Is There Such a Thing as a Biosignature?

The concept of a biosignature is widely used in astrobiology to suggest a link between some observation and a biological cause, given some context. The term itself has been defined and used in several ways in different parts of the scientific community involved in the search for past or present life on Earth and beyond. With the ongoing acceleration in the search for life in distant time and/or deep space, there is a need for clarity and accuracy in the formulation and reporting of claims. Here, we critically review the biosignature concept(s) and the associated nomenclature in light of several problems and ambiguities emphasized by recent works. One worry is that these terms and concepts may imply greater certainty than is usually justified by a rational interpretation of the data. A related worry is that terms such as "biosignature" may be inherently misleading, for example, because the divide between life and non-life-and their observable effects-is fuzzy. Another worry is that different parts of the multidisciplinary community may use non-equivalent or conflicting definitions and conceptions, leading to avoidable confusion. This review leads us to identify a number of pitfalls and to suggest how they can be circumvented. In general, we conclude that astrobiologists should exercise particular caution in deciding whether and how to use the concept of biosignature when thinking and communicating about habitability or life. Concepts and terms should be selected carefully and defined explicitly where appropriate. This would improve clarity and accuracy in the formulation of claims and subsequent technical and public communication about some of the most profound and important questions in science and society. With this objective in mind, we provide a checklist of questions that scientists and other interested parties should ask when assessing any reported detection of a "biosignature" to better understand exactly what is being claimed.

Adsorption of Polycyclic Aromatic Hydrocarbons and C60 onto Forsterite: C-H Bond Activation by the Schottky Vacancy.

Understanding how to catalytically break the C-H bond of aromatic molecules, such as polycyclic aromatic hydrocarbons (PAHs), is currently a big challenge and a subject of study in catalysis, astrochemistry, and planetary science. In the latter, the study of the breakdown reaction of PAHs on mineral surfaces is important to understand if PAHs are linked to prebiotic molecules in regions of star and planet formation. In this work, we employed a periodic density functional theory along with Grimme's D4 (DFT-D4) approach for studying the adsorption of a sample of PAHs (naphthalene, anthracene, fluoranthene, pyrene, coronene, and benzocoronene) and fullerene on the [010] forsterite surface and its defective surfaces (Fe-doped and Ni-doped surfaces and a MgO-Schottky vacancy) for their implications in catalysis and astrochemistry. On the basis of structural and binding energy analysis, large PAHs and fullerene present stronger adsorption on the pristine, Fe-doped, and Ni-doped forsterite surfaces than small PAHs. On a MgO-Schottky vacancy, parallel adsorption of the PAH leads to the chemisorption process (C-Si and/or C-O bonds), whereas perpendicular orientation of the PAH leads to the catalytic breaking of the aromatic C-H bond via a barrierless reaction. Spin density and charge analysis show that C-H dissociation is promoted by electron donation from the vacancy to the PAH. As a result of the undercoordinated Si and O atoms, the vacancy acts as a Frustrated Lewis Pair (FLP) catalyst. Therefore, a MgO-Schottky vacancy [010] forsterite surface proved to have potential catalytic activity for the activation of C-H bond in aromatic molecules.

Experimental and Theoretical Constraints on Amino Acid Formation from PAHs in Asteroidal Settings.

Amino acids and polycyclic aromatic hydrocarbons (PAHs) belong to the range of organic compounds detected in meteorites. In this study, we tested empirically and theoretically if PAHs are precursors for amino acids in carbonaceous chondrites, as previously suggested. We conducted experiments to synthesize amino acids from fluoranthene (PAH), with ammonium bicarbonate as a source for ammonia and carbon dioxide under mimicked asteroidal conditions. In our thermodynamic calculations, we extended our analysis to additional PAH-amino acid combinations. We explored 36 reactions involving the PAHs naphthalene, anthracene, fluoranthene, pyrene, triphenylene, and coronene and the amino acids glycine, alanine, valine, leucine, phenylalanine, and tyrosine. Our experiments do not show the formation of amino acids, whereas our theoretical results hint that PAHs could be precursors of amino acids in carbonaceous chondrites at low temperatures.

Interaction of Aromatic Molecules with Forsterite: Accuracy of the Periodic DFT-D4 Method.

Density functional theory (DFT) has provided deep atomic-level insights into the adsorption behavior of aromatic molecules on solid surfaces. However, modeling the surface phenomena of large molecules on mineral surfaces with accurate plane wave methods (PW) can be orders of magnitude more computationally expensive than localized atomic orbitals (LCAO) methods. In the present work, we propose a less costly approach based on the DFT-D4 method (PBE-D4), using LCAO, to study the interactions of aromatic molecules with the {010} forsterite (Mg2SiO4) surface for their relevance in astrochemistry. We studied the interaction of benzene with the pristine {010} forsterite surface and with transition-metal cations (Fe2+ and Ni2+) using PBE-D4 and a vdW-inclusive density functional (Dion, Rydberg, Schröder, Langreth, and Lundqvist (DRSLL)) with LCAO methods. PBE-D4 shows good agreement with coupled-cluster methods (CCSD(T)) for the binding energy trend of cation complexes and with PW methods for the binding energy of benzene on the forsterite surface with a difference of about 0.03 eV. The basis set superposition error (BSSE) correction is shown to be essential to ensure a correct estimation of the binding energies even when large basis sets are employed for single-point calculations of the optimized structures with smaller basis sets. We also studied the interaction of naphthalene and benzocoronene on pristine and transition-metal-doped {010} forsterite surfaces as a test case for PBE-D4. Yielding results that are in good agreement with the plane wave methods with a difference of about 0.02-0.17 eV, the PBE-D4 method is demonstrated to be effective in unraveling the binding structures and the energetic trends of aromatic molecules on pristine and transition-metal-doped forsterite mineral surfaces. Furthermore, PBE-D4 results are in good agreement with its predecessor PBE-D3(BJM) and with the vdW-inclusive density functionals, as long as transition metals are not involved. Hence, PBE-D4/CP-DZP has been proven to be a robust theory level to study the interaction of aromatic molecules on mineral surfaces.

Circular Spectropolarimetric Sensing of Vegetation in the Field: Possibilities for the Remote Detection of Extraterrestrial Life.

Homochirality is a generic and unique property of all biochemical life, and the fractional circular polarization of light it induces therefore constitutes a potentially unambiguous biosignature. However, while high-quality circular polarimetric spectra can be easily and quickly obtained in the laboratory, accurate measurements in the field are much more challenging due to large changes in illumination and target movement. In this study, we measured various targets in the field, up to distances of a few kilometers, using the dedicated circular spectropolarimeter TreePol. We show how photosynthetic life can readily be distinguished from abiotic matter. We underline the potential of circular polarization signals as a remotely accessible means to characterize and monitor terrestrial vegetation, for example, for agriculture and forestry. In addition, we discuss the potential of circular polarization for the remote detection of extraterrestrial life.

Circular spectropolarimetric sensing of higher plant and algal chloroplast structural variations.

Photosynthetic eukaryotes show a remarkable variability in photosynthesis, including large differences in light-harvesting proteins and pigment composition. In vivo circular spectropolarimetry enables us to probe the molecular architecture of photosynthesis in a non-invasive and non-destructive way and, as such, can offer a wealth of physiological and structural information. In the present study, we have measured the circular polarizance of several multicellular green, red, and brown algae and higher plants, which show large variations in circular spectropolarimetric signals with differences in both spectral shape and magnitude. Many of the algae display spectral characteristics not previously reported, indicating a larger variation in molecular organization than previously assumed. As the strengths of these signals vary by three orders of magnitude, these results also have important implications in terms of detectability for the use of circular polarization as a signature of life.

Imaging linear and circular polarization features in leaves with complete Mueller matrix polarimetry.

Spectropolarimetry of intact plant leaves allows to probe the molecular architecture of vegetation photosynthesis in a non-invasive and non-destructive way and, as such, can offer a wealth of physiological information. In addition to the molecular signals due to the photosynthetic machinery, the cell structure and its arrangement within a leaf can create and modify polarization signals. Using Mueller matrix polarimetry with rotating retarder modulation, we have visualized spatial variations in polarization in transmission around the chlorophyll a absorbance band from 650 nm to 710 nm. We show linear and circular polarization measurements of maple leaves and cultivated maize leaves and discuss the corresponding Mueller matrices and the Mueller matrix decompositions, which show distinct features in diattenuation, polarizance, retardance and depolarization. Importantly, while normal leaf tissue shows a typical split signal with both a negative and a positive peak in the induced fractional circular polarization and circular dichroism, the signals close to the veins only display a negative band. The results are similar to the negative band as reported earlier for single macrodomains. We discuss the possible role of the chloroplast orientation around the veins as a cause of this phenomenon. Systematic artefacts are ruled out as three independent measurements by different instruments gave similar results. These results provide better insight into circular polarization measurements on whole leaves and options for vegetation remote sensing using circular polarization.

In Situ Nanoscale Investigation of Step Retreat on Fluoranthene Crystal Surfaces.

Fluoranthene, a polycyclic aromatic hydrocarbon, has been detected on Earth as well as in asteroids and meteorites and may have played a role in the formation of life. Increasing the ionic strength of aqueous solutions has been observed to lower the fluoranthene solubility, but it is unclear how solution composition controls the release rate of fluoranthene to an aqueous solution. To elucidate this, we performed in situ atomic force microscopy experiments in which we characterized the sublimation and dissolution behavior of fluoranthene crystal surfaces. From this, we quantify the step retreat rate upon exposure to air, deionized water, and a 0.4 M NaCl or 0.1 M MgSO4 solution. Surface roughness is the main factor that determines the dissolution or sublimation rate. The results imply that during fluoranthene remediation or breakdown in meteorites and asteroids, ionic strength will be more important than chemical composition for controlling fluoranthene release into solution.

The Significance of Microbe-Mineral-Biomarker Interactions in the Detection of Life on Mars and Beyond.

The detection of biomarkers plays a central role in our effort to establish whether there is, or was, life beyond Earth. In this review, we address the importance of considering mineralogy in relation to the selection of locations and biomarker detection methodologies with characteristics most promising for exploration. We review relevant mineral-biomarker and mineral-microbe interactions. The local mineralogy on a particular planet reflects its past and current environmental conditions and allows a habitability assessment by comparison with life under extreme conditions on Earth. The type of mineral significantly influences the potential abundances and types of biomarkers and microorganisms containing these biomarkers. The strong adsorptive power of some minerals aids in the preservation of biomarkers and may have been important in the origin of life. On the other hand, this strong adsorption as well as oxidizing properties of minerals can interfere with efficient extraction and detection of biomarkers. Differences in mechanisms of adsorption and in properties of minerals and biomarkers suggest that it will be difficult to design a single extraction procedure for a wide range of biomarkers. While on Mars samples can be used for direct detection of biomarkers such as nucleic acids, amino acids, and lipids, on other planetary bodies remote spectrometric detection of biosignatures has to be relied upon. The interpretation of spectral signatures of photosynthesis can also be affected by local mineralogy. We identify current gaps in our knowledge and indicate how they may be filled to improve the chances of detecting biomarkers on Mars and beyond.