During its early youth, the Earth was the site of extremely violent processes. In particular, the energy of the impact of the planet Theia with the young Earth was such that the latter became entirely covered with a thick layer of molten magma, called the "magma ocean". On the now calmed Earth that we currently know, the objects classified as "living" by our sense organs are distinguished from those classified as "non-living" by two main characteristics: i) living objects have a completely original organic molecular constitution and ii) in contrast to non-living objects, which tend to equilibrate with the outside, living objects never reach equilibrium and are therefore "obligatory dynamical systems" out of equilibrium. It seems that the dynamic characteristic was acquired before the molecular characteristic for the genesis on Earth of the first living object(s). We propose that hypothetical "ante-cells" reached a "dynamic although inorganic" state on the nascent Earth, and then, that these ante-cells gradually transformed into real cells once the Earth had cooled sufficiently for organic molecules to appear there. The vestigial pentameric RNAs would mark this key moment when the ante-cells have begun to join the organic world.
The oldest geological samples containing indisputable traces of life date back approximately 3.7 billion years [1]. It was already bacteria. There are no fossils of previous life forms. Trying to understand what such previous life forms might have been is therefore a matter of speculation.
After a few reminders concerning the history of the Earth, we shall revisit the acquisition of the characteristics of current living cells from both points of view of their molecular constitution and their dynamic behavior. We shall propose a scenario alternative of the classical approach for the appearance on Earth of the first living system(s). It is based on what our sense organs can and cannot do and on the likely role of vestigial pentameric RNAs.
The solar system, including our Earth, arose from the gravitational collapse of a gigantic cosmic cloud of gas and dust approximately 4.568 billion years ago. This was taken as instant zero of the age of the solar system. What followed was a complicated series of violent events [2-4].
Briefly, the sun formed by the progressive accretion of most of the cloud material, while the part not yet accreted organized itself into a disk rotating around it. Within the disk, dust agglomerated and formed bodies of extremely variable size (up to a few km in diameter). The largest bodies, most effectively attracting material from the disk, grew exponentially until they formed bodies of several hundred km in diameter, which were continuously impacted by the smaller bodies that they captured. Giant impacts occurred between the bodies the most massive. Due to the considerable energies involved in these processes, all these colliding bodies are assumed to have been in the molten state and to have differentiated into an inner metallic core and a silicate mantle at the periphery.
After a few tens of millions of years, most of the disk had accreted into planets, including Earth. One of the planets, Theia, would have collided with the Earth, thus fusing most of its core to that of the Earth. The debris resulting from the collision eventually formed the moon. The colossal energy released by the shock caused the fusion of what had begun to crystallize on Earth; the Earth’s surface thus became entirely covered with a deep “magma ocean” stirred by giant waves of molten rock. After about 160 millions of years, the Earth gradually differentiated with a proto-core where iron accumulated, a lower mantle which solidified and an upper mantle of molten magma on the surface of which solidified islands appeared.
Continuing its slow cooling the Earth acquired a solid crust by the progressive crystallization of its magma ocean; there was an atmosphere; water vapor condensed and the liquid water was collected in the coldest areas: the Earth began to look like it does now.
Following the discovery by Miller that small organic molecules (in particular nucleotides and amino-acids) could appear spontaneously in the Earth's atmosphere assumed to have existed some 4 billion years ago [5], a great deal of skill has gone into clarifying how the macromolecules and the cell structure typical of now-a-day living beings were acquired, as well as determining the origin of life.
Following Erwin Schrödinger [6,7] whose little book "What is life? The physical aspect of the living cell" introduced the concept of coded macromolecules; a huge literature has accumulated, with contributions ranging from biology to astrophysics (see for instance [8-27]). A large number of events possibly involved in the progressive complexification of cellular constituents have been explored. Two main stream of interpretative theories have been followed, which are usually referred to as "DNA first" and "RNA first", which was the subject of much debate during the Cold Spring Harbor Laboratory’s 74th Symposium focuses on evolution in a molecular age in 2009 [11-13].
However, although almost a century has elapsed since the pioneering work of Aleksandr Oparine [9], all the steps have still not been completely arranged into a logical continuum from small organic molecules up to living cells. Besides, the ambitious project to develop a mixture of reagents capable of changing into a living system [14,15] has still not been achieved.
In 1999, Freeman Dyson [10] stated that living organisms can be distinguished from inanimate matter by the existence of two dynamic processes, metabolism and replication. Recently, one of us (M.T.) [28] has suggested revisiting the question, starting from what our sense organs (our only source of information about our environment) can or cannot do.
Let us call "an object" anything the presence of which is detected by at least one of our sense organs, e.g. grain of sand, pebble, butterfly, solution of various substances, rat, human being, car, oak, whale, comet, etc. None of our five sense organs (hearing, sight, smell, taste and touch) can detect life, which is therefore unknowable to us. What our sense organs can do is classify the objects they detect into two, and only two, categories: non-living and living. It is possible to give life an operational definition such as "Life exists wherever our sense organs detect at least one living object" or "Life is the set of properties possessed by all objects classified as living by our sense organs, and that those classified as non-living do not possess". That said, it is indeed on the objects, recognized as non-living or living, rather than on life per se, that reasoning or experimentation is carried out.
When objects (living or not) evolve, they are said to be “dynamic”. In free contact with the outside, the objects recognized as non-living spontaneously evolve towards equilibrium with the outside (all evolution ceasing when they have reached it), while those recognized as living will never reach equilibrium. For example, a human, as long as he is alive, maintains his temperature constant and continues incoming and outgoing transport with the outside. Thus, objects recognized as living are not conceivable in equilibrium; they can exist only in a dynamic state; they are said to be "obligatory dynamic systems". It cannot be excluded that forms of resistance exist that can remain in truly suspended life for more or less long periods of time; but we do not know of any object recognized as living by our sense organs which is not an obligatory dynamic system nor of any obligatory dynamic system which is not an object recognized as living.
That one day a living object appeared for the first time on Earth implies that, in one way or another, the property of being in an obligatory dynamic state has been conferred on it.
In a series of ingenious experiments by various authors discussed in [28] a straightforward transition from non-living to living objects was never observed. The probability that the two characteristics of currently living cells, organic molecular constitution and necessarily dynamic behavior, were acquired at the same time on the Earth as it is at present is therefore extremely low if not nil. The probability of the simultaneous acquisition of both characteristics on the nascent Earth (the moment when it was most different from what it is now) is also zero because it was then much too hot for organic molecules to have existed there. The two characteristics were therefore acquired independently of each other. Moreover the molecular characteristic was probably acquired after the dynamic one, since it could be acquired only on the Earth as it is now but without this apparently being enough to allow life to arise.
We propose that the following scenario was carried out in two successive stages. In the first stage, hypothetical entities would have acquired an obligatory dynamic behavior on the nascent Earth. We shall call them “ante-cells” to mean that they were on the path leading to the first living cells without this being yet obvious. The ante-cells would have remained unchanged, dynamic although inorganic (i.e. involving only mineral substances in their functioning) for millions of years, and still in no way resembling living objects. The progressive crystallization of the magma ocean caused the appearance of colder areas where more and more numerous and diversified organic molecules could be formed and maintained. In the second stage of the scenario, the ante-cells would have involved these molecules in their functioning, thus progressively transforming themselves into real cells along with the slow cooling of the Earth. The events described in the classic "DNA first" or "RNA first" theories are suitable for describing the history of life from the moment it joined the organic domain, but these events would have occurred within the ante-cells.
It may seem unreasonable to assume that the obligatory dynamic behavior was triggered in the ante-cells on the nascent Earth. However, human kind has never witnessed dynamic processes as violent as those that occurred on Earth at the beginning of its existence; so it would not be surprising if events could have happened there that seem incomprehensible to us today. Furthermore, for the sake of simplicity, as there must have been a time when life acquired its dynamic characteristics, isn't the most logical one when the Earth itself was in the most dynamic state it has ever met?
There is no record to support that ante-cells have really existed or to reveal what they looked like. Is it by transport between compartments that one of the violent events occurring on the nascent Earth would have conferred on the ante-cells their dynamic characteristics? Did the ante-cells already have the structure of a closed bag? If so, was the formation of their envelope somehow related to the occurrence of micro-drops or micro-vortices in the molten magma? These may forever remain unanswered questions, unless further studies of the oldest known geological samples can shed some light.
One of us (J.D.) discovered that same pentanucleotide sequences were found repeatedly in the tRNA loops of various archae as well as in Arabidopsis thaliana [29-31]. In our scenario, these pentanucleotide sequences arrive at the right time to mark the key event which was the moment when the ante-cells joined the organic world.
Interpreting these sequences as being the remains of archaic forms on the way to the elaboration of nucleic acids has begun to be used to reconstruct the pathway of ribosome formation [32-34].
Our sense organs do not tell us directly about “life”. Even when defining life by the properties of the objects that our sense organs classify as living, this is not an absolutely rigorous approach because the way in which they carry out their classification (most often at a single glance) is subject to hesitation or error. We have however to be content with this: there is nothing better to offer.
In our ante-cell scenario, the arising on Earth of the first living cell(s) is the culmination of a long genesis devoted to the acquisition of the molecular and dynamic characteristics of objects currently recognized as alive by our sense organs. Since the acquisition of the obligatory dynamic character seems to have taken place before that of the molecular characteristics, the hypothesis which seemed to us the simplest is that it would have occurred on the nascent Earth. On the one hand it is a period when the Earth itself was in an extremely dynamic state, where it is least surprising that an obligatory dynamic state was created. On the other hand, once this dynamic characteristic was acquired, the acquisition of the molecular characteristics could be done without any further difficulty. The reason why it was never observed that a living object arose from the non-living on the Earth as it is now would then be simply that there no longer occurs a process violent enough to allow the acquisition of the necessarily dynamic character.
In our scenario, the probability of appearance on Earth of a first living object depends directly on the probability of appearance of dynamic although inorganic ante-cells. If the latter is weak, our planet could be one of the few (perhaps the only one) to host life in the universe. Will new data one day make it possible to evaluate these probabilities? In the absence of fossil remains, the continuation of the study of the vestigial nucleotide pentamers and the generalization of the method to other living species and other nucleotides will perhaps help to achieve this.
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