Rhizome of life, catastrophes, sequence exchanges, gene creations and giant viruses: How microbial genomics challenges Darwin

REVIEW ARTICLE published: 2778 August 2012 doi: 10.3389/fcimb.2012.00113 CELLULAR AND INFECTION MICROBIOLOGY Rhizome of life, catastrophes, sequence exchanges, gene creations, and giant viruses: how microbial genomics challenges Darwin Vicky Merhej and Didier Raoult* URMITE, UM63, CNRS 7278, IRD 198, INSERM U1095, Aix Marseille Université, Marseille, France Edited by: Eugene V. Koonin, National Institutes of Health, USA Reviewed by: James E. Graham, University of Louisville School of Medicine, USA Jose Vazquez-Boland, University of Edinburgh, UK *Correspondence: Didier Raoult, Faculté de Médecine, URMITE, UMR CNRS 7278, IRD 198, INSERM U1095, 27 Bd Jean Moulin, 13385 Marseille cedex 5, France. e-mail: Darwin’s theory about the evolution of species has been the object of considerable dispute. In this review, we have described seven key principles in Darwin’s book The Origin of Species and tried to present how genomics challenge each of these concepts and improve our knowledge about evolution. Darwin believed that species evolution consists on a positive directional selection ensuring the “survival of the fittest.” The most developed state of the species is characterized by increasing complexity. Darwin proposed the theory of “descent with modification” according to which all species evolve from a single common ancestor through a gradual process of small modification of their vertical inheritance. Finally, the process of evolution can be depicted in the form of a tree. However, microbial genomics showed that evolution is better described as the “biological changes over time.” The mode of change is not unidirectional and does not necessarily favors advantageous mutations to increase fitness it is rather subject to random selection as a result of catastrophic stochastic processes. Complexity is not necessarily the completion of development: several complex organisms have gone extinct and many microbes including bacteria with intracellular lifestyle have streamlined highly effective genomes. Genomes evolve through large events of gene deletions, duplications, insertions, and genomes rearrangements rather than a gradual adaptative process. Genomes are dynamic and chimeric entities with gene repertoires that result from vertical and horizontal acquisitions as well as de novo gene creation. The chimeric character of microbial genomes excludes the possibility of finding a single common ancestor for all the genes recorded currently. Genomes are collections of genes with different evolutionary histories that cannot be represented by a single tree of life (TOL). A forest, a network or a rhizome of life may be more accurate to represent evolutionary relationships among species. Keywords: catastrophes, Darwin, gene creation, giant viruses, micorbial genomics, rhizome of life, sequence exchange INTRODUCTION The theory of evolution became a subject of deep reflection toward the end of the twentieth century. The development of the theory of evolution has benefited from the contributions of several authors, including Lamarck and Darwin (Koonin and Wolf, 2009). Their findings have been subjected to intense criticism. Indeed, their claim that all living species were transformed over time to give rise to new species was much to the dismay of the creationists (the equivalent of the “fixistes” in France) who believed that each species was created once and for all and that no species had disappeared since the creation. This latter perception of the worlds is a synthesis between the Socratic Greek philosophy, the harmonious cosmos and the essentialism of Plato (427–327 BCE) and Aristotle (384–322 BCE) on one hand and the Christians’ view of the world’s creation as described in the bible on the other hand. In contrast, the monistic view of Heraclitus (535–475 BCE), the constant motion of Democritus (460–370 BCE) and the dynamic theory of atomic Frontiers in Cellular and Infection Microbiology motion described by Lucretius (94?–55 BCE) considered life to be an interplay of physical-chemical forces immanent to matter and in which living things live in perpetual motion. In this context, Lucretius’ Epicurean poem, De rerum natura, postulated the extinction of species that are not well suited to surviving and reproducing successfully (Lucretius, 1995). Darwin developed a highly disputed theory that was largely influenced by the works of Buffon on transformism (de Buffon, 1753), the concept of the differential fertility of Malthus (Malthus, 1798; Barlow, 1958) and the gradualism of Leibniz (Leibniz, 1996). Darwin proposed a straightforward mechanism of evolution that involves an interplay between heritable variation and natural selection, collectively described as the survival of the fittest. Under Darwin’s concept, the material for evolution is provided by heritable random variation; natural selection is the main driving force of evolution, which introduces order and produces increasingly complex adaptive features of organisms. Darwin thought of natural selection in terms of the fixation of www.frontiersin.org August 2012 | Volume 2 | Article 113 | 1 Merhej and Raoult How microbial genomics challenge Darwin beneficial changes, i.e., evolutionarily relevant mutations. These beneficial changes have infinitesimally small effects on fitness, and, as a result, evolution occurs via numerous, successive and slight modifications according to the theory of strict gradualism. Finally, Darwin suggested that all life forms evolved from a single common ancestor (Darwin, 1859). Indeed, based on his observations on the evolution of animals, Darwin attempted to issue a general theory about the evolution of life. He proposed that the relationships among all species resemble a tree, the Tree of Life (TOL), in which all living organisms are considered to have descended from a single ancestor (Darwin, 1859). Darwin’s theory was later the object of considerable dispute, particularly because Darwin was unaware of Mendel’s work and of the importance of genetics for understanding evolution (Charlesworth and Charlesworth, 2009). Fisher, Haldane, Dobzhansky, Wright and Mayr, among many others, integrated genetics, paleontology, systematics, and cytology within a newly expanded structure of biological thought that is often referred to as “the modern Synthesis” (Huxley, 1942; Koonin, 2009d). The modern synthesis provided useful foundations for biological thought, including the idea that changes in genotype, the genetic material, precede changes in the phenotype, which determines the appearance of an individual. The modern synthesis framework provided many fundamental insights into evolutionary biology, especially with regards to the main topic of Darwin’s famous book, The Origin of Species (Darwin, 1859). Darwin thought that species were the result of the human predilection to perceive discontinuity among continuously varying individuals. Mayr’s extensive knowledge about variation in morphology, overlain with an (...truncated)