Living matter has always appeared highly singular against the background of “inert” matter so as (i) to interrogate its emergence and (ii) to attempt to convey its original features to inanimate objects. In the course of the 20th century, both latter perspectives have started to be interrogated at the cellular level with a continuously increasing content of information about the molecular components of living cells, their interactions and reactivity.
Most attempts have considered that addressing the issue of the emergence of life could reduce to reproducing the composition and organization of living cells as we currently know them. In the corresponding picture, a living cell is mostly the assembly of its components. This perspective has generated much experimental work in the field of prebiotic chemistry, which has attempted the synthesis of (possibly homochiral) molecular modules (amino-acids, nucleotides, sugars, lipids….) integrated in the present biomolecules (proteins, nucleic acids…) within the postulated astrophysical and planetary context of the emergence of life. In particular, these works have demonstrated that such molecular modules could be obtained and could react after appropriate activation to produce macromolecules and supramolecular assemblies exhibiting similarities with the ones presently encountered in living cells.
Another trend has considered life as a historical process, which has acted by dissipating available energy. In the corresponding picture, a living cell is an evolving network of interactions and chemical reactions. In this alternative perspective, the final goal is not anymore the present structure and composition of a living cell but the mechanism, leading from the initial state of non-living matter to the present level of biological organization. Up to the present time, most of the work performed along these lines has been theoretical. In particular, it has emphasized the significance of thermodynamic and kinetic considerations, bringing forward the concepts of energy dissipation, autocatalysis, replication, symbiosis, fitness, or Darwinian molecular evolution. Despite those theoretical developments we still currently lack a principled, quantitative, chemically explicit theory of the requirements needed to stabilize a metabolic network and a self-generated control system far from thermodynamic equilibrium. However, emerging experimental work has benefited from the developments of analysis, including imaging, high-throughput screening, and microfluidics, to bring promising results. In this project, we will challenge the relevance of the theoretical models and opening the possibility to develop experimental chemical systems that exhibit features of living systems, and might ultimately have the potential to evolve.
Beyond the preceding considerations, unravelling the transition from prebiotic to biological stages will forever remain a speculative task, except that the emergence of life on Earth has been a likely unique and successful experiment, highlighting the extraordinary potentialities of the chemical world. Since the appearance of the first living organisms (from a biological perspective) around 3.5 billion years ago, life has been constantly remodelled throughout evolution together with an extreme conservation of the basic features shared by virtually all cells. These two aspects will be considered in our project. The first aspect will encompass major evolution events, from the transition from prokaryote to eukaryote and the emergence of sub-cellular compartmentalization to the building of multi-cellular organisms. The second aspect will focus on the minimal components (at the molecular and structural levels) and their interactions mandatory to build a living organism, and how they have been co-opted to create new functions. The ultimate goal that would consist in building an artificial “living” organism should certainly help us understand how life can start.
What is clear is that the driving process behind the development of complex and sophisticated living systems on Earth is evolution by natural selection. A living system can be thought of in Darwinian terms as one that comprises entities capable of reproduction (one entity gives rise to many), heredity (like begets like), and variation (entities are not all alike). Any population of entities possessing these Darwinian properties, with at least a component of variation affecting reproductive success, will evolve by natural selection.
On Earth, the emergence of life and the evolution of complex (even intelligent) organisms, required a series of major evolutionary transitions, in which lower level self-replicating entities experience transition from autonomous replication to replicate as part of a (higher level) corporate body (a collective). During each transition, the focus of natural selection shifts from individual entities to collectives, but selection cannot simply choose to shift levels. Selection shifts only when collectives acquire Darwinian properties. Thus, understanding major evolutionary transitions requires understanding of how Darwinian properties (reproduction, heredity and variation) evolve in collectives that on first emergence likely lack these properties.
While major evolutionary transitions are a feature of life on Earth, there is no reason to think that similar transitions will not be required for the emergence of life on other planets. A central issue is evolution of the “Darwinian machine”, that is, the emergence of entities with Darwinian properties sufficient to ensure that entities participate – blindly – in the process of evolution by natural selection. Without such Darwinian properties evolution can take place, but evolution in the absence of natural selection is an impotent process.
The transitions are likely to be characterized by the emergence of the following:
1. Chemical systems showing pre-evolutionary dynamics (possibly).
2. Self-replicating molecular systems.
3. Evolving (living) systems (the origin of life).
4. Replicating protocells.
5. Cooperation between cells (including symbiosis).
6. Multicellular organisms.
We aim to explore these major transitions, the conditions necessary for them to occur at different levels of organisation (atoms, molecules, organelles, cells, cellular assemblies); their ecological consequences (i.e. how higher-level units interact among themselves and with their environment, and how as a consequence communities of these units flux material and energy); and the potential signatures that the emerging and evolving ecosystems may leave on the planetary environment. These major transitions, their environmental drivers, and their ecological consequences correspond, without exception, to highly open conceptual challenges which are timely to address, given the development of experimental methods either to create artificial models of such transitions in the laboratory, or to characterize existing systems.
With respect to all the preceding criteria, the PSL consortium is definitively relevant with already engaged individuals, a long tradition of interactions/collaborations at the triple Biology-Chemistry-Physics interface (e.g. as evidenced by the success of the Pierre-Gilles de Gennes Foundation), the balanced presence of theoreticians and experimentalists, the implementation of facilities (e.g. Institut Pierre-Gilles de Gennes dedicated to microfluidics, which should in particular provides powerful approaches and tools for screening and directed evolution; and the ENS-CNRS Ecotron, a unique infrastructure to investigate the environmental factors and consequences of evolution in microbial communities), and an evident interest for innovation. Beyond providing additional financial means, this PSL action will capitalize on the latter favourable features to considerably enrich the perspectives on questioning the emergence of life. In particular, we anticipate that our multidisciplinary blend of open-minded and motivated researchers will (i) bring original views to successfully identify the key technologies which have governed the evolution of living matter and (ii) draw potential applications associated to designing and constructing artificial “living” organisms that could reproduce and evolve under safety conditions, which will be thoroughly defined and implemented.