Viruses and cells intertwined since the dawn of evolution

Abstract

Many attempts have been made to define nature of viruses and to uncover their origin. Our aim within this work was to show that there are different perceptions of viruses and many concepts to explain their emergence: the virus-first concept (also called co-evolution), the escape and the reduction theories. Moreover, a relatively new concept of polyphyletic virus origin called "three RNA cells, three DNA viruses" proposed by Forterre is described herein. In this paper, not only is each thesis supported by a body of evidence but also counter-argued in the light of various findings to give more insightful considerations to the readers. As the origin of viruses and that of living cells are most probably interdependent, we decided to reveal ideas concerning nature of cellular last universal common ancestor (LUCA). Furthermore, we discuss monophyletic ancestry of cellular domains and their relationships at the molecular level of membrane lipids and replication strategies of these three types of cells. In this review, we also present the emergence of DNA viruses requiring an evolutionary transition from RNA to DNA and recently discovered giant DNA viruses possibly involved in eukaryogenesis. In the course of evolution viruses emerged many times. They have always played a key role through horizontal gene transfer in evolutionary events and in formation of the tree of life or netlike routes of evolution providing a great deal of genetic diversity. In our opinion, future findings are crucial to better understand past relations between viruses and cells and the origin of both.

Fig. 1

Three major theories of virus origin. Arrows show the direction of evolutionary changes. a. According to the virus-first hypothesis at the dawn of life there were no cellular forms but only first RNA molecules possessing enzymatic activities and capable of self-replication, also called selfish genetic elements. b. According to the escape hypothesis viruses derived from cellular RNA or/and DNA fragments such as plasmids and transpozons. During asymmetrical cell fission a vesicle (smaller cell-like entity) could have formed engulfing a self replicating RNA and a coat encoding RNA segment. c. According to the reduction hypothesis viruses come from small primordial cells (not necessarily primitive), which lost their cellular elements in the course of evolution. They maintained, however, their genetic material and certain elements needed for replication. Proto-cells presented in this picture already contained ribosomes (black small plain circles) and were able to produce proteins/capsids, whereas cells containing a nucleus correspond to modern cells, which descended from LUCA. Eukaryotic cells were used to depict all three hypotheses of virus origin and underline a possible involvement of viruses in eukaryogenesis

Fig. 2

Tree of life. Schematic presentation of the tree of life. Viruses are depicted as small hexagons. Viral lineages are traced as “lianas” wrapping around the trunk and three major branches - domains of life. Horizontal gene transfer (HGT) between cells and viruses is marked as a source of genetic diversity. Viral origin of eukaryal nucleus and bacterial origin of mitochondria and chloroplasts are depicted. Only chosen phyla are presented on the top of the tree. The taxonomy of Archaea is presented according to Brochier-Armanet et al. [91]. For a more detailed taxonomy of major phyla in Eukarya and Bacteria one may refer to Zhao et al. [92], and Chun et al. [93], respectively