Perspectives
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PERSPECTIVES for all cellular organisms. Carl Woese17,18 OPINION discovered the existence of three differ- ent ribosomes in the living world, which Redefining viruses: lessons from replaced the old prokaryote–eukaryote dichotomy with a trinity — archaea, bacteria Mimivirus and eukarya. All cellular organisms could thus be placed together in a universal tree of life. Viruses, however, were missing from Didier Raoult and Patrick Forterre this picture. Abstract | Viruses are the most abundant living entities and probably had a major role Unlike most other microorganisms, viruses are obligate intracellular parasites that in the evolution of life, but are still defined using negative criteria. Here, we propose cannot replicate independently. They can to divide biological entities into two groups of organisms: ribosome-encoding infect organisms from all three domains of organisms, which include eukaryotic, archaeal and bacterial organisms, and capsid- life, and can even parasitize other viruses; encoding organisms, which include viruses. Other replicons (for example, plasmids for example, the delta agent (with the 19 and viroids) can be termed ‘orphan replicons’. Based on this suggested classification hepatitis B virus ) and satellite viruses (with an adenovirus or tobacco mosaic system, we propose a new definition for a virus — a capsid-encoding organism that is virus (TMV)20,21). Despite their ubiquity composed of proteins and nucleic acids, self-assembles in a nucleocapsid and uses a and enormous importance to human ribosome-encoding organism for the completion of its life cycle. health, viruses have long been neglected by evolutionary biologists, and are thought to The Darwinian revolution created a new bacteria9, and the recent discovery of the be derived from cells. Indeed, as a direct approach to classification by proposing a largest known virus, Mimivirus10–13 (FIG. 1), consequence of the cellular theory that common origin for living organisms. Since we propose a new definition for the virus life was established in the nineteenth century, then, scientists have grouped animals and form. Of course, any attempt to redefine an living organisms and cellular organisms are plants phylogenetically, rather than by gross entire field will be controversial; however, a synonymous to most scientists. appearance. The genetic revolution and our debate of this issue, using all of the currently Viruses were initially thought to be ability to build trees based on genetic simi- available data, is needed. We propose a defi- infectious agents that are not visible under larities provided support for this method nition of viruses (and cells) that is based on a microscope and can be filtered through of classification. Over the past 30 years, the the hypothesis that viruses are more than just 0.22 µm ultrafilters (hence the name development of more efficient sequencing parasitic nucleic acids and that the presence ‘ultravirus’)22,23. During the twentieth strategies has led to the reclassification of of either capsids or ribosomes forms the century, researchers developed two theories organisms into a universal tree of life based basis of the principal classification system in about viruses. The bacteriologists Felix on ribosomal RNA sequences1. Viruses, the living world. d’Herelle, who discovered bacteriophages, however, lack ribosomes and have not yet and Macfarlane Burnet, who received the been incorporated into this universal tree Defining viruses — a history Nobel Prize in medicine in 1960, believed of life. According to Karl Popper14, definitions that viruses were organisms24,25 (as did Louis Until now, the genetic information that are based on the data and tools that are Pasteur), whereas Wendell Stanley26, who is encoded by viruses was not thought to available at a specific moment in time. In crystallized TMV and received the Nobel contain sufficient information to allow their the nineteenth century, the word ‘microbes’ Prize in chemistry in 1946, believed that general phylogenetic classification, and was coined by Sedillot15 to define cellular viruses were biomolecules. Later, while pro- consequently no clear definition of viruses microorganisms that were only visible using moting the eukaryote–prokaryote dichotomy, is currently available. This is unfortunate, as a microscope. In the middle of the twentieth Andre Lwoff 22 defined viruses as small (one viruses are the most abundant living entities century, microorganisms were divided into dimension smaller than 0.2 µm), infectious, on the planet2 and metagenomic studies from two groups, eukaryotes and prokaryotes, but not autonomous, agents that cannot randomly sequenced environmental samples based on cellular structural features16. divide by binary fission, and consist of pro- have revealed that viral genes constitute Eukaryotic cells have a nucleus and a nuclear teins and a single type of nucleic acid. Lwoff the largest part of the genosphere2,3. Recent membrane, whereas prokaryotic cells do not insisted that viruses are not organisms and research has revealed an important role for (although Planctomycetes, such as Gemmata maintained that the infectious element of viruses in various evolutionary scenarios, obscuriglobus, are bacteria that have a nucleus the virus is the nucleic acid, unlike bacteria including the origin of DNA and mam- and a nuclear membrane)16. In the last part of or other pathogens, in which the infectious mals4–7. Here, based on our knowledge of the twentieth century, molecular-biology tools agent is the organism itself (although this archaea, archaeal viruses8 and intracellular opened the way for a new classification system theory has been contradicted recently27). nature reviews | MICROBIOLOGY volume 6 | april 2008 | 315 © 2008 Nature Publishing Group PERS P ECTIVES as “An individual living system such as animal, plant, fungus or microorganism” by Wikipedia, “An individual animal, plant or single-celled life form” by the Oxford English Dictionary Online and “Any living structure capable of growth and reproduc- MV tion” by Chambers Reference Online (see Further information). The definitions N from Wikipedia and the Oxford English Dictionary Online exclude intracellular VF parasites, symbionts, organelles and viruses. The definition from Chambers Reference Online, however, includes viruses and nucleic acids, as it does not retain the word cell. Mimivirus changed the perception of viruses and could also change the defini- tion of an organism. Mimivirus virions are assembled at the periphery of a large membrane-bound nucleus-like structure — the viral factory — within the host cell (FIG. 1). Although viral factories have been described for most eukaryotic viruses 2 µm (both RNA and DNA)33, the viral factory 12 Figure 1 | Mimivirus infecting Acanthamoeba polyphaga. Transmission electron microscope image of the Mimivirus is especially spectacular that shows A. polyphaga infected with Mimivirus. Note the giant virus factory. N, nucleus; VF, virus and, when first observed using an electron factory; MV, Mimivirus virions. Nature Reviews | Microbiology microscope, was initially thought to be the nucleus of its giant amoebae host. Jean- Michel Claverie34 proposed that viruses Viruses were thus tacitly defined by most Defining organisms and living entities are entities that are associated with an molecular biologists as molecular genetic The general consensus of what constitutes intracellular viral factory, and should not be parasites that use cellular systems for their life can be sampled by consulting a global confused with virions. Interestingly, from own replication22. Indeed, with such a broad resource such as Wikipedia (the largest this view, a virus is similar to an intracellu- definition, many types of selfish genetic free online encyclopaedia; see Further lar organism, which therefore further blurs elements (such as plasmids, transposons, information), which defines life as ‘‘a the boundary between cellular organisms retroposons, viroids and virusoids) were condition that distinguishes organisms and viruses. determined to be viruses. For example, from inorganic objects’’. However, there The virus definition can also be modi- Koonin et al.28,29 recently grouped all infec- is no universal definition of life. The fied by the distinction between a virus tious-material-containing nucleic acids as frequently used ‘reproduction’ criterion and a virion. A virus can be generated either selfish elements and/or viruses and does not apply to sterile organisms. The from synthetic oligonucleotides by whole- used these terms synonymously. distinction between parasites (replicators) genome assembly to produce infectious Each of the definitions for viruses has and free-living organisms cannot be used virions35. Therefore, we believe that a recently been challenged by the discovery to distinguish between organisms. There is virus can be entirely defined by its coding of viruses that are larger than cellular now no clear-cut limit between mitochon- capacity. As for bacteria, it was recently organisms10,30. Indeed, both the particle and dria, small symbionts, intracellular bacteria shown that genome transplantation from genome sizes of viruses now overlap sig- (such as Rickettsia spp. and Candidatus one species to another is possible, and nificantly with those of bacteria, eukaryotes Carsonella spp.) and free-living bacteria that cells which were transplanted with and archaea. Mimivirus, the largest known in size or phylogenetically31. Some recent the genome of Mycoplasma mycoides were