False Biosignatures on Mars: Anticipating Ambiguity

It is often acknowledged that the search for life on Mars might produce false positive results, particularly via the detection of objects, patterns or substances that resemble the products of life in some way but are not biogenic. The success of major current and forthcoming rover missions now calls for significant efforts to mitigate this risk. Here, we review known processes that could have generated false biosignatures on early Mars. These examples are known largely from serendipitous discoveries rather than systematic research and remain poorly understood; they probably represent only a small subset of relevant phenomena. These phenomena tend to be driven by kinetic processes far from thermodynamic equilibrium, often in the presence of liquid water and organic matter, conditions similar to those that can actually give rise to, and support, life. We propose that strategies for assessing candidate biosignatures on Mars could be improved by new knowledge on the physics and chemistry of abiotic self-organization in geological systems. We conclude by calling for new interdisciplinary research to determine how false biosignatures may arise, focusing on geological materials, conditions and spatiotemporal scales relevant to the detection of life on Mars, as well as the early Earth and other planetary bodies

Why do microbes make minerals?

Prokaryotes have been shaping the surface of the Earth and impacting geochemical cycles for the past four billion years. Biomineralization, the capacity to form minerals, is a key process by which microbes interact with their environment. While we keep improving our understanding of the mechanisms of this process (“how?”), questions around its functions and adaptive roles (“why?”) have been less intensively investigated. Here, we discuss biomineral functions for several examples of prokaryotic biomineralization systems, and propose a roadmap for the study of microbial biomineralization through the lens of adaptation. We also discuss emerging questions around the potential roles of biomineralization in microbial cooperation and as important components of biofilm architectures. We call for a shift of focus from mechanistic to adaptive aspects of biomineralization, in order to gain a deeper comprehension of how microbial communities function in nature, and improve our understanding of life co-evolution with its mineral environment

False biosignatures on Mars: anticipating ambiguity

It is often acknowledged that the search for life on Mars might produce false positive results, particularly via the detection of objects, patterns or substances that resemble the products of life in some way but are not biogenic. The success of major current and forthcoming rover missions now calls for significant efforts to mitigate this risk. Here, we review known processes that could have generated false biosignatures on early Mars. These examples are known largely from serendipitous discoveries rather than systematic research and remain poorly understood; they probably represent only a small subset of relevant phenomena. These phenomena tend to be driven by kinetic processes far from thermodynamic equilibrium, often in the presence of liquid water and organic matter, conditions similar to those that can actually give rise to, and support, life. We propose that strategies for assessing candidate biosignatures on Mars could be improved by new knowledge on the physics and chemistry of abiotic self-organization in geological systems. We conclude by calling for new interdisciplinary research to determine how false biosignatures may arise, focusing on geological materials, conditions and spatiotemporal scales relevant to the detection of life on Mars, as well as the early Earth and other planetary bodies

Organic stabilization of extracellular elemental sulfur in a Sulfurovum-rich biofilm: a new role for extracellular polymeric substances?

This work shines light on the role of extracellular polymeric substance (EPS) in the formation and preservation of elemental sulfur biominerals produced by sulfur-oxidizing bacteria. We characterized elemental sulfur particles produced within a Sulfurovum-rich biofilm in the Frasassi Cave System (Italy). The particles adopt spherical and bipyramidal morphologies, and display both stable (α-S8) and metastable (β-S8) crystal structures. Elemental sulfur is embedded within a dense matrix of EPS, and the particles are surrounded by organic envelopes rich in amide and carboxylic groups. Organic encapsulation and the presence of metastable crystal structures are consistent with elemental sulfur organomineralization, i.e., the formation and stabilization of elemental sulfur in the presence of organics, a mechanism that has previously been observed in laboratory studies. This research provides new evidence for the important role of microbial EPS in mineral formation in the environment. We hypothesize that the extracellular organics are used by sulfur-oxidizing bacteria for the stabilization of elemental sulfur minerals outside of the cell wall as a store of chemical energy. The stabilization of energy sources (in the form of a solid electron acceptor) in biofilms is a potential new role for microbial EPS that requires further investigation

A re-examination of the mechanism of whiting events: a new role for diatoms in Fayetteville Green Lake (New York, USA)

Whiting events—the episodic precipitation of fine-grained suspended calcium carbonates in the water column—have been documented across a variety of marine and lacustrine environments. Whitings likely are a major source of carbonate muds, a constituent of limestones, and important archives for geochemical proxies of Earth history. While several biological and physical mechanisms have been proposed to explain the onset of these precipitation events, no consensus has been reached thus far. Fayetteville Green Lake (New York, USA) is a meromictic lake that experiences annual whitings. Materials suspended in the water column collected through the whiting season were characterized using scanning electron microscopy and scanning transmission X-ray microscopy. Whitings in Fayetteville Green Lake are initiated in the spring within the top few meters of the water column, by precipitation of fine amorphous calcium carbonate (ACC) phases nucleating on microbial cells, as well as on abundant extracellular polymeric substances (EPS) frequently associated with centric diatoms. Whiting particles found in the summer consist of 5–7 μm calcite grains forming aggregates with diatoms and EPS. Simple calculations demonstrate that calcite particles continuously grow over several days, then sink quickly through the water column. In the late summer, partial calcium carbonate dissolution is observed deeper in the water column. Settling whiting particles, however, reach the bottom of the lake, where they form a major constituent of the sediment, along with diatom frustules. The role of diatoms and associated EPS acting as nucleation surfaces for calcium carbonates is described for the first time here as a potential mechanism participating in whitings at Fayetteville Green Lake. This mechanism may have been largely overlooked in other whiting events in modern and ancient environments

Organic biomorphs may be better preserved than microorganisms in early Earth sediments

The Precambrian rock record contains numerous examples of microscopic organic filaments and spheres, commonly interpreted as fossil microorganisms. Microfossils are among the oldest traces of life on Earth, making their correct identification crucial to our understanding of early evolution. Yet, spherical and filamentous microscopic objects composed of organic carbon and sulfur can form in the abiogenic reaction of sulfide with organic compounds. Termed organic biomorphs, these objects form under geochemical conditions relevant to the sulfidic environments of early Earth. Furthermore, they adopt a diversity of morphologies that closely mimic a number of microfossil examples from the Precambrian record. Here, we tested the potential for organic biomorphs to be preserved in cherts; i.e., siliceous rocks hosting abundant microbial fossils. We performed experimental silicification of the biomorphs along with the sulfur bacterium Thiothrix. We show that the original morphologies of the biomorphs are well preserved through encrustation by nano-colloidal silica, while the shapes of Thiothrix cells degrade. Sulfur diffuses from the interior of both biomorphs and Thiothrix during silicification, leaving behind empty organic envelopes. Although the organic composition of the biomorphs differs from that of Thiothrix cells, both types of objects present similar nitrogen/carbon ratios after silicification. During silicification, sulfur accumulates along the organic envelopes of the biomorphs, which may promote sulfurization and preservation through diagenesis. Organic biomorphs possessing morphological and chemical characteristics of microfossils may thus be an important component in Precambrian cherts, challenging our understanding of the early life record

Resistance-associated point mutations of organophosphate insensitive acetylcholinesterase, in the olive fruit fly Bactrocera oleae

A 2.2-kb full length cDNA containing an ORF encoding a putative acetylcholinesterase (AChE) precursor of 673 amino acid residues was obtained by a combined degenerate PCR and RACE strategy from an organophosphate-susceptible Bactrocera oleae strain. A comparison of cDNA sequences of individual insects from susceptible and resistant strains, coupled with an enzyme inhibition assay with omethoate, indicated a novel glycine-serine substitution (G488S), at an amino acid residue which is highly conserved across species (13396 of Torpedo californica AChE), as a likely cause of AChE insensitivity. This mutation was also associated with a 35-40% reduction in AChE catalytic efficiency. The I199V substitution, which confers low levels of resistance in Drosophila, was also present in B. oleae (I214V) and in combination with G488S produced up to a 16-fold decrease in insecticide sensitivity. This is the first agricultural pest where resistance has been associated with an alteration in AChE, which arises from point mutations located within the active site gorge of the enzyme

Magnetotactic bacteria form magnetite from a phosphate-rich ferric hydroxide via nanometric ferric (oxyhydr)oxide intermediates

The iron oxide mineral magnetite (Fe(3)O(4)) is produced by various organisms to exploit magnetic and mechanical properties. Magnetotactic bacteria have become one of the best model organisms for studying magnetite biomineralization, as their genomes are sequenced and tools are available for their genetic manipulation. However, the chemical route by which magnetite is formed intracellularly within the so-called magnetosomes has remained a matter of debate. Here we used X-ray absorption spectroscopy at cryogenic temperatures and transmission electron microscopic imaging techniques to chemically characterize and spatially resolve the mechanism of biomineralization in those microorganisms. We show that magnetite forms through phase transformation from a highly disordered phosphate-rich ferric hydroxide phase, consistent with prokaryotic ferritins, via transient nanometric ferric (oxyhydr)oxide intermediates within the magnetosome organelle. This pathway remarkably resembles recent results on synthetic magnetite formation and bears a high similarity to suggested mineralization mechanisms in higher organisms

Nanometer-scale characterization of exceptionally preserved bacterial fossils in Paleocene phosphorites from Ouled Abdoun (Morocco)

International audienceMicrometer-sized spherical and rod-shaped forms have been reported in many phosphorites and often interpreted as microbes fossilized by apatite, based on their morphologic resemblance with modern bacteria inferred by scanning electron microscopy (SEM) observations. This interpretation supports models involving bacteria in the formation of phosphorites. Here, we studied a phosphatic coprolite of Paleocene age originating from the Ouled Abdoun phosphate basin (Morocco) down to the nanometer-scale using focused ion beam milling, transmission electron microscopy (TEM), and scanning transmission x-ray microscopy (STXM) coupled with x-ray absorption near-edge structure spectroscopy (XANES). The coprolite, exclusively composed of francolite (a carbonate-fluroapatite), is formed by the accumulation of spherical objects, delimited by a thin envelope, and whose apparent diameters are between 0.5 and 3 lm. The envelope of the spheres is composed of a continuous crown dense to electrons, which measures 20-40 nm in thickness. It is surrounded by two thinner layers that are more porous and transparent to electrons and enriched in organic carbon. The observed spherical objects are very similar with bacteria encrusting in hydroxyapatite as observed in laboratory experiments. We suggest that they are Gram-negative bacteria fossilized by francolite, the precipitation of which started within the periplasm of the cells. We discuss the role of bacteria in the fossilization mechanism and propose that they could have played an active role in the formation of francolite. This study shows that ancient phosphorites can contain fossil biological subcellular structures as fine as a bacterial periplasm. Moreover, we demonstrate that while morphological information provided by SEM analyses is valuable, the use of additional nanoscale analyses is a powerful approach to help inferring the biogenicity of biomorphs found in phosphorites. A more systematic use of this approach could considerably improve our knowledge and understanding of the microfossils present in the geological record