the environment and thus became more “complex”.
The invention of the microscope in the 21st Century revealed that all living organisms are made up of cells of different shapes. Since then, the cell has been regarded as the fundamental structural and functional biological unit of all living beings.
A student of Justus von Liebig, Moritz Traube, developed an “artificial mineral cell” from copper and potassium ferrocyanide in 1867. He observed the growth and budding of structures that resembled cell-like forms like those observed by Robert Hooke in 1665.
Then, Stéphane Leduc, inventor of the term “synthetic biology” (1912), declared at the beginning of the 20th Century, despite the craze for chemistry at the time: “Why is it less acceptable to try to find out how to make a cell than to make a molecule?”
Later, in the 1920s, the Soviet biochemist Alexander Oparin and the English geneticist John Burdon Sanderson Haldane proposed that elementary bricks of life, formed from gaseous elements in the atmosphere, were deposited in the primitive ocean, creating a “prebiotic soup” rich in assorted molecules that, when assembled, formed protocells or coacervates. From then on, all sorts of microspheres, micelles, protobionts and other models of single cells were imagined to represent simple compartments.
In order to “come alive”, the first processes were therefore able to take place in micro-environments that were capable of keeping the different components close to each other, thus promoting their interactions. Initially, this could be in the hollow of a rock or on clay dust, then in tiny organic vesicles, a kind of small bag that fills with molecules until it splits in two.
Coacervates were synthesized in a laboratory in the 1930s by Bungenberg de Jong. Proteinoids (Fox 1988), microspheres, marigranules and other compartmentalizing structures were obtained in order to mimic early cell forms.
In 1951, the young biochemist Boris Pavlovitch Belooussov, who worked in the Biophysics Laboratory of the Ministry of Health of the USSR, wanted to create an inorganic reaction that was similar to the energy-producing reaction in all aerobic organisms. Such a pathway, called the “Krebs cycle” (or “citric acid cycle”, abundant in lemons), works in living cells to break down sugars and produce energy. Belooussov mixed bromate ions BrO3- with citric acid C6H8O7 in the presence of ceric ions Ce4+ in an acidic medium. He hoped to reduce cerium (4+) to cerium (3+), which would have caused a discoloration in the solution. However, his observations were quite different, since he noticed a periodic succession of colors and discolorations of the reaction medium: Belooussov had just discovered the first oscillating reaction by chance. Ten years later, Anatol Zhabotinsky confirmed these observations, which had previously received little credit, and in turn described these oscillating, colored and “budding” waves, which earned the two authors the Lenin Prize for the now famous Beloousov-Zhabotinsky reaction. These observations inspired Heinz von Foerster’s (1961) and Henri Atlan’s (1972) theories on selforganization, Francisco Varela’s autopoiesis (1974) and Ilya Prigogine’s (1947) “thermodynamics far from equilibrium”, with related speculations on the origins of life.
1.3. Fossil traces?
Despite laboratory experiments and increasingly sophisticated techniques, we are faced with the absence of traces of the past, irrefutable “evidence” of the first moments. Indeed, down-to-earth, strictly geological considerations make it difficult to explore morphological evidence of the past. Volcanoes, tectonic plates, metamorphism and massive meteorite bombardments occurred during the Hadean period1 (4.5 to 4 billion years ago), during which warm, iron-laden oceans were formed, the Archean period2 (4 to 2.5 billion years ago), and the billions of years that preceded us.
Geological records provide direct evidence of the presence of primitive life on Earth in four main ways: through microfossils, stromatolites (literally “layers of stone”, from the Greek: stroma, “carpet”, and lithos, “stone”), molecular biomarkers, and stable isotope ratios. However, the interpretation of the samples and in situ analyses is still under discussion, as Archean rocks are scarce and poorly preserved.
Traces of ancient life may be hidden in fossil remains, which careful excavations are trying to discover. Fossils are rare because the fossilization process takes a long time, and when traces remain, they must escape decomposition and destruction, only to reappear later through soil erosion. Of the evidence left by ancient organisms, 99% is recent, dating back 545 million years. They include leaves, footprints, shells, bones, teeth, and spores or skeletons of fish or dinosaurs, most often preserved by sedimentation.
However, micropaleontologists refer to persistent traces of microorganisms in the form of stromatolites that existed almost 4 billion years ago (Schopf 1993; Allwood et al. 2006).
So, what happened in the first billion years of Earth’s history that led to the appearance of organisms that are similar to today’s bacteria?
Today, microbial communities build laminated “stone mats” in two ways. The cyanobacteria’s method is to trap fine sediments with a sticky film of mucus that each cell secretes, then cement the sediment grains with calcium carbonate precipitated in water. Because living cyanobacteria are photosynthetic, they move towards the light, so the bacterial mat always remains on the outside of the stromatolite. The cyanobacteria’s second method of constructing stromatolites is the precipitation of their own carbonate structure in water, with the incorporation of sediments (Awramik 1994).
Corrugated forms, resulting from probable laminations, have been observed in the south-west of Greenland at sites dating back 3.8 billion years. In the Isua region, the outcrops of ancient sedimentary rocks show forms in the metamorphosed minerals that resemble layers of stromatolites 1 to 4 cm high, produced by microorganisms that would have developed at that time, as suggested by the presence of yttrium (Y), a rare earth typical of sediments deposited in a shallow marine environment. However, these results have been contested by some, who instead point to formations of tectonic origin (Nutman 2016).
Elsewhere, in the Pilbara region (Warrawoona rock formation) in Western Australia, small sedimentary cushions, or domes, aged at 3.5 billion years old can be found. Early life environments in the Pilbara Craton also included shallow marine sedimentary environments and hydrothermal regions. Other such formations, dating back 2.5 billion years, can be found in the Transvaal in South Africa.
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,
