Research in Microbiology 160 (2009) 437e440 www.elsevier.com/locate/resmic From the primordial soup to the latest universal common ancestor Mario Vaneechoutte a,*, Renato Fani b a Laboratory Bacteriology Research, Faculty Medicine & Health Sciences, University of Ghent, 3 Blok A, De Pintelaan 185, 9000 Gent, Belgium b Dept. of Evolutionary Biology, Via Romana 17-19, University of Florence, I-50125 Florence, Italy Received 4 September 2009; accepted 7 September 2009 Available online 12 September 2009 Abstract This special issue of Research in Microbiology is dedicated to the origin of Life and of microbiology. One hundred and fifty years after Darwin’s ‘Origin of the Species’, which is basically about the principles of natural selection, the origin of Life, which largely coincides with the origin of natural selection, remains the most enigmatic and fascinating problem in biology. Ó 2009 Elsevier Masson SAS. All rights reserved. Keywords: Life; Natural selection; Darwin; Last universal common ancestor; Horizontal gene transfer 1. Introduction metabolic activity e or the potential for metabolic activity, as in seeds and spores e of unicellular and multicellular organ- This fascinating dilemma exists not only because the origin isms, which is only a transient state of being. When of Life requires the explanation of many origins, i.e. those of a prokaryote cell divides, it is no longer alive, because it is nucleotides, proteins, lipid membranes, bacterial cell walls and replaced by two other living cells. Multicellular organisms are those of metabolism and genetic coding, but especially because metabolically active with the purpose of getting their germ these molecules and processes are so intrinsically intertwined cells into the next generation and as such are only transient, within each cell that resolving the problems related to one origin temporary constructions. E.g., when devoid of oxygen, water immediately poses new problems in understanding the origin(s) or food, a human multicellular colony ceases to be alive within of other processes and building blocks. Not one, but many resp. minutes, days or weeks. Viruses, not metabolically ‘chicken and egg’ problems are involved. active, are not alive according to this definition. Obviously, a single issue is far from sufficient to present all However, the question ‘What is Life’ requires another the available data, gathered recently by origin of Life approach. Since it is generally agreed that all extant living researchers. Therefore, we have tried to cover only those cells are the descendants of the Last Universal Common aspects of the origin of Life which we consider to be most Ancestor (LUCA), which probably originated some 3e3.5 illuminating or where refreshing insights have been proposed. billion years ago, in our opinion Life can most easily and most When trying to define Life, of which we are trying to correctly be defined as the currently existing 3.5 billion year- explain the origin(s?), we suggest making the distinction old organism, consisting of all extant trillion trillion cells on between ‘Life’ and ‘being alive’ as two very different Earth, AND their associated viruses. Life is a single organism concepts, which are usually not distinguished from each other which exists since the LUCA started duplicating for the first by most philosophers, leading to several misconceptions and time, and continued to do so with, as a result, all extant cells at irrelevant discussions [14]. ‘Being alive’ concerns the this moment of which it is composed. Because Life could be considered as a single organism, we suggest writing Life with a capital ‘L’. * Corresponding author. In appreciating the model of Life as a single organism, E-mail addresses: [email protected] (M. Vaneechoutte), [email protected]fi.it (R. Fani). derived by continued and uninterrupted duplication of the first 0923-2508/$ - see front matter Ó 2009 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.resmic.2009.09.002 438 M. Vaneechoutte, R. Fani / Research in Microbiology 160 (2009) 437e440 cell, one should realize that all cells of the organism Life not all three domains of Life and ii) by acting as an important only share a common past but also are strongly interconnected, selective force, strongly influencing population dynamics being interdependent on each others’ metabolism. Prokaryote through infection, e.g. think of phage-driven bacterial pop- and eukaryote cells influence each others’ activity, whereby ulation dynamics [3] and of viral pandemics like the current the waste products of the metabolism of one cell provide the one caused by HIV. Viruses both made immune defense energy and building blocks for another cell, and these cells and possible (as important agents of HGT) and necessary (as their intrinsically associated viruses helped shape each others’ infectious agents). Viruses were probably around before the evolution through genetic exchange. Commensal, symbiotic, LUCA [8,12] and also played an important role in the origin of parasitic and pathogenic organisms and parasitic viruses, the first cell, i.e. the origin of Life. living on and within other organisms continuously influence In summary, Life includes the interactions among the the activity of the cells of their hosts and are mutually influ- metabolically active cells, which are all descendants of enced by them. Think of the continuous interaction between a common ancestral cell, with the biosphere as a whole, which our estimated log13 cells and the estimated log14 bacterial is a product of Life’s activity, and with the associated viruses. cells in our bodies, e.g. the way our native and adaptive The ‘being alive’ of individual living cells, whether existing as immune system is influenced by and influences bacterial separate entities or joined into clonal temporary colonies, can metabolism. Cells within each multicellular colony, as well, only be understood by considering the many interactions with interact continuously with each other by collaboration and other cells, viruses and the biosphere at present AND in the competition, e.g. the induction of apoptosis in other cells past. during embryology. And of course, multicellular colonies The success of research aiming at unravelling the origin of interact with each other and with their (multicellular) para- Life has increased exponentially due to the availability of sites. Even within most eukaryotic cells, we find remnants of completely sequenced genomes belonging to organisms of the ancient cooperations which have crystallized into irreversible three cell domains of Life, i.e. Bacteria, Archaea and Eukarya. endosymbioses, e.g. mitochondria and chloroplasts. For This sequence information made possible comparative anal- instance, at first sight, photosynthesizing plants might be ysis of genes and genomes, which has led to spectacular considered as autonomous, as long as there is sunlight and developments in the understanding of the molecular basis of fertile soil, but their ability to photosynthesize relies on the many biological phenomena, which, in turn, enabled shedding ancient acquisitions of photosynthetic cyanobacteria (or of light on the molecular mechanisms and forces driving the other eukaryotic photosynthesizing cells, already containing evolution of (micro)organisms. cyanobacterial descendants) by the first plant ancestor line- ages. And the fertile soil on which most plants depend was 2. Prebiotic chemistry itself created by and depends largely on the activity of bacteria and fungi and maybe also on complex microbial communities The first strong impulse for the study of the origin of Life inhabiting the phloem and xylem of the plants. was the MillereUrey experiment in 1953 [13], which repre- In brief, all present cells of the organism Life form one sents the starting point of prebiotic chemistry, a discipline giant network of multiple and very different interactions, which during the following years led to the demonstration that which can only be understood by considering the ‘evolu- the building blocks of cells can be easily synthesized under tionary history’, or in this context the ‘past lifetime’ of the putative primitive conditions, supporting Alexander Oparin’s organism Life. To quote Theodosius Dobzhansky [6]:‘Nothing ‘‘primordial soup’’ idea on the origin of Life on Earth [15]. in biology makes sense except in the light of evolution’. This special issue starts with a prebiotic chemistry paper. Another example of the importance of understanding the Saladino et al. [19] propose that formamide and water may biogeological record as determined by the activity of Life is have played a central role in the evolution of the first nucle- that Life itself has reshaped its own environment, including the otides, and propose plausible mechanisms whereby nucleo- atmosphere, the oceans and the soil, partially by ‘polluting’ it, sides, nucleotides and nucleotide oligomerization may have e.g. with oxygen, a pollution which turned out to enable the occurred in an environment of formamide, and later water. development of multicellular organisms. So Life includes the Their proposal is a very elegant one, e.g. because this oligo- interactions among the metabolically active cells, but also with merization does not require templates, catalysts or dry- the biosphere as a whole, largely a product of Life’s activity. chemistry conditions. Moreover, the proposed cyclic Our proposal to clearly distinguish ‘Life’ as an organism synthesis/degradation process for nucleic acid bases in form- from the ‘being alive’