks. We are in the final stages of development of similar bioisotopic models for methanogenesis. Together with microbial sulfate reduction, methanogenesis is considered to be one of the earliest metabolisms, and the bio-isotopic models are expected to allow a more robust understanding of isotopic signals preserved in Earth’s earliest sedimentary rocks.

Origin of Life

Recent work focused on the publication a retrospective review on our work on the Graded Autocatalysis Replication Domain (GARD) model (Armstrong et al., 2018) and its relevance to life’s origin under extreme conditions. The review, published earlier this year (Lancet et al., 2018), summarized 42 papers written by us on the model, which offers a novel vista on how life may have arisen on planet earth. One of the key features of the model is its focus on lipid assemblies as the first replicators, and a key conclusion is that life’s emergence is a relatively high probability event. Another is a careful assessment of the validity of the autocatalytic set school of thought, seeking evidence for its legitimacy as a bona fide scenario for life’s origin. Further, unlike the widely invoked model of “RNA world”, the “Lipid World” model is much more compatible with extreme conditions, which means that the first relevant events could have occurred on planet earth just after the oceans condensed, and temperatures were as high as 100℃, or even 230℃, if one accepts the scenario of high pressure CO₂ atmosphere.

We have also performed studied the relevance of the GARD model in view of a recent breakthrough publication that has reported complex organic molecules emanating from the water ocean of Saturn’s moon Enceladus (PMID: 29950623). Based on detailed chemical scrutiny, the authors invoke complex polymeric carbon-rich compounds with mass of 1000 atomic units or more, immersed in a moon-wide subglacial ocean at temperatures of above 100 ℃. One may then ask which origin of life scenarios appears more consistent with this report. We did this based on studies of extracts of carbonaceous chondritic meteorites published by Prof. Philippe Schmitt-Kopplin from the Helmholtz-Zentrum (Muenchen, Germany). In collaboration with the author, we reanalyzed the data, revealing that the majority of compounds dissolved or chemically broken out of the polymers are lipid-like amphiphiles, and that the much more polar compounds relevant to the RNA world origin scenario are rare. This appears to be a first direct analysis of what constitutes a “prebiotic soup”, which provides strong support to our Lipid World scenario. These results were reported at the European Astrobiology Network Association held at the Free University Berlin 24-28 September 2018 (Lancet, 2018; Kahana & Lancet, 2018).

A newly established collaboration with Prof. Christian Mayer's from the University of Duisburg-Essen (Essen, Germany) is examining the GARD lipid world model by nuclear magnetic resonance experiments. We ask what are the thermodynamic and kinetic parameters that allow small heterogeneous assemblies of lipid-like compounds (lipid micelles) to generate the specific interactions allowing the assemblies to grow homeostatically, namely with conservation of lipid concentrations, a key feature of the GARD model.

Extremophiles

Hypersaline environments with salt concentrations up to NaCl saturation are inhabited by a great diversity of microorganisms belonging to the three domains of life. They all must cope with the low water activity of their environment, but different strategies exist to provide osmotic balance of the cells' cytoplasm with the salinity of the medium. One option used by many halophilic Archaea and a few representatives of the Bacteria is to accumulate salts, mainly KCl and to adapt the entire intracellular machinery to function in the presence of molar concentrations of salts. A more widespread option is the synthesis or accumulation of organic osmotic, so-called compatible solutes. We have reviewed the mechanisms of osmotic adaptation in a number of model organisms, including the KCl accumulating Halobacterium salinarum (Archaea) and Salinibacter ruber (Bacteria), Halomonas elongata as a representative of the Bacteria that synthesize organic osmotic solutes, eukaryotic microorganisms including the unicellular green alga Dunaliella salina and the black yeasts Hortaea werneckii and the basidiomycetous Wallemia ichthyophaga, which use glycerol and other compatible solutes. The strategies used by these model organisms and by additional halophilic microorganisms presented were compared to obtain an integrative picture of the adaptations to life at high salt concentrations in the microbial world.

NaCl-saturated brines such as saltern crystalliser ponds, inland salt lakes, deep-sea brines and liquids-of-deliquescence on halite are commonly regarded as a paradigm for the limit of life on Earth. There are, however, other habitats that are thermodynamically more extreme. Typically, NaCl-saturated environments contain all domains of life and perform complete biogeochemical cycling. Despite their reduced water activity, ∼0.755 at 5 M NaCl, some halophiles belonging to the Archaea and Bacteria exhibit optimum growth/metabolism in these brines. Furthermore, the recognised water-activity limit for microbial function, ∼0.585 for some strains of fungi, lies far below 0.755. Other biophysical constraints on the microbial biosphere (temperatures of >121°C; pH > 12; and high chaotropicity; e.g. ethanol at >18.9% w/v (24% v/v) and MgCl₂ at >3.03 M) can prevent any cellular metabolism or ecosystem function. By contrast, NaCl-saturated environments contain biomass-dense, metabolically diverse, highly active and complex microbial ecosystems; and this underscores their moderate character. Here, we survey the evidence that NaCl-saturated brines are biologically permissive, fertile habitats that are thermodynamically mid-range rather than extreme. Indeed, were NaCl sufficiently soluble, some halophiles might grow at concentrations of up to 8 M. It may be that the finite solubility of NaCl has stabilised the genetic composition of halophile populations and limited the action of natural selection in driving halophile evolution towards greater xerophilicity. Further implications are considered for the origin(s) of life and other aspects of astrobiology. This research is highlighted in Gunde-Cimerman et al. (2018) and Lee et al. (2018).