Figure 1.1. Stromatolites dating back 2.5 billion years, observed in the Transvaal in South Africa. Courtesy of Pierre Thomas (2016). For a color version of this figure, see www.iste.co.uk/chapouthier/life.zip
This variety of environments, combined with the variety of stromatolite forms found, would indicate a biosphere that was already diverse 3 to 4 billion years ago.
Biodiversity originates from the origins of life itself.
A major contribution highlights a point that is rarely addressed in the study of the metabolism of early stromatolites. Indeed, the hypothesis that cyanobacteria formed fossil stromatolites by mineralization and lithification of microbial mats assumes that oxygenic photosynthesis is a very old process, one that was active more than 3 billion years ago. However, the surface of the Earth was predominantly anoxic in the Archean period, containing less than 1% of today’s oxygen concentration. The increase in oxygen in the ocean, as a result of cyanobacterial photosynthesis, gradually turned it into an oxidizing environment, whereas it was initially reductive. This means that the oldest stromatolites are the product of phototrophic anoxygenic microorganisms, which do not produce oxygen. Supporting this hypothesis, researchers have recently observed that phototrophic sulpho- oxidizing alpha-proteobacteria are responsible for the precipitation of aragonite, the main calcium carbonate constituting the stromatolites of Lake Dziani Dzaha in Mayotte (Gérard et al. 2018).
In addition, other anaerobic methanotrophic microbial communities were present prior to the oxygenation of the Earth’s atmosphere. Using sulfate ions or organic sulfur to oxidize methane, these microorganisms that lived in sedimentary lake environments left traces in the Tumbiana formation, aged at 2.7 billion years old (Lepot et al. 2019).
The anoxygenic photosynthesis forming the first stromatolites was carried out by phototrophic anoxygenic microorganisms and would therefore have occurred before oxygen photosynthesis.
1.4. Geochemical elements confirming these recent results
The vast majority of the world’s iron is known as Banded Iron Formation (BIF). Archean banded-iron deposits are marine sedimentary rocks that are very rich in iron and today account for 90% of the iron mined in the world.
Figure 1.2. The figure shows changes in the abundance of elements over time, mainly sulfur (S) and iron (Fe). The color gradations indicate a transition from anoxic oceans, e.g. low in sulfur, before 2.4 billion years (light blue) to oceans rich in H2S between 1.8 billion and 800 million years (dark blue), and then to complete oxygenation of the oceans (green). Courtesy of Ariel Anbar (2008). For a color version of this figure, see www.iste.co.uk/chapouthier/life.zip
Figure 1.3. Banded Iron Formation (BIF). Courtesy of Pierre Thomas (2011). For a color version of this figure, see www.iste.co.uk/chapouthier/life.zip
The ocean and the Earth’s surface were without oxygen 4 to 2.5 billion years ago.
The weathering of minerals from iron-rich continents produced ferrous ions (Fe2+) that were soluble in water, and therefore particularly mobile, and which were able to spread into the oceans. Volcanic activity at hydrothermal springs may also have contributed to the presence of ferrous ions in solution.
Oxygenation of the oceans by the oxygenic photosynthesis of cyanobacteria, up to about 2.4 billion years ago, caused soluble ferrous iron (Fe2+) to disappear by oxidation into insoluble ferric iron (Fe3+), which precipitated as magnetite and hematite.
When most of the reduced forms of iron were oxidized in the Paleoproterozoic era, sedimentation of banded iron deposits became rare. As a result, the O2 content first increased in the oceans, then in the atmosphere, becoming toxic to anaerobic organisms. This was the Great Oxidation or “Oxygen Catastrophe”.
Given that sea iron precipitated in an insoluble form (Fe3+) in the Archean era, the sea water of that time contained iron in solution, in a soluble form (Fe2+). This proves that the sea of that time was reduced, as was the overlying atmosphere.
Another type of photosynthesis, which is rare and little known, could explain an abundant precipitation of iron oxide: photoferrotrophy, a process where iron provides electrons.
Photoferrotrophy is a photosynthesis (less energy efficient than conventional photosynthesis) that oxidizes the iron (Fe2+) of FeO into iron (Fe3+) of Fe2O3; it can be written in a very simplified way: 2 FeO + H2O + photons → Fe2O3 + 2 H+ + 2 e-.
The H+ ions and e- electrons are then used by mechanisms, similar to those of classical photosynthesis, to synthesize carbohydrates from CO2; this metabolism requires the presence of iron (Fe2+) in the environment and leads to the massive precipitation of hematite Fe2O3.
Life is determined by the environment and, as multiple environments coexist, the origins of life and biodiversity coincide and evolve together.
1.5. Compartmentalization of resources and primary biomass
In September 1969, a fireball exploded in the sky over Murchison, Australia, followed by a shower of meteorite fragments gathered in a few days. Extraterrestrial amino acids and hydrocarbons in the Murchison meteorite were quickly identified by David Deamer (1985), who showed that organic compounds in the meteorite could also assemble into membranes. Since then, many molecules of biological interest have been identified in other meteorites (Callahan et al. 2011).
Figure 1.4. Carbonaceous chondrite. Courtesy of Pierre Thomas (2016). For a color version of this figure, see www.iste.co.uk/chapouthier/life.zip
Deamer and Barchfeld (1982), Deamer and Pashley (1989), Deamer (1997), Dworkin et al. (2001), will be pioneers in the experimental study of organic compounds synthesized in space. Entering into the planetary atmosphere of the primitive Earth, they mixed with endogenous species, some of them amphiphilic, with polar and non-polar groups on the same molecule. They spontaneously self-assemble to form more complex bimolecular structures which, in turn, form membrane vesicles.
The self-assembly of amphiphilic compounds, lipids forming spherical vesicles, called “liposomes”, are capable of capturing macromolecules. The lipid bilayer is sufficiently permeable to allow exchanges with ionic and polar compounds from outside the compartment, allowing polymerization reactions, a kind of protometabolism, within these vesicles (Zepik et al. 2007). Hydrothermal sites are good candidates for the realization of such prebiotic evolution on the primitive Earth. Vesicles formed on mineral surfaces capture and produce diverse molecular systems. Each vesicle represents a protocell, a kind of chemical microreactor (Damer and Deamer 2015).
Laboratory simulations show that such vesicles easily encapsulate functional macromolecules, including nucleic acids and enzymes. RNA-type polymers are synthesized non-enzymatically in the laboratory from mononucleotides in lipid environments. RNA-type polymers identified by nanopore were analyzed by standard enzyme labeling methods, followed by gel electrophoresis. Chemical activation of the mononucleotides is not required. Instead, the synthesis of phosphodiester bonds is stimulated by the chemical potential of fluctuating anhydrous and hydrated conditions, with heat providing activation energy during the dehydration. In the final hydration step, the RNA-type polymer is encapsulated in lipid vesicles. This process provides the model for a possible first step in the evolution towards an RNA world (Rajamani