What contemporary viruses tell us about evolution: a personal view

Abstract

Recent advances in information about viruses have revealed novel and surprising properties such as viral sequences in the genomes of various organisms, unexpected amounts of viruses and phages in the biosphere, and the existence of giant viruses mimicking bacteria. Viruses helped in building genomes and are driving evolution. Viruses and bacteria belong to the human body and our environment as a well-balanced ecosystem. Only in unbalanced situations do viruses cause infectious diseases or cancer. In this article, I speculate about the role of viruses during evolution based on knowledge of contemporary viruses. Are viruses our oldest ancestors?

Fig. 1

Pre-protein synthesis. (top) Early protein synthesis may have started with a short target RNA or ribozyme (Rz), binding to basic amino acids (K + lysine). Some plant viral genomes end with a tRNA, shown as fold-back – perhaps the future tRNA. The basic amino acids protected and enhanced the catalytic activity of the ribozyme. (bottom) This is reminiscent of today’s initiation of replication of retroviruses, which have an initiation complex similar to the early protein synthesis complex. The tRNA binds a protein, reverse transcriptase (RT) and basic proteins, the nucleocapsid proteins (NC), which melt or match the RNAs. Initiation of replication is reminiscent of primitive protein synthesis. RNA is shown in red and DNA in black. PBS, primer-binding site

Fig. 2

From RNA to proteins and DNA. Molecules may have surrounded black smokers or hot vents in the oceans and led to the formation of ribozymes or viroids, which can replicate, cleave and fuse, and evolve, which are hallmarks of life. The protein synthesis machinery consists of ribozymes and basic proteins, ribonucleoproteins (RNPs). Reverse transcriptase (RT) achieved the transition from RNA to DNA

Fig. 3

From RNA to DNA. (Top) This reaction is performed by the telomerase in every embryonic eukaryotic cell and in tumor cells at chromosomal ends. The telomerase is an RNP and copies a simple stretch of RNA into DNA up to 1000-fold. (Bottom) Reverse transcriptase (RT) copies RNA into an RNA-DNA hybrid and into a double-stranded DNA, supported by ribonuclease H (RNase H), which removes the RNA in RNA-DNA hybrids and RNA primers

Fig. 4

From RNA to cells: the putative role of viruses during evolution, viruses first. Ribozymes or viroids, perhaps in lipid bags, may have bound basic amino acids (AA+) and formed peptides (black dots), which stimulated ribozyme activities and became important multifunctional components in all RNA viruses. Self-assembling viral core structures, RNA polymerases and the RT leading to DNA, may have formed. Pararetroviruses and retroviruses used the RT to make DNA, which integrated into other DNA and helped to build up genomes. Up to 50 % retroelements are detectable today in humans. Perhaps something like giant viruses evolved into cells, with bacterial (B), archaeal (A) or eukaryotic cells (E) shedding DNA or RNA viruses. Small tailed structures symbolize phages, which are the fastest replicating and most diverse species, perhaps before separation of A,E and B. Paretroviruses are indicated by incomplete DNA genomes with RNA primers

Fig. 5

Endogenization. The endogenous retroviral elements in the human genome are attributed to previous horizontal retroviral infections. Retroviruses can in rare cases infect germline cells and be passed vertically to future generations. The host cell suppresses these genes during embryogenesis, but outside events can activate the viral elements to influence other genes. This happened to koalas in less than 100 years and made them resistant to the exogenous retrovirus. Integrated retroviruses, foamy viruses, can be dated back about 50 Mio years [53]. They do not cause diseases

Fig. 6

Endogenous retroelements (RE). (Top) A virus in a virus in a virus can be detected in cellular genes. One example is shown here with a protein kinase B inhibitor gene, which consists of up to 85 % REs [13, 59]. An integrated HERV-K(C4) is indicated. The inserts accumulate within introns, where integrations are less harmful than they would be in exons (Ex). REs comprise retroviruses and shorter versions, LINE, SINE or only LTRs [19]. (Left) The human endogenous retroviruses (HERV-K (C4)) can influence regulation of other genes, as shown for DAP3, a proapoptotic gene [13]. Antisense transcripts can shut off sense transcripts of a tumor suppressor gene and can thereby cause cancer. (Right) The number of human REs is shown as segments [modified from ref. 9]. The white area is investigated by ENCODE project

Fig. 7

Increase in the number of genes. Genes can be cut out and pasted at another site in the genome, as described for transposons. This cut-and-paste happens actively in plants but ended in human genomes 35 Mio years ago [46, 81]. This leads to new phenotypes, depending on the site of integration, e.g., different colors in maize. A copy-and-paste mechanism requires an RT and increases the gene content of a genome, in 100 Mio years accounting for 20 % of the human genome [59]

Fig. 8

Coevolution of RNase H. Viruses and hosts harbor similar elements. Viruses can provoke antiviral responses. The viral and host elements coevolve. A striking example is the composition of a retrovirus, which is analogous to that of the antiviral defense machinery [70, 72]. The RNase H is structurally related to the enzyme component of Argonaute of the small interfering siRNA machinery. The components are similar, and the enzymes involved are structurally closely related, which cannot be detected at the primary-sequence level