Abstract
This paper follows the circuitous path of theories concerning the origins of viruses from the early years of the twentieth century until the present, considering RNA viruses in particular. I focus on three periods during which new understandings of the nature of viruses guided the construction and reconstruction of origin hypotheses. During the first part of the twentieth century, viruses were mostly viewed from within the framework of bacteriology and the discussion of origin centered on the “degenerative” or the “retrograde evolution theory.” However, concomitantly, in the context of origin-of-life theorizing, the notion that viruses are vestiges of a prebiotic world was also being contemplated. In the 1960s the idea that viruses were genetic elements that “escaped” from cells became prevalent. These traditional hypotheses are being revisited nowadays by evolutionary virologists, who have placed them within a new conceptual framework that is supported by cutting-edge genomic and proteomic data. Two current, opposing scenarios of virus origin are presented. The philosophical dimensions of “revisiting” the original hypotheses are briefly discussed.
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Notes
Note, for example, articles appearing in Biological Theory, a new publication “devoted to theoretical advances in the fields of evolution and cognition with an emphasis on the conceptual integration afforded by evolutionary and developmental approaches.” http://www.mitpressjournals.org/loi/biot.
Histories of virology and virus research consulted in the writing of this article were Smith Hughs (1977) for general information on the history of virology, and Creager (2002) on the history of tobacco mosaic virus research. As concerns the history of bacterial virus research, Brock (1990) and Helvoort (1994a, b) were most helpful. Additional accounts of the history of virology used in this paper are listed in the text.
Reverse transcriptase, also known as RNA-dependent DNA polymerase, is a DNA polymerase enzyme that transcribes single-stranded RNA into double-stranded DNA. According to the “central dogma of molecular biology,” genetic information is transferred from DNA to RNA to protein. The copying of DNA into RNA is designated transcription and the process is carried out by a transcriptase (a DNA directed RNA polymerase). However, in the case of a unique group of RNA viruses, the first step in the replication of viral RNA is actually the copying of the viral RNA into a complementary DNA. This DNA is then integrated into the cell’s DNA and transcribed, i.e., new copies of the viral RNA are made serving both as viral genomes and viral mRNA. The enzyme responsible for this process was given the name “reverse transcriptase.” RNA viruses that multiply by this "reverse" mechanism were called retroviruses.
This parting of ways, however, probably began even earlier when, in the late 1940s, viruses started to be used in the context of origin-of-life theories metaphorically, and archaic macromolecules were no longer expected to fulfill the role of phylogenetic ancestors of extant viruses and organisms (Podolsky 1996).
For example, Eigen writes, "Perhaps the simplest form of virus is represented by a single strand of ribonucleic acid (RNA), made up of several thousand individual nucleotide subunits…” (1993, p. 42).
As technological advances were made during the 1930s regarding filters and microscopes, the only defining feature of viruses left was their “obligate intracellular parasitism.” (Podolsky 1996, p. 86).
Not all researchers viewed viruses as external agents. Prominent immunologist and Nobel laureate Jules Bordet saw viruses as internal products of the cell itself that caused the cell’s own destruction (Helvoort 1994b); hence my discussion of virus origin will not refer to his concept of a bacterial virus.
Laidlaw does not elaborate on this particular argument; it may be that he is referring to “spontaneous generation” controversies.
During the 1960s, Howard Temin claimed that the relationship between Rous sarcoma virus (RSV), an avian RNA cancer virus and its host cell, greatly resembled that of temperate phage/lysogenic bacteria, thus extending this special relationship between viruses and their host cells to include animal cancer viruses as well (Fisher 2009; Temin 1964).
During the early 1960s, some leading scientists, Sol Spiegelman in particular, actually thought that DNA might be a necessary intermediate in the process of RNA replication (Fisher 2009).
This is precisely where new genomic data assists virologists today to determine sequence relationships between a host cell’s genome and its virus and construct evidence-based virus origin hypotheses. See Sect. 8 in this paper.
RSV was the RNA tumor virus that Temin used, during the 1960s, in his in vitro investigation of viral induced cell transformation. The virus was first discovered in 1911 by the renowned virologist Peyton Rous, who attempted to isolate a filterable agent that apparently caused chicken sarcomas. In his Nobel lecture, Temin suggested that the virus was formed by a rare event of recombination of an avian leukosis virus (non-cancerous) and pre-existing cellular cancer genes while Rous was attempting to produce and isolate the infectious agent (Temin 1975; Cairns 1978). This way, by recombining with a functional virus, the newly formed virus would not have to acquire all the missing mechanisms to become independent (Temin 1975, p. 19).
All viruses are covered with a protein coat but some viruses—enveloped viruses—are also covered with a lipid membrane, picked up from the host cell when it is released. The lipid membrane is called an envelope.
Such as one of the ribosomal RNAs being responsible for linking the amino acids to form a new polypeptide, and not the protein component of the ribosome, as was once thought (Gesteland et al. 2006). In general, in addition to the three traditional informational roles of RNA messenger, RNA transfer and ribosomal RNA, it is now recognized that RNA takes part in down regulating gene expression; various types of RNAs have been discovered in different biological systems acting in this capacity, such as siRNA, microRNAs and RNAi (Watson et al. 2004).
Interestingly, while Rich speculated on the origin of this molecule, he still proposed a degenerative evolution theory: “It is possible that the RNA containing viruses may be regarded as present-day examples which may have degenerated evolutionarily from such a primitive life” (1962, p. 124).
In both articles (Koonin et al. 2006; Forterre 2006) extensive experimental data is provided. For example, Forterre notes that the results of analyzing more than 250 cellular genomes from the three domains of life: Archaea, Bacteria and Eukarya show that most of the viral proteins detected in viral genomes have no cellular homologues.
The idea of Last Universal Common Ancestor (LUCA) presumes a single cell from which all life has evolved.
Koonin et al. (2006). This is an open access article, which allows unrestricted use, distribution and reproduction in any medium, provided the original work is properly cited. Page numbers of the online version are not for citation purposes. Therefore, I note section titles when possible.
Koonin et al. (2006), in section “Conflicting concepts.”
A basic search in JSTOR brought up the following: “Results 1–25 of 5517 for <<revisit>>”. JSTOR search conducted 10 October 2009.
For example, in Fry’s extensive study of theories of origin of life (2000), the idea that viruses may have taken part in origin-of-life processes is barely mentioned, and the term “virus” does not even appear in the index.
Goldenfeld and Woese write: “Equally exciting is the growing realization that the virosphere plays an absolutely fundamental role in the biosphere on both immediate and long term evolutionary senses” (Goldenfeld and Woese 2007).
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Acknowledgments
The author is very grateful to Anthony S. Travis and to Ute Deichmann for their constructive advice and for their encouragement in writing this paper and would also like to thank two anonymous reviewers for their helpful comments and suggestions. Eugene V. Koonin is thanked for permission to reproduce the two figures from Koonin et al. (2006).
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Fisher, S. Are RNA Viruses Vestiges of an RNA World?. J Gen Philos Sci 41, 121–141 (2010). https://doi.org/10.1007/s10838-010-9119-8
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DOI: https://doi.org/10.1007/s10838-010-9119-8