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Cellular domains and viral lineages Patrick Forterre1,2, Mart Krupovic1, and David Prangishvili1 1
Institut Pasteur, 25 rue du Dr Roux, 75015, Paris, France Institut de Ge´ne´tique et Microbiologie, University Paris-Sud, Centre National de la Recherche Scientifique (CNRS) UMR 8621, 91405 Orsay CEDEX, France
2
It has been claimed that giant DNA viruses represent a separate, fourth domain of life in addition to the domains of Bacteria, Archaea, and Eukarya. Such classification disregards fundamental differences between the two types of living entities – viruses and cells – and results in confusion and controversies in evolutionary scenarios. We highlight these problems and emphasize the importance of restricting the term ‘domain’ to the descendants of the last universal cellular ancestor (LUCA), based on the shared ribosome structure. We suggest tracing phylogeny of viruses along evolutionary lineages primarily defined by virion architectures and the structures of the major capsid proteins. Domains of life More than two decades ago Woese, Kandler, and Wheelis proposed the term ‘domain’ for the three evolutionary cellular lineages identified by 16/18S rRNA comparison: Archaea, Bacteria, and Eukarya [1]. This tripartite division has been validated by comparative genomics, although the tree of life topology is still debated [2–4]. However, in recent years, the notion of a ‘fourth domain’ has made its way into scientific literature [5–10]. Didier Raoult and coworkers have argued that giant DNA viruses of the proposed order Megavirales [11] (formerly nucleocytoplasmic large DNA viruses, NCLDV) represent a fourth domain of life [9] because their genomes encode some universal proteins, such as RNA polymerases, that in some phylogenetic analyses form a fourth monophyletic group in addition to the domains of Bacteria, Archaea, and Eukarya [5,6,11,12]. The term ‘fourth domain’ can imply either that Megavirales universal proteins originated from a fourth cellular lineage descending from the LUCA – that is now extinct but passed its genes to the ancestor of Megavirales – or that this ancient cellular lineage was itself transformed into the ancestor of the Megavirales. The term ‘fourth domain’ is now often used in the scientific literature [7,13,14], although the four-domain hypothesis itself is controversial. Notably, recent discussions in review papers in Nature and Science led to contradictory statements [8,10]. For example, it has been claimed that more than four domains of life possibly exist [8] or, on the contrary, that the ‘domain of life is an archaic Corresponding author: Forterre, P. ([email protected]). Keywords: viruses; phylogeny; evolution; tree of life; mimivirus. 0966-842X/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tim.2014.07.004
concept’ [8]. Indeed, the ‘viral’ domain hypothesis opens a Pandora box because it is unclear how many viral domains should be considered. Notably, some large DNA viruses, such as members of the families Baculoviridae and Nudiviridae, encode RNA polymerases that are extremely divergent from their homologs in the genomes of cellular organisms and viruses of the Megavirales, sharing no detectable sequence similarity at the amino acid level [15,16]. These viruses are therefore good candidates for additional domains (Figure 1A). Moreover, the question arises of whether, besides large DNA viruses, additional viral domain(s) should be introduced for classification of small DNA viruses, or even RNA viruses. It may be tempting to separate large (giant) and small viruses and restrict the term ‘domain’ to the giant ones. However, this is clearly unjustified because there is a continuum of genome sizes in the viral world, and any threshold between small and large viruses seems arbitrary: the genome sizes of viruses of the Megavirales (including pandoraviruses [17], see below) overlap with those of members of the families Baculoviridae and Nimaviridae, and of the order Caudovirales (Figure 1B). Finally, consideration of double-stranded DNA (dsDNA) viruses separately from the rest of the virosphere appears to be artificial because some groups of dsDNA viruses are clearly related to single-stranded DNA (ssDNA) viruses, and even to RNA viruses, and should be considered in the framework of an evolutionary continuum [18,19]. As expected, the four-domain hypothesis has been hotly debated and criticized [20–24]. The notion that viruses could form domains of life was first rejected by scientists who argued that viruses are not living, for example because they lack integrated metabolic activity and the ability to capture and store free energy [23]. The four-domain hypothesis has also been refuted on methodological grounds by some authors who revisited the phylogenies of universal proteins from viruses of the order Megavirales. They concluded that these proteins were in fact derived from eukaryotes because they sometimes branch within eukaryotic sequences in their phylogenetic analyses [20–22,24]. However, these criticisms are themselves controversial. On theoretical grounds, the nature of viruses, living or not, is a matter of debate. For instance, one of us proposed that viruses may be considered as living organisms once they have redirected the metabolism of the infected cell (the virocell) for their own purposes ([25] and references therein). Considering viruses as non-living biological entities usually pairs with underestimating their role in the evolution of life [23]. By contrast, regarding viruses as Trends in Microbiology xx (2014) 1–5
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Schemac of evoluonary relaonships between DNA-dependent RNA polymerases
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Figure 1. (A) Schematic evolutionary relationships between viral (red) and cellular (blue) DNA-dependent RNA polymerases. The baculovirus RNA polymerase is very divergent and cannot be aligned with the other RNA polymerases (indicated by a broken line). However, its size and conserved active site residues [16] suggest homology to cellular polymerases. (B) Range of genome sizes for different groups of viruses with double-stranded DNA genomes. Pandoravirus genomes have been grouped with the proposed order Megavirales, according to [42], although final classification awaits further analyses of proteins involved in virion formation.
living emphasizes their major contribution to the evolution of cellular organisms, placing viruses and cells on the same footing. In fact, the definition of a living organism is not as trivial as it could seem a priori. For example, there is an evolutionary continuum between ‘living’ bacteria, on the one hand, and mitochondria and hydrogenosomes, two biological ‘non-living’ entities, on the other. In any case, if viruses are considered by some to be living, it becomes a priori reasonable to ask the question of their place, possibly as new domain(s), in the tree of life. On methodological grounds, the phylogenetic analyses used to dismiss the four-domain hypothesis as well as their interpretation can be disputed. Phylogenies of megaviral proteins with eukaryotic affinity are often ambiguous and can be interpreted differently depending on the evolutionary scenario favored by the authors [26]. In some cases, eukaryotic proteins that branch with megaviral proteins in phylogenetic trees could have been transferred from megaviruses to eukaryotic cells, confusing the picture. Indeed, ancient transfers from Megavirales to eukaryotes (or protoeukaryotes) cannot be excluded because Megavirales can integrate their genomes into the genomes of their hosts [27–29]. In many cases, eukaryotes branch within clades corresponding to members of the Megavirales, supporting the idea that several important eukaryotic informational proteins were recruited from the giant viruses [30–32]. Moreover, universal proteins encoded by viruses belonging to various families of the Megavirales are often very divergent [28,30,32]; this muddles the picture even further in phylogenetic analyses and could suggest the existence of more than four domains if virus classification into domains is based on these proteins. Finally, the term ‘fourth domain’ 2
is difficult to accommodate in the scenarios in which informational proteins working with DNA, including those encoded by members of the Megavirales, originated in an ancient viral world and were later recruited by cellular organisms [33]. Under such a scenario the last common ancestors of these proteins might not have been present in LUCA but in ancient viral ancestors, whereas the hallmark of the three domains is their common descent from LUCA. Thus, the arguments used pro and con for the fourdomain hypothesis are often based on controversial interpretations, and this debate could remain undecided for a long time. In the meantime, much confusion may be created in the scientific and public debate concerning the nature and origin of viruses, and the concept of the domain [8,9]. However, in our opinion, besides the problems already mentioned (such as how many viral domains there are and whether RNA viruses are also eligible for forming additional domains) the four-domain hypothesis raises a major concern that we would like to discuss here. We also take this opportunity to revisit the domain definition itself, the major legacy of the late Carl Woese to biology [34]. Our goal is to help to define terminology, which would be based on solid ground and would be acceptable to scientists with different views on viruses. Domains do not apply to viruses In our opinion, the concept of domain applied to viruses is inappropriate because it blurs the gap between viruses and the rest of the biosphere, weakening the uniqueness and originality of viruses. The idea to conflate viruses and cells may appear tempting as a way to unify the entire biosphere. This idea has been promoted, for instance, by authors who have suggested that giant viruses originated
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Opinion via regressive evolution from extinct cellular domains [7,35]. Hence, in a recent review, Claverie and Abergel argue that: ‘the discovery of increasingly reduced parasitic cellular organisms and that of giant viruses exhibiting a widening array of cellular-like functions may ultimately abolish the historical discontinuity between the viral and the cellular world’ [36]. However, the regressive hypothesis for the origin of giant viruses is far from proven. Giant members of the Megavirales are not only evolutionarily related to much smaller viruses of the Megavirales (e.g., poxviruses) but also (via their major capsid proteins and packaging ATPases) to small DNA viruses infecting Archaea and Bacteria [37–40]. For some authors this suggests that giant viruses of the Megavirales did not derive from an extinct fourth domain of life but instead evolved from smaller viruses by genome expansions [26,40,41]. A recent analysis suggests, for instance, that giant pandoraviruses do not represent a new domain but are evolutionarily related to algae-infecting viruses of the family Phycodnaviridae (one of the families within the Megavirales), implying that giant viruses originated independently at least twice in the Megavirales order [42]. Comparative genomic analyses suggest that members of the Megavirales evolved by successive steps of genome expansions and reduction (genomic accordion) [41]. In any case, even if giant viruses have originated from extinct cellular domains (something we do not believe in), they would be now completely different organisms compared to their cellular ancestors. The discontinuity between the viral and cellular worlds is not a convention of biologists biased by the history of virus discovery, but is a reflection of the existence of two very different types of biological organisms in the biosphere. Whereas cellular organisms (Archaea, Bacteria, and Eukarya) reproduce by cell division (as well as a step of cell fusion in the case of sexual eukaryotes), viruses reproduce by producing virions, a completely different mode of genome dissemination. Moreover, viruses and cells clearly have very distinct, even if intertwined, evolutionary histories. Archaea, bacteria, and eukaryotes encode the ribosome, allowing them to synthesize their proteins and to live either as free-living organisms or as parasites of other organisms. By contrast, because viruses lack the protein synthesis machinery they can only propagate their genetic information as parasites of organisms encoding ribosomes: members of the domains Archaea, Bacteria, or Eukarya. This distinction still holds, even after the discovery of the pandoraviruses, because their megagenomes (for the two described species) do not encode any ribosomal protein or ribosomal RNA (rRNA). By contrast, all cellular organisms, with the exception of some reduced intracellular bacteria en route to becoming organelles, encode a complete set of ribosomal proteins and rRNA-encoding genes. To emphasize these distinctions, viruses have been defined by Raoult and Forterre as capsid-encoding organisms, as opposed to ribosome-encoding organisms [43]. The capsid indeed can be considered as the hallmark of the virus to prevent confusion between viruses and other types of biological entity such as plasmids or infectious RNA [44,45]. These parasitic elements (orphan replicons sensu Raoult and Forterre [43]) are evolutionarily related to
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viruses [45] and, as suggested by Koonin and Dolja, can be viewed as members of a ‘greater viral world’ characterized by parasitism and shared information [46,47]. However, they should not be confused with bona fide viruses because they do not rely on the production of virions to propagate their genetic information. To be consistent with the definition of viruses and cells based on capsids and ribosomes, respectively, we find it important to restrict the term domain to ribosome-encoding organisms. This opinion is based on the fact that archaea, bacteria, and eukaryotes are classified according to their evolutionary relationships based on properties of rRNA. By contrast, viruses can be grouped into lineages, based on the evolutionary trajectories of the virions and their production mechanisms. Analysis of major capsid proteins is one way to follow these trajectories. This is not always an easy task because these trajectories can be complex, involving possible recombination of gene cassettes encoding structural components with those encoding replication proteins [48,49]. Nevertheless, two major lineages of dsDNA viruses have been already successfully defined based on the structures of the major capsid proteins and genome-packaging ATPases [37–40]. Members of the Megavirales belong to one of them, the so-called PRD1like lineage. This lineage encompasses archaeal, bacterial, and eukaryotic viruses whose major capsid proteins adopt the double-jelly roll fold and whose genome-packaging machineries are based on homologous ATPases of the FtsK/HerA superfamily. The other major lineage, the socalled HK97-like lineage, groups archaeal and bacterial members of the Caudovirales with eukaryotic members of the order Herpesvirales whose major capsid proteins adopt the HK97 fold and whose genome-packaging machineries are based on homologous ATPases, different from those operating in viruses of the PRD1-like lineage. Evolutionary lineages based on major capsid proteins have been also used to define three major groups of archaeal dsDNA viruses, the order Ligamenvirales, and the families Bicaudaviridae and Fuselloviridae [50,51]. Finally, major evolutionary lineages based on virion architecture have been also proposed for RNA viruses [38]. However, it should be emphasized that, owing to pervasive recombination between viruses belonging to widely different groups [32,41,52,53], a classification based on a single virusencoded component, however important for virus propagation this component may be, will not necessarily faithfully reflect the complete evolutionary history of a viral group. For instance, in the case of capsid-based classification, one can expect that in the course of evolution of viruses with complex virions a particular capsid protein might be lost or exchanged for a different one. Indeed, the recently described pandoravirus lacks the major capsid protein typical of the PRD1-like lineage [17], although some of its replication proteins linked this virus to other members of the Megavirales [42]. Considering the huge complexity of the Pandoravirus virion, it is possible that the lacking protein became dispensable in this particular family of the Megavirales. Indeed, although a homolog of the double jelly-roll major capsid protein is still present in poxviruses, its function in virion assembly and architecture has been considerably modified [54]. Alternatively, it is possible that 3
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Opinion the Pandoravirus represents an independent evolutionary lineage which acquired specific genes from members of the Megavirales. More information is clearly necessary to determine to what extent the evolutionary trajectories of the Pandoravirus and the Megavirales overlap. Finally, whereas knowledge of virion architecture is essential for defining the major evolutionary lineages of viruses, information regarding other components that are important for virus replication and dissemination should also be taken into account. The classification of ribosome-encoding organisms into domains, and virion-producing organisms into evolutionary lineages, has several advantages. In both cases we have a natural classification based on the evolution of the hallmarks of the organism, the ribosome and virion, respectively. Besides rectifying the confusion between the two types of organisms, such classification avoids giving similar names to evolutionary lineages with very different histories. The three cellular domains are monophyletic, with all members of these domains being ultimately descendants of LUCA. The existence of such an ancestor is a logical consequence of the binary mechanism of cell division: the coalescence of all modern lineages when going back in time for each of them from daughter cells to mother cells, and so forth. By contrast, viruses are polyphyletic. Indeed, protein components defining major viral lineages, such as PRD1-like and HK97-like, are not homologous, indicating independent origins [37,38]. In fact, the mode of genome dissemination typical of viruses, in other words, the production of virions, most likely originated several times independently at an early stage of evolution, and after the emergence of ribosome-encoded proteins (by definition), but before the time of LUCA [55]. Importantly, the definition of viruses as capsid- or more precisely virion-encoding organisms, and of archaea, bacteria, and eukarya as ribosome-encoding organisms, is operational in our time of metagenomic analyses. When a large genome is sequenced and assembled from metagenomic data, the absence of ribosomal proteins- and rRNA-encoding genes immediately suggests that such genome does not correspond to a novel domain of life but instead to a viral genome (or to a megaplasmid). The presence of a gene encoding a recognizable capsid protein will indicate that we are dealing with a viral genome, allowing assignment of the genome to a particular viral lineage. Concluding remarks and future directions In conclusion, the major differences between viruses and cells strongly call for restricting the term domain to the descendants of LUCA, based on their ribosome structure, in agreement with its historical definition [1]. We therefore think that the concept of domain is far from being archaic, but on the contrary is still valid and remains a major legacy of the late Carl Woese to biology [34,56]. Finally, where should we place viral lineages in the tree of life describing the evolutionary relationships between the three cellular domains? Viruses are both major quantitative components of the biosphere and major growth factors for cellular evolution [57–59]. Thus, viruses are an essential part of the living world and should be, one way or 4
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the other, integrated in a metaphoric tree of life. Exploration of the viral world has revealed that many lineages of viruses indeed co-evolved with their hosts within each cellular domain, producing three ‘viral spaces’ that overlap with the three cellular domains [60]. Viruses are therefore here, there, and everywhere; the tree of life being infected by viruses from the roots to the leaves. In other words, denying domain status to viruses does not diminish their importance in the evolution of life. References 1 Woese, C.R. et al. (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. U.S.A. 87, 4576–4579 2 Forterre, P. (2013) The common ancestor of archaea and eukarya was not an archaeon. Archaea 2013, 372396 3 Gribaldo, S. et al. (2010) The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat. Rev. Microbiol. 8, 743–752 4 Williams, T.A. et al. (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504, 231–236 5 Boyer, M. et al. (2010) Phylogenetic and phyletic studies of informational genes in genomes highlight existence of a 4 domain of life including giant viruses. PLoS ONE 5, e15530 6 Colson, P. et al. (2011) The giant Cafeteria roenbergensis virus that infects a widespread marine phagocytic protist is a new member of the fourth domain of life. PLoS ONE 6, e18935 7 Legendre, M. et al. (2012) Genomics of Megavirus and the elusive fourth domain of Life. Commun. Integr. Biol. 5, 102–106 8 Pennisi, E. (2013) Ever-bigger viruses shake tree of life. Science 341, 226–227 9 Raoult, D. et al. (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306, 1344–1350 10 Zakaib, G.D. (2011) The challenge of microbial diversity: out on a limb. Nature 476, 20–21 11 Colson, P. et al. (2013) ‘Megavirales’, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch. Virol. 158, 2517–2521 12 Sharma, V. et al. (2014) DNA-dependent RNA polymerase detects hidden giant viruses in published databanks. Genome Biol. Evol. 6, 1603–1610 13 Yutin, N. et al. (2013) Mimiviridae: clusters of orthologous genes, reconstruction of gene repertoire evolution and proposed expansion of the giant virus family. Virol. J. 10, 106 14 Wu, D. et al. (2011) Stalking the fourth domain in metagenomic data: searching for, discovering, and interpreting novel, deep branches in marker gene phylogenetic trees. PLoS ONE 6, e18011 15 Passarelli, A.L. and Guarino, L.A. (2007) Baculovirus late and very late gene regulation. Curr. Drug Targets 8, 1103–1115 16 Ruprich-Robert, G. and Thuriaux, P. (2010) Non-canonical DNA transcription enzymes and the conservation of two-barrel RNA polymerases. Nucleic Acids Res. 38, 4559–4569 17 Philippe, N. et al. (2013) Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341, 281–286 18 Krupovic, M. (2013) Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr. Opin. Virol. 3, 578–586 19 Roine, E. et al. (2010) New, closely related haloarchaeal viral elements with different nucleic acid types. J. Virol. 84, 3682–3689 20 Lopez-Garcia, P. and Moreira, D. (2009) Yet viruses cannot be included in the tree of life. Nat. Rev. Microbiol. 7, 615–617 21 Moreira, D. and Brochier-Armanet, C. (2008) Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol. Biol. 8, 12 22 Moreira, D. and Lopez-Garcia, P. (2005) Comment on ‘The 1.2megabase genome sequence of Mimivirus’. Science 308, 1114 23 Moreira, D. and Lopez-Garcia, P. (2009) Ten reasons to exclude viruses from the tree of life. Nat. Rev. Microbiol. 7, 306–311 24 Williams, T.A. et al. (2011) Informational gene phylogenies do not support a fourth domain of life for nucleocytoplasmic large DNA viruses. PLoS ONE 6, e21080
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Opinion 25 Forterre, P. (2013) The virocell concept and environmental microbiology. ISME J. 7, 233–236 26 Forterre, P. (2010) Giant viruses: conflicts in revisiting the virus concept. Intervirology 53, 362–378 27 Delaroque, N. and Boland, W. (2008) The genome of the brown alga Ectocarpus siliculosus contains a series of viral DNA pieces, suggesting an ancient association with large dsDNA viruses. BMC Evol. Biol. 8, 110 28 Maumus, F. et al. (2014) Plant genomes enclose footprints of past infections by giant virus relatives. Nat. Commun. 5, 4268 29 File´e, J. (2014) Multiple occurrences of giant virus core genes acquired by eukaryotic genomes: The visible part of the iceberg? Virology http:// dx.doi.org/10.1016/j.virol.2014.06.004 30 File´e, J. et al. (2002) Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J. Mol. Evol. 54, 763–773 31 Forterre, P. et al. (2007) Origin and evolution of DNA topoisomerases. Biochimie 89, 427–446 32 Yutin, N. and Koonin, E.V. (2012) Hidden evolutionary complexity of nucleo-cytoplasmic large DNA viruses of eukaryotes. Virol. J. 9, 161 33 Forterre, P. (2002) The origin of DNA genomes and DNA replication proteins. Curr. Opin. Microbiol. 5, 525–532 34 Albers, S.V. et al. (2013) The legacy of Carl Woese and Wolfram Zillig: from phylogeny to landmark discoveries. Nat. Rev. Microbiol. 11, 713– 719 35 Nasir, A. et al. (2012) Viral evolution: primordial cellular origins and late adaptation to parasitism. Mob. Genet. Elements 2, 247–252 36 Claverie, J.M. and Abergel, C. (2013) Open questions about giant viruses. Adv. Virus Res. 85, 25–56 37 Krupovic, M. and Bamford, D.H. (2011) Double-stranded DNA viruses: 20 families and only five different architectural principles for virion assembly. Curr. Opin. Virol. 1, 118–124 38 Abrescia, N.G. et al. (2012) Structure unifies the viral universe. Annu. Rev. Biochem. 81, 795–822 39 Benson, S.D. et al. (2004) Does common architecture reveal a viral lineage spanning all three domains of life? Mol. Cell 16, 673–685 40 Krupovic, M. and Bamford, D.H. (2008) Virus evolution: how far does the double beta-barrel viral lineage extend? Nat. Rev. Microbiol. 6, 941–948 41 File´e, J. (2013) Route of NCLDV evolution: the genomic accordion. Curr. Opin. Virol. 3, 595–599 42 Yutin, N. and Koonin, E.V. (2013) Pandoraviruses are highly derived phycodnaviruses. Biol. Direct 8, 25 43 Raoult, D. and Forterre, P. (2008) Redefining viruses: lessons from Mimivirus. Nat. Rev. Microbiol. 6, 315–319
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44 Forterre, P. (2009) Evolution, viral. In The Encyclopedia of Microbiology (3rd edn) (Schaechter, M., ed.), pp. 370–389, Elsevier 45 Krupovic, M. and Bamford, D.H. (2010) Order to the viral universe. J. Virol. 84, 12476–12479 46 Koonin, E.V. and Dolja, V.V. (2013) A virocentric perspective on the evolution of life. Curr. Opin. Virol. 3, 546–557 47 Koonin, E.V. and Dolja, V.V. (2014) Virus world as an evolutionary network of viruses and capsidless selfish elements. Microbiol. Mol. Biol. Rev. 78, 278–303 48 Diemer, G.S. and Stedman, K.M. (2012) A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses. Biol. Direct 7, 13 49 Roux, S. et al. (2013) Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses. Nat. Commun. 4, 2700 50 Krupovic, M. et al. (2014) Unification of the globally distributed spindle-shaped viruses of the Archaea. J. Virol. 88, 2354–2358 51 Prangishvili, D. and Krupovic, M. (2012) A new proposed taxon for double-stranded DNA viruses, the order ‘Ligamenvirales’. Arch. Virol. 157, 791–795 52 Krupovic, M. and Koonin, E.V. (2014) Evolution of eukaryotic singlestranded DNA viruses of the Bidnaviridae family from genes of four other groups of widely different viruses. Sci. Rep. 4, 5347 53 Krupovic, M. et al. (2011) Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol. Mol. Biol. Rev. 75, 610–635 54 Bahar, M.W. et al. (2011) Insights into the evolution of a complex virus from the crystal structure of vaccinia virus D13. Structure 19, 1011– 1020 55 Forterre, P. and Krupovic, M. (2012) The origin of virions and virocells: the Escape hypothesis revisited. In Viruses: Essential Agents of Life (Witzany, G., ed.), pp. 43–60, Springer 56 Sapp, J. and Fox, G.E. (2013) The singular quest for a universal tree of life. Microbiol. Mol. Biol. Rev. 77, 541–550 57 Brussow, H. (2009) The not so universal tree of life or the place of viruses in the living world. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 364, 2263–2274 58 Forterre, P. and Prangishvili, D. (2009) The great billion-year war between ribosome- and capsid-encoding organisms (cells and viruses) as the major source of evolutionary novelties. Ann. N. Y. Acad. Sci. 1178, 65–77 59 Forterre, P. and Prangishvili, D. (2013) The major role of viruses in cellular evolution: facts and hypotheses. Curr. Opin. Virol. 3, 558–565 60 Pina, M. et al. (2011) The archeoviruses. FEMS Microbiol. Rev. 35, 1035–1054
5
Opinion
Cellular domains and viral lineages Patrick Forterre1,2, Mart Krupovic1, and David Prangishvili1 1
Institut Pasteur, 25 rue du Dr Roux, 75015, Paris, France Institut de Ge´ne´tique et Microbiologie, University Paris-Sud, Centre National de la Recherche Scientifique (CNRS) UMR 8621, 91405 Orsay CEDEX, France
2
It has been claimed that giant DNA viruses represent a separate, fourth domain of life in addition to the domains of Bacteria, Archaea, and Eukarya. Such classification disregards fundamental differences between the two types of living entities – viruses and cells – and results in confusion and controversies in evolutionary scenarios. We highlight these problems and emphasize the importance of restricting the term ‘domain’ to the descendants of the last universal cellular ancestor (LUCA), based on the shared ribosome structure. We suggest tracing phylogeny of viruses along evolutionary lineages primarily defined by virion architectures and the structures of the major capsid proteins. Domains of life More than two decades ago Woese, Kandler, and Wheelis proposed the term ‘domain’ for the three evolutionary cellular lineages identified by 16/18S rRNA comparison: Archaea, Bacteria, and Eukarya [1]. This tripartite division has been validated by comparative genomics, although the tree of life topology is still debated [2–4]. However, in recent years, the notion of a ‘fourth domain’ has made its way into scientific literature [5–10]. Didier Raoult and coworkers have argued that giant DNA viruses of the proposed order Megavirales [11] (formerly nucleocytoplasmic large DNA viruses, NCLDV) represent a fourth domain of life [9] because their genomes encode some universal proteins, such as RNA polymerases, that in some phylogenetic analyses form a fourth monophyletic group in addition to the domains of Bacteria, Archaea, and Eukarya [5,6,11,12]. The term ‘fourth domain’ can imply either that Megavirales universal proteins originated from a fourth cellular lineage descending from the LUCA – that is now extinct but passed its genes to the ancestor of Megavirales – or that this ancient cellular lineage was itself transformed into the ancestor of the Megavirales. The term ‘fourth domain’ is now often used in the scientific literature [7,13,14], although the four-domain hypothesis itself is controversial. Notably, recent discussions in review papers in Nature and Science led to contradictory statements [8,10]. For example, it has been claimed that more than four domains of life possibly exist [8] or, on the contrary, that the ‘domain of life is an archaic Corresponding author: Forterre, P. ([email protected]). Keywords: viruses; phylogeny; evolution; tree of life; mimivirus. 0966-842X/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tim.2014.07.004
concept’ [8]. Indeed, the ‘viral’ domain hypothesis opens a Pandora box because it is unclear how many viral domains should be considered. Notably, some large DNA viruses, such as members of the families Baculoviridae and Nudiviridae, encode RNA polymerases that are extremely divergent from their homologs in the genomes of cellular organisms and viruses of the Megavirales, sharing no detectable sequence similarity at the amino acid level [15,16]. These viruses are therefore good candidates for additional domains (Figure 1A). Moreover, the question arises of whether, besides large DNA viruses, additional viral domain(s) should be introduced for classification of small DNA viruses, or even RNA viruses. It may be tempting to separate large (giant) and small viruses and restrict the term ‘domain’ to the giant ones. However, this is clearly unjustified because there is a continuum of genome sizes in the viral world, and any threshold between small and large viruses seems arbitrary: the genome sizes of viruses of the Megavirales (including pandoraviruses [17], see below) overlap with those of members of the families Baculoviridae and Nimaviridae, and of the order Caudovirales (Figure 1B). Finally, consideration of double-stranded DNA (dsDNA) viruses separately from the rest of the virosphere appears to be artificial because some groups of dsDNA viruses are clearly related to single-stranded DNA (ssDNA) viruses, and even to RNA viruses, and should be considered in the framework of an evolutionary continuum [18,19]. As expected, the four-domain hypothesis has been hotly debated and criticized [20–24]. The notion that viruses could form domains of life was first rejected by scientists who argued that viruses are not living, for example because they lack integrated metabolic activity and the ability to capture and store free energy [23]. The four-domain hypothesis has also been refuted on methodological grounds by some authors who revisited the phylogenies of universal proteins from viruses of the order Megavirales. They concluded that these proteins were in fact derived from eukaryotes because they sometimes branch within eukaryotic sequences in their phylogenetic analyses [20–22,24]. However, these criticisms are themselves controversial. On theoretical grounds, the nature of viruses, living or not, is a matter of debate. For instance, one of us proposed that viruses may be considered as living organisms once they have redirected the metabolism of the infected cell (the virocell) for their own purposes ([25] and references therein). Considering viruses as non-living biological entities usually pairs with underestimating their role in the evolution of life [23]. By contrast, regarding viruses as Trends in Microbiology xx (2014) 1–5
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Schemac of evoluonary relaonships between DNA-dependent RNA polymerases
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Figure 1. (A) Schematic evolutionary relationships between viral (red) and cellular (blue) DNA-dependent RNA polymerases. The baculovirus RNA polymerase is very divergent and cannot be aligned with the other RNA polymerases (indicated by a broken line). However, its size and conserved active site residues [16] suggest homology to cellular polymerases. (B) Range of genome sizes for different groups of viruses with double-stranded DNA genomes. Pandoravirus genomes have been grouped with the proposed order Megavirales, according to [42], although final classification awaits further analyses of proteins involved in virion formation.
living emphasizes their major contribution to the evolution of cellular organisms, placing viruses and cells on the same footing. In fact, the definition of a living organism is not as trivial as it could seem a priori. For example, there is an evolutionary continuum between ‘living’ bacteria, on the one hand, and mitochondria and hydrogenosomes, two biological ‘non-living’ entities, on the other. In any case, if viruses are considered by some to be living, it becomes a priori reasonable to ask the question of their place, possibly as new domain(s), in the tree of life. On methodological grounds, the phylogenetic analyses used to dismiss the four-domain hypothesis as well as their interpretation can be disputed. Phylogenies of megaviral proteins with eukaryotic affinity are often ambiguous and can be interpreted differently depending on the evolutionary scenario favored by the authors [26]. In some cases, eukaryotic proteins that branch with megaviral proteins in phylogenetic trees could have been transferred from megaviruses to eukaryotic cells, confusing the picture. Indeed, ancient transfers from Megavirales to eukaryotes (or protoeukaryotes) cannot be excluded because Megavirales can integrate their genomes into the genomes of their hosts [27–29]. In many cases, eukaryotes branch within clades corresponding to members of the Megavirales, supporting the idea that several important eukaryotic informational proteins were recruited from the giant viruses [30–32]. Moreover, universal proteins encoded by viruses belonging to various families of the Megavirales are often very divergent [28,30,32]; this muddles the picture even further in phylogenetic analyses and could suggest the existence of more than four domains if virus classification into domains is based on these proteins. Finally, the term ‘fourth domain’ 2
is difficult to accommodate in the scenarios in which informational proteins working with DNA, including those encoded by members of the Megavirales, originated in an ancient viral world and were later recruited by cellular organisms [33]. Under such a scenario the last common ancestors of these proteins might not have been present in LUCA but in ancient viral ancestors, whereas the hallmark of the three domains is their common descent from LUCA. Thus, the arguments used pro and con for the fourdomain hypothesis are often based on controversial interpretations, and this debate could remain undecided for a long time. In the meantime, much confusion may be created in the scientific and public debate concerning the nature and origin of viruses, and the concept of the domain [8,9]. However, in our opinion, besides the problems already mentioned (such as how many viral domains there are and whether RNA viruses are also eligible for forming additional domains) the four-domain hypothesis raises a major concern that we would like to discuss here. We also take this opportunity to revisit the domain definition itself, the major legacy of the late Carl Woese to biology [34]. Our goal is to help to define terminology, which would be based on solid ground and would be acceptable to scientists with different views on viruses. Domains do not apply to viruses In our opinion, the concept of domain applied to viruses is inappropriate because it blurs the gap between viruses and the rest of the biosphere, weakening the uniqueness and originality of viruses. The idea to conflate viruses and cells may appear tempting as a way to unify the entire biosphere. This idea has been promoted, for instance, by authors who have suggested that giant viruses originated
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Opinion via regressive evolution from extinct cellular domains [7,35]. Hence, in a recent review, Claverie and Abergel argue that: ‘the discovery of increasingly reduced parasitic cellular organisms and that of giant viruses exhibiting a widening array of cellular-like functions may ultimately abolish the historical discontinuity between the viral and the cellular world’ [36]. However, the regressive hypothesis for the origin of giant viruses is far from proven. Giant members of the Megavirales are not only evolutionarily related to much smaller viruses of the Megavirales (e.g., poxviruses) but also (via their major capsid proteins and packaging ATPases) to small DNA viruses infecting Archaea and Bacteria [37–40]. For some authors this suggests that giant viruses of the Megavirales did not derive from an extinct fourth domain of life but instead evolved from smaller viruses by genome expansions [26,40,41]. A recent analysis suggests, for instance, that giant pandoraviruses do not represent a new domain but are evolutionarily related to algae-infecting viruses of the family Phycodnaviridae (one of the families within the Megavirales), implying that giant viruses originated independently at least twice in the Megavirales order [42]. Comparative genomic analyses suggest that members of the Megavirales evolved by successive steps of genome expansions and reduction (genomic accordion) [41]. In any case, even if giant viruses have originated from extinct cellular domains (something we do not believe in), they would be now completely different organisms compared to their cellular ancestors. The discontinuity between the viral and cellular worlds is not a convention of biologists biased by the history of virus discovery, but is a reflection of the existence of two very different types of biological organisms in the biosphere. Whereas cellular organisms (Archaea, Bacteria, and Eukarya) reproduce by cell division (as well as a step of cell fusion in the case of sexual eukaryotes), viruses reproduce by producing virions, a completely different mode of genome dissemination. Moreover, viruses and cells clearly have very distinct, even if intertwined, evolutionary histories. Archaea, bacteria, and eukaryotes encode the ribosome, allowing them to synthesize their proteins and to live either as free-living organisms or as parasites of other organisms. By contrast, because viruses lack the protein synthesis machinery they can only propagate their genetic information as parasites of organisms encoding ribosomes: members of the domains Archaea, Bacteria, or Eukarya. This distinction still holds, even after the discovery of the pandoraviruses, because their megagenomes (for the two described species) do not encode any ribosomal protein or ribosomal RNA (rRNA). By contrast, all cellular organisms, with the exception of some reduced intracellular bacteria en route to becoming organelles, encode a complete set of ribosomal proteins and rRNA-encoding genes. To emphasize these distinctions, viruses have been defined by Raoult and Forterre as capsid-encoding organisms, as opposed to ribosome-encoding organisms [43]. The capsid indeed can be considered as the hallmark of the virus to prevent confusion between viruses and other types of biological entity such as plasmids or infectious RNA [44,45]. These parasitic elements (orphan replicons sensu Raoult and Forterre [43]) are evolutionarily related to
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viruses [45] and, as suggested by Koonin and Dolja, can be viewed as members of a ‘greater viral world’ characterized by parasitism and shared information [46,47]. However, they should not be confused with bona fide viruses because they do not rely on the production of virions to propagate their genetic information. To be consistent with the definition of viruses and cells based on capsids and ribosomes, respectively, we find it important to restrict the term domain to ribosome-encoding organisms. This opinion is based on the fact that archaea, bacteria, and eukaryotes are classified according to their evolutionary relationships based on properties of rRNA. By contrast, viruses can be grouped into lineages, based on the evolutionary trajectories of the virions and their production mechanisms. Analysis of major capsid proteins is one way to follow these trajectories. This is not always an easy task because these trajectories can be complex, involving possible recombination of gene cassettes encoding structural components with those encoding replication proteins [48,49]. Nevertheless, two major lineages of dsDNA viruses have been already successfully defined based on the structures of the major capsid proteins and genome-packaging ATPases [37–40]. Members of the Megavirales belong to one of them, the so-called PRD1like lineage. This lineage encompasses archaeal, bacterial, and eukaryotic viruses whose major capsid proteins adopt the double-jelly roll fold and whose genome-packaging machineries are based on homologous ATPases of the FtsK/HerA superfamily. The other major lineage, the socalled HK97-like lineage, groups archaeal and bacterial members of the Caudovirales with eukaryotic members of the order Herpesvirales whose major capsid proteins adopt the HK97 fold and whose genome-packaging machineries are based on homologous ATPases, different from those operating in viruses of the PRD1-like lineage. Evolutionary lineages based on major capsid proteins have been also used to define three major groups of archaeal dsDNA viruses, the order Ligamenvirales, and the families Bicaudaviridae and Fuselloviridae [50,51]. Finally, major evolutionary lineages based on virion architecture have been also proposed for RNA viruses [38]. However, it should be emphasized that, owing to pervasive recombination between viruses belonging to widely different groups [32,41,52,53], a classification based on a single virusencoded component, however important for virus propagation this component may be, will not necessarily faithfully reflect the complete evolutionary history of a viral group. For instance, in the case of capsid-based classification, one can expect that in the course of evolution of viruses with complex virions a particular capsid protein might be lost or exchanged for a different one. Indeed, the recently described pandoravirus lacks the major capsid protein typical of the PRD1-like lineage [17], although some of its replication proteins linked this virus to other members of the Megavirales [42]. Considering the huge complexity of the Pandoravirus virion, it is possible that the lacking protein became dispensable in this particular family of the Megavirales. Indeed, although a homolog of the double jelly-roll major capsid protein is still present in poxviruses, its function in virion assembly and architecture has been considerably modified [54]. Alternatively, it is possible that 3
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Opinion the Pandoravirus represents an independent evolutionary lineage which acquired specific genes from members of the Megavirales. More information is clearly necessary to determine to what extent the evolutionary trajectories of the Pandoravirus and the Megavirales overlap. Finally, whereas knowledge of virion architecture is essential for defining the major evolutionary lineages of viruses, information regarding other components that are important for virus replication and dissemination should also be taken into account. The classification of ribosome-encoding organisms into domains, and virion-producing organisms into evolutionary lineages, has several advantages. In both cases we have a natural classification based on the evolution of the hallmarks of the organism, the ribosome and virion, respectively. Besides rectifying the confusion between the two types of organisms, such classification avoids giving similar names to evolutionary lineages with very different histories. The three cellular domains are monophyletic, with all members of these domains being ultimately descendants of LUCA. The existence of such an ancestor is a logical consequence of the binary mechanism of cell division: the coalescence of all modern lineages when going back in time for each of them from daughter cells to mother cells, and so forth. By contrast, viruses are polyphyletic. Indeed, protein components defining major viral lineages, such as PRD1-like and HK97-like, are not homologous, indicating independent origins [37,38]. In fact, the mode of genome dissemination typical of viruses, in other words, the production of virions, most likely originated several times independently at an early stage of evolution, and after the emergence of ribosome-encoded proteins (by definition), but before the time of LUCA [55]. Importantly, the definition of viruses as capsid- or more precisely virion-encoding organisms, and of archaea, bacteria, and eukarya as ribosome-encoding organisms, is operational in our time of metagenomic analyses. When a large genome is sequenced and assembled from metagenomic data, the absence of ribosomal proteins- and rRNA-encoding genes immediately suggests that such genome does not correspond to a novel domain of life but instead to a viral genome (or to a megaplasmid). The presence of a gene encoding a recognizable capsid protein will indicate that we are dealing with a viral genome, allowing assignment of the genome to a particular viral lineage. Concluding remarks and future directions In conclusion, the major differences between viruses and cells strongly call for restricting the term domain to the descendants of LUCA, based on their ribosome structure, in agreement with its historical definition [1]. We therefore think that the concept of domain is far from being archaic, but on the contrary is still valid and remains a major legacy of the late Carl Woese to biology [34,56]. Finally, where should we place viral lineages in the tree of life describing the evolutionary relationships between the three cellular domains? Viruses are both major quantitative components of the biosphere and major growth factors for cellular evolution [57–59]. Thus, viruses are an essential part of the living world and should be, one way or 4
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the other, integrated in a metaphoric tree of life. Exploration of the viral world has revealed that many lineages of viruses indeed co-evolved with their hosts within each cellular domain, producing three ‘viral spaces’ that overlap with the three cellular domains [60]. Viruses are therefore here, there, and everywhere; the tree of life being infected by viruses from the roots to the leaves. In other words, denying domain status to viruses does not diminish their importance in the evolution of life. References 1 Woese, C.R. et al. (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. U.S.A. 87, 4576–4579 2 Forterre, P. (2013) The common ancestor of archaea and eukarya was not an archaeon. Archaea 2013, 372396 3 Gribaldo, S. et al. (2010) The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat. Rev. Microbiol. 8, 743–752 4 Williams, T.A. et al. (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504, 231–236 5 Boyer, M. et al. (2010) Phylogenetic and phyletic studies of informational genes in genomes highlight existence of a 4 domain of life including giant viruses. PLoS ONE 5, e15530 6 Colson, P. et al. (2011) The giant Cafeteria roenbergensis virus that infects a widespread marine phagocytic protist is a new member of the fourth domain of life. PLoS ONE 6, e18935 7 Legendre, M. et al. (2012) Genomics of Megavirus and the elusive fourth domain of Life. Commun. Integr. Biol. 5, 102–106 8 Pennisi, E. (2013) Ever-bigger viruses shake tree of life. Science 341, 226–227 9 Raoult, D. et al. (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306, 1344–1350 10 Zakaib, G.D. (2011) The challenge of microbial diversity: out on a limb. Nature 476, 20–21 11 Colson, P. et al. (2013) ‘Megavirales’, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch. Virol. 158, 2517–2521 12 Sharma, V. et al. (2014) DNA-dependent RNA polymerase detects hidden giant viruses in published databanks. Genome Biol. Evol. 6, 1603–1610 13 Yutin, N. et al. (2013) Mimiviridae: clusters of orthologous genes, reconstruction of gene repertoire evolution and proposed expansion of the giant virus family. Virol. J. 10, 106 14 Wu, D. et al. (2011) Stalking the fourth domain in metagenomic data: searching for, discovering, and interpreting novel, deep branches in marker gene phylogenetic trees. PLoS ONE 6, e18011 15 Passarelli, A.L. and Guarino, L.A. (2007) Baculovirus late and very late gene regulation. Curr. Drug Targets 8, 1103–1115 16 Ruprich-Robert, G. and Thuriaux, P. (2010) Non-canonical DNA transcription enzymes and the conservation of two-barrel RNA polymerases. Nucleic Acids Res. 38, 4559–4569 17 Philippe, N. et al. (2013) Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341, 281–286 18 Krupovic, M. (2013) Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr. Opin. Virol. 3, 578–586 19 Roine, E. et al. (2010) New, closely related haloarchaeal viral elements with different nucleic acid types. J. Virol. 84, 3682–3689 20 Lopez-Garcia, P. and Moreira, D. (2009) Yet viruses cannot be included in the tree of life. Nat. Rev. Microbiol. 7, 615–617 21 Moreira, D. and Brochier-Armanet, C. (2008) Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol. Biol. 8, 12 22 Moreira, D. and Lopez-Garcia, P. (2005) Comment on ‘The 1.2megabase genome sequence of Mimivirus’. Science 308, 1114 23 Moreira, D. and Lopez-Garcia, P. (2009) Ten reasons to exclude viruses from the tree of life. Nat. Rev. Microbiol. 7, 306–311 24 Williams, T.A. et al. (2011) Informational gene phylogenies do not support a fourth domain of life for nucleocytoplasmic large DNA viruses. PLoS ONE 6, e21080
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