Ann. N.Y. Acad. Sci. ISSN 0077-8923
A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S Issue: DNA Habitats and Their RNA Inhabitants
Archaeal viruses: living fossils of the ancient virosphere? David Prangishvili Department of Microbiology, Institut Pasteur, Paris, France Address for correspondence: David Prangishvili, Department of Microbiology, Institut Pasteur, 25. Rue du Dr. Roux, Paris 75015, France. [email protected]
Studies on viruses parasitizing archaea reveal their specific nature and complete the tripartite division of the biosphere, indicating that each of the three domains of life—Archaea, Bacteria, and Eukarya—has its own set of associated DNA viruses. I argue that the remarkable morphotypical diversity of archaea-specific viruses could have originated from diverse viral archetypes that predated the divergence of the three domains of cellular life. It is possible that the descendants of many of these viral archetypes are able to parasitize extant archaea owing to their ability to evade archaea-specific defenses against virus infection, specifically the defenses linked to the evolution of cell envelope structure. Keywords: virus; archaea; domains of life; virus origin; virus evolution
Introduction The evolutionary history of the living world—since the development of molecular phylogeny in the second part of the last century—is mainly inferred from comparison of marker genes from different organisms. The most spectacular result of this approach was based on the comparative sequence analysis of universally conserved marker genes—ribosomal RNA genes—that “revealed that living systems represent one of three aboriginal lines of descent: (i) the eubacteria, . . . ; (ii) the archaebacteria, . . . ; and (iii) the urkaryotes, now represented in the cytoplasmic component of eukaryotic cells.”1 The discovery of the “three lines of the aboriginal descent,” later renamed as Bacteria, Archaea, and Eukarya,2 had a profound impact on the understanding of cellular evolution. The three-branch tree is an essential framework for reconstructing cellular evolution and the features of ancestral life forms, which predated the divergence between the ancestors of the three domains, the Bacteria, Archaea, and Eukarya, about 3.5 Ga. Molecular phylogeny is less efficient for studies on virus evolution. First, genomic similarity may not provide an optimal measure of viral phylogeny because of extensive exchange of genes between viruses, between viruses and plasmids, and between
viruses and host cells, confusing the gene origin and mixing up horizontal and vertical inheritance. Second, as there are no universal genes shared by all viruses, molecular phylogeny would be inapplicable for the measurement of large evolutionary distances and the assignment of viruses to higher-order taxa. In fact, the only feature that can be considered as a universal marker for all viruses appears to be the virus capsid—the virion. Consequently, is has been argued that comparison of virion architectures and/or the structures of virion proteins of different viruses could be an appropriate approach for the phylogenetic classification of viruses.3–5 Below, I will briefly summarize the knowledge on the morphological characteristics of viruses parasitizing archaea and attempt to infer what we have learned about the evolution of the viral world from the studies on archaeal viruses and their comparison with viruses from the other two domains. Morphotypes of archaeal viruses Viruses that parasitize archaea have been isolated nearly exclusively from two types of aquatic systems: extreme geothermal environments with temperatures exceeding 80°C and high-saline waters with nearly saturating concentrations of sodium chloride. The number of described species, all carrying
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DNA genomes, single stranded (ss) or double stranded (ds), represents only a small percentage, hardly more than 1%, of known viruses from the two other domains, Bacteria and Eukarya. However, even this limited number of species reveals a remarkable—unprecedented in other domains— diversity of virion morphotypes (for recent reviews, see Refs. 6–8). The morphological landscape of archaeal viruses comprises a number of virus types never observed among viruses from the other two domains. These include viruses with particles resembling bottles (family Ampullaviridae),9 spindles—tail-less, tailed, and two-tailed (families Fuselloviridae and Bicaudaviridae),10 droplets (family Guttaviridae),11,12 and spirals (family Spiraviridae).13 Also specific to archaea are viruses with unique combinations of dsDNA genomes with virions of linear (families Rudiviridae and Lipothrixviridae from the order Ligamenvirales),14 bacilliform (family Clavaviridae),15 and spherical (family Globuloviridae)16 shape. In addition to these archaea-specific viruses, archaea replicate all types of dsDNA viruses known to infect bacteria, including head-tailed viruses (families Myoviridae, Siphoviridae, and Podoviridae from the order Caudovirales),17 icosahedral viruses with internal lipid envelopes (families Sphaerolipoviridae and Turriviridae in archaea; Tectiviridae and Corticoviridae in bacteria),8–18 and pleomorphic viruses (families Pleolipoviridae in archaea and Plasmaviridae in bacteria).19,20 There are reasons to believe that the bewildering morphotypical diversity of known archaeal viruses, far exceeding (and including) that of bacterial viruses, represents only the tip of an iceberg. Observations of virus-like particles in natural habitats where archaea dominate are consistent with this suggestion.21–25 Moreover, the number of archaeal virus morphotypes constantly expands with the exploration of new hosts and new habitats. By contrast, no new morphotype of bacterial virus has been found since the 1970s, despite isolation of thousands of new species.26 Virion morphogenesis and constituents of archaeal viruses The archaeal viruses with morphotypes similar to those of bacterial viruses (e.g., head-tailed and icosahedral viruses) apparently follow the same prin36
ciples of virion morphogenesis as their bacterial counterparts:27 DsDNA is packaged into a preformed capsid as a tightly wound spool, with help from a nucleoside triphosphate–dependent molecular motor.28 Moreover, the major capsid proteins (MCPs) of some archaeal and bacterial viruses are highly similar in structure, carrying Hong-Kong 79 (HK79)-like fold (head-tailed viruses) or double jelly-roll fold (icosahedral viruses with internal lipid layer).29,30 The archaeal viruses with archaea-specific virion types seem to exploit particular pathways of virion assembly, different from the translocation of the genome into the preformed capsid. For several of these viruses, distinct steps of virion morphogenesis could be postulated based on electron microscopy (EM) examination of virions in native and partially disintegrated states (Fig. 1). An essential step in virion morphogenesis appears to be the formation of a nucleoprotein filament by the interaction of DNA with multiple copies of virusencoded DNA-binding MCPs; for members of the Ampullaviridae, Spiraviridae, Bicaudaviridae, Rudiviridae, Lipothrixviridae, and Globuloviridae, the existence of such nucleoprotein filaments has been documented by EM observations (Fig. 1). Depending on the properties of the MCPs, the nucleoprotein is condensed into virion cores of different shapes, which often determine the virion morphotype. A good example showing that the manner of nucleoprotein organization shapes the virion morphotype is provided by the Ampullaviridae.9 In their virions, the dsDNA-containing nucleoprotein is folded into an unusual cone-shaped core that, after being encased in the lipid-containing envelope, determines the exceptional bottle-shaped morphotype of the mature virion (Fig. 1). Behind the exceptional coil shape of the Spiraviridae virions is another special manner of nucleoprotein organization.13 The circular nucleoprotein, formed by ssDNA and MCP copies, is folded into a structure with two levels of helical organization: the two halves of the circular nucleoprotein intertwine with each other and form a rope-like fiber, which is condensed into the helical coil spring of the virus particle (Fig. 1). The spherical and spindle-like shapes of the Globuloviridae and Bicaudaviridae virions, respectively, are likely also coupled with unusual mechanisms of condensation of their dsDNA-containing nucleoproteins.
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Figure 1. Virions of six families of archaeal viruses in native and partially degraded states (transmission and cryo-electron micrographs). For all virions, the DNA–protein filament represents a basic structural element and is highlighted by black arrows. For the Ampullaviridae and Spiraviridae, nucleoprotein organization in the native virion is schematically illustrated. Two forms of the Bicaudaviridae virion are shown, (I) immature and (M) mature two-tailed; in inset: horizontal slice through the threedimensional reconstruction of part of the mature virion. The virion of the Lipothrixviridae is shown in two states: (N) native and (Δ env) devoid of the lipid-containing envelope. The structures of the MCP of the rudivirus SIRV and two MCPs of the lipothrixvirus AFV1 are colored using a rainbow color gradient from the N-terminus (blue) to the C-terminus (red). Adapted from Refs. 9, 13, 16, 23, 34, and 47.
The manner of folding of nucleoprotein filaments in archaea-specific viruses, as mentioned earlier, is apparently controlled by the physicochemical properties of their MCPs. The MCP structures have only been resolved for members of the families Rudiviridae, Lipothrixviridae, and Bicaudaviridae.31–33 They all carry unique four-helix-bundle folds, which are highly similar for Rudiviridae and Lipothrixviridae, but different for Bicaudaviridae. The wrapping of similar MCPs of Rudiviridae and Lipothrixviridae around linear dsDNA forms helical nucleoprotein filaments of similar structure, as observed by cryoEM (Fig. 1). In the linear virions of Lipothrixviridae, the helical nucleoprotein is encased in a lipidcontaining envelope, whereas in virions of the Rudiviridae it remains nonenveloped (Fig. 1).
The role of the four-helix-bundle MCP of the Bicaudaviridae in virion morphogenesis is unknown. The spindle-shaped virion extruded from the host cell undergoes extensive changes in the course of its extracellular maturation, leading to the formation of helical appendages at both pointed ends of the immature virion.34 Observation of a nucleoprotein filament inside these appendages (Fig. 1) indicates its release, during virion maturation, from the condensed state it has in the spindleshaped virion. Polyphyletic origin of archaeal viruses from primordial ancestors The morphological distinctiveness of archaeal viruses extends to the genetic information that they
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carry and the structures of the proteins that they encode: the vast majority of their genes do not resemble any gene in the extant databases in terms of sequence,35,36 and many encode proteins that carry unusual folds.29,37 Moreover, for some cases it was shown that proteins without known homologues encode peculiar features of the infection cycle, specifically those of virion egress, not encountered in viruses of bacteria and eukaryotes.38 The available information leads to the notion that viruses that parasitize archaea form a special group in the viral world and, thus, each of the three domains of life has its own set of associated DNA viruses. Despite the pronounced differences, some members of the distinct, domain-specific groups of viruses share a few genes. For example, homologous genes encoding protein-primed DNA polymerases and replication-initiator Rep proteins have been identified in virus species from all three domains (for review, see Ref. 7). These virus species are extremely diverse in their morphotypes and genomic properties, and the occurrence of homologous genes in them could hardly be owing to close evolutionary relationships. Neither is horizontal gene transfer a probable explanation, given the large evolutionary distances between their hosts and the low probability of cross-domain spreading. The incidence of virus-specific genes that encode homologous proteins in viral species from the three domains of life is most consistent with the acquisition of these genes directly from an ancestral pool of viral genes that predated the divergence of the three domains of life, in the times of the last universal common ancestor of cellular organisms (LUCA). The notion of an ancestral pool of viral genes is consistent with the existence of viral lineages— a group of viruses with structurally similar virions and MCPs—that span all three domains of cellular life and originate from an ancestor parasitizing on the LUCA.3,4 Two such structure-based lineages of dsDNA viruses have now been defined.39 One comprises icosahedral viruses with MCPs carrying the double jelly-roll fold: archaeal Turriviridae, bacterial Tectiviridae and Corticoviridae, and eukaryal Adenoviridae and the “Megavirales.” Another includes bacterial and archaeal head-tailed viruses (Caudovirales) and eukaryal Herpesvirales, which carry MCPs with the HK97-like fold. Thus, it appears that in the time of the LUCA, at least two ancestral morphotypes—archetypes—of icosahedral viruses 38
existed, one that gave rise to the extant viruses with the double jelly-roll MCP and another that generated the viruses with the HK97 type of MCP. If ancestors of the icosahedral viruses were present in the times of the LUCA, it is reasonable to suggest that the diverse morphotypes of archaeal DNA viruses may have also had their origins in the archetypes present in the ancient virosphere,40 predating the divergence of the three cellular domains.7,41 Although possible, it is highly improbable that these viruses, with diverse architectural principles and assembly pathways of their virions, appeared specifically in extreme environmental conditions later in the evolution of the biosphere. The primordial existence of archetypes of extant archaeal viruses with fundamentally different solutions for packaging and protection of genomic material depicts the ancient virosphere as a kind of laboratory for structural and functional designs of virus particles. In this laboratory, the viral lifestyle seems to have been developed,42 and multiple efficient ways were explored for the packaging and delivery of viral genomes, using different proteins for these functions. Moreover, such a scenario implies that there must have been a certain predisposition in the biosphere for the development of the viral lifestyle, and it was not a rare or accidental event. The specific nature of the archaeal virosphere is linked with the envelope composition of host cells The origin of the differences between the virus types parasitizing archaea and those parasitizing bacteria—the former including all bacterial types— is unclear. Recently, I suggested that these differences are linked to different strategies developed in the two domains against virus infection and that these strategies concerned modifications of the cell envelope: the bacterial strategy involved increasing the complexity of the cell wall—by introduction of peptidoglycan, outer membrane, capsule, and so on—while the archaeal solution mainly involved chemical modification of the cell surface.7 Indeed, the cell wall of bacteria is much more complex in its organization compared to the cell envelope of archaea, the sole constituent of which, in many cases (specifically in hyperthermophiles—the hosts for the majority of archaeal viral morphotypes), is an S-layer, a paracrystalline protein layer that presumably is the earliest cell wall structure to have
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evolved.43 On the other hand, archaea, with their relatively simple cell envelope, have all the surfaceexposed proteins modified; the most common is N-glycosylation of S-layer proteins, a modification rarely observed in bacteria.43 Seeing the interplay between viruses and their hosts as the driving force for the emergence of extant cell envelopes of Bacteria and Archaea is in line with the hypothesis, proposed by Patrick Forterre and me, that states that the arms race between viruses and cells was the driving force behind major evolutionary novelties in the biosphere.44,45 Under the proposed scenario, the majority of ancestral virus types do not parasitize bacteria because the latter have developed a complex cell wall structure, through which only very few virus types can channel their genomic material.7 However, chemical modification of the cell surface, the strategy preferred by archaea, is apparently less restrictive, and many ancestral virus types could develop mechanisms allowing them to evade it and remain associated with archaeal hosts.7 With extremely scarce available information on the entry process of archaeal viruses,46 it is impossible to provide support for the proposed scenario. The merit of the presented attempts to rationalize the data on the morphological peculiarities of archaeal viruses, especially for the purpose of reconstructing evolutionary scenarios, is significantly constrained by our limited knowledge on the subject. Only rudimentary information is available on the structure of virions and MCPs of known archaeal virus species. Moreover, we are a long way from a full comprehension of the global viral diversity—much more remains to be known on viral diversity in different environments and in a broader range of host taxa. These are now the lines of research that promise to provide critical insights into the evolutionary history of viruses and their interactions with host cells. Acknowledgment I gratefully acknowledge the support of l’Agence Nationale de la Recherche, and stimulating discussion with Patrick Forterre and Mart Krupovic, and their critical comments on the manuscript. Conflicts of interest The author declares no conflicts of interest.
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References 1. Woese, C.R. & G.E. Fox. 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. U.S.A. 74: 5088–5090. 2. Woese, C.R., O. Kandler & M.L. Wheelis. 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. 3. Bamford, D.H. 2003. Do viruses form lineages across different domains of life? Res. Microbiol. 154: 231–236. 4. Krupovic, M. & D.H. Bamford. 2010. Order to the viral universe. J. Virol. 84:12476–12479. 5. Forterre, P., M. Krupovic & D. Prangishvili. 2014. Cellular domains and viral lineages. Trends Microbiol. 22:554– 558. 6. Pina, M., A. Bize, P. Forterre & D. Prangishvili. 2011. The Archeoviruses. FEMS Microbiol. Rev. 35: 1035–1054. 7. Prangishvili, D. 2013. The wonderful world of archaeal viruses. Ann. Rev. Microbiol. 67: 565–585. 8. Pietil¨a, M.K., T. A. Demina, N. S. Atanasova, et al. 2014. Archaeal viruses and bacteriophages: comparisons and contrasts. Trends Microbiol. 22:334–344. 9. H¨aring, M., R. Rachel, X. Peng, et al. 2005. Diverse viruses in hot springs of Pozzuoli, Italy, including a unique bottle-shaped archaeal virus ABV from a new family, the Ampullaviridae. J. Virol. 147: 2419–2429. 10. Krupovic, M., E.R.J. Quemin, D.H. Bamford, et al. 2013. Unification of the globally-distributed spindle-shaped viruses of Archaea. J. Virol. 88: 2354–2358. 11. Arnold, H.P., U. Ziese & W. Zillig. 2000. SNDV, a novel virus of the extremely thermophilic and acidophilic archaeon Sulfolobus. Virology 272: 409–416. 12. Mochizuki, T., Y. Sako & D. Prangishvili. 2011. Provirus induction in hyperthermophilic archaea: characterization of Aeropyrum pernix spindle-shaped virus 1 and Aeropyrum pernix ovoid virus 1. J. Bacteriol. 193: 5412–5419. 13. Mochizuki, T., M. Krupovic, G. Pehau-Arnaudet, et al. 2012. Archaeal virus with exceptional virion architecture and the largest single-stranded DNA genome. Proc. Natl. Acad. Sci. U. S. A. 109: 13386–13391. 14. Prangishvili, D. & M. Krupovic. 2012. A new proposed taxon for double-stranded DNA viruses, the order “Ligamenvirales”. Arch. Virol. 157: 791–795. 15. Mochizuki, T., T.Yoshida, R. Tanaka, et al. 2010. Diversity of viruses of the hyperthermophilic archaeal genus Aeropyrum, and isolation of the Aeropyrum pernix bacilliform virus 1, APBV1, the first representative of the family “Clavaviridae” Virology 402: 347–354. 16. H¨aring, M., X. Peng, K. Br¨ugger, et al. 2004. Morphology and genome organisation of the virus PSV of the hyperthermophilic archaeal genera Pyrobaculum and Thermoproteus: a novel virus family, the Globuloviridae. Virology 323: 232– 242. 17. Pietil¨a, M K., P. Laurinm¨aki, D.A. Russell, et al. 2013. Insights into head-tailed viruses infecting extremely halophilic archaea. J. Virol. 87: 3248–3260. 18. Pawlowski, A., I. Rissanen, J.K. Bamford, et al. 2014. Gammasphaerolipovirus, a newly proposed bacteriophage genus, unifies viruses of halophilic archaea and thermophilic
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33. Goulet, A., G. Vestergaard, C. Felisberto-Rodrigues, et al. 2010. Getting the best out of long-wavelength X-rays: de novo chlorine/sulfur SAD phasing of a structural protein from ATV. Acta Crystallogr. D. Biol. Crystallogr. 66:304–308. 34. Prangishvili, D., et al. 2006. Structural and genomic properties of the hyperthermophilic archaeal virus ATV with an extracellular stage of the reproductive cycle. J. Mol. Biol. 359: 1203–1216. 35. Prangishvili, D., R.A. Garrett & E.V. Koonin. 2006. Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res. 117: 52–67. 36. Krupovic, M., D. Prangishvili, R. Hendrix & D. Bamford. 2011. Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol. Mol. Biol. Rev. 75: 610–635. 37. Krupovic, M., M.F. White, P. Forterre & D. Prangishvili. 2012. Postcards from the edge: structural genomics of Archaeal viruses. Adv. Virus Res. 2: 51–81. 38. Prangishvili, D. & T. Quax. 2011. Exceptional virion release mechanism: one more surprise from archaeal viruses. Curr. Opin. Microbiol. 14: 315–320. 39. Krupovic, M.& D.H. Bamford. 2011. Double-stranded DNA viruses: 20 families and only five different architectural principles for virion assembly. Curr. Opin. Virol. 1: 118–124. 40. Prangishvili, D. 2003. Evolutionary insights from studies on viruses of hyperthermophilic archaea. Res. Microbiol. 154: 289–294. 41. Prangishvili, D., P. Forterre & R.A. Garrett. 2006. Viruses of the Archaea: a unifying view. Nat. Rev. Microbiol. 4: 837–848. 42. Koonin, E.V. & V.V. Dolja. 2013. A virocentric perspective on the evolution of life. Curr. Opin. Virol. 3: 546–557. 43. Albers, S.V. & B.H. Meyer. 2011. The archaeal cell envelope. Nat. Rev. Microbiol. 9:414–426. 44. Forterre, P. & D. Prangishvili. 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. 45. Forterre, P. & D. Prangishvili. 2013. The major role of viruses in cellular evolution: facts and hypotheses. Curr. Opin. Virol. 3: 558–365. 46. Quemin, E.R., S. Lucas, B. Daum, et al. 2013. First insights into the entry process of hyperthermophilic archaeal viruses. J. Virol. 87:13379–13385. 47. Prangishvili, D., H.P. Arnold, U. Ziese et al. 1999. A novel virus family, the Rudiviridae: structure, virus-host interactions and genome variability of Sulfolobus viruses SIRV1 and SIRV2. Genetics. 153:1387–1396.
C 2015 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1341 (2015) 35–40
A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S Issue: DNA Habitats and Their RNA Inhabitants
Archaeal viruses: living fossils of the ancient virosphere? David Prangishvili Department of Microbiology, Institut Pasteur, Paris, France Address for correspondence: David Prangishvili, Department of Microbiology, Institut Pasteur, 25. Rue du Dr. Roux, Paris 75015, France. [email protected]
Studies on viruses parasitizing archaea reveal their specific nature and complete the tripartite division of the biosphere, indicating that each of the three domains of life—Archaea, Bacteria, and Eukarya—has its own set of associated DNA viruses. I argue that the remarkable morphotypical diversity of archaea-specific viruses could have originated from diverse viral archetypes that predated the divergence of the three domains of cellular life. It is possible that the descendants of many of these viral archetypes are able to parasitize extant archaea owing to their ability to evade archaea-specific defenses against virus infection, specifically the defenses linked to the evolution of cell envelope structure. Keywords: virus; archaea; domains of life; virus origin; virus evolution
Introduction The evolutionary history of the living world—since the development of molecular phylogeny in the second part of the last century—is mainly inferred from comparison of marker genes from different organisms. The most spectacular result of this approach was based on the comparative sequence analysis of universally conserved marker genes—ribosomal RNA genes—that “revealed that living systems represent one of three aboriginal lines of descent: (i) the eubacteria, . . . ; (ii) the archaebacteria, . . . ; and (iii) the urkaryotes, now represented in the cytoplasmic component of eukaryotic cells.”1 The discovery of the “three lines of the aboriginal descent,” later renamed as Bacteria, Archaea, and Eukarya,2 had a profound impact on the understanding of cellular evolution. The three-branch tree is an essential framework for reconstructing cellular evolution and the features of ancestral life forms, which predated the divergence between the ancestors of the three domains, the Bacteria, Archaea, and Eukarya, about 3.5 Ga. Molecular phylogeny is less efficient for studies on virus evolution. First, genomic similarity may not provide an optimal measure of viral phylogeny because of extensive exchange of genes between viruses, between viruses and plasmids, and between
viruses and host cells, confusing the gene origin and mixing up horizontal and vertical inheritance. Second, as there are no universal genes shared by all viruses, molecular phylogeny would be inapplicable for the measurement of large evolutionary distances and the assignment of viruses to higher-order taxa. In fact, the only feature that can be considered as a universal marker for all viruses appears to be the virus capsid—the virion. Consequently, is has been argued that comparison of virion architectures and/or the structures of virion proteins of different viruses could be an appropriate approach for the phylogenetic classification of viruses.3–5 Below, I will briefly summarize the knowledge on the morphological characteristics of viruses parasitizing archaea and attempt to infer what we have learned about the evolution of the viral world from the studies on archaeal viruses and their comparison with viruses from the other two domains. Morphotypes of archaeal viruses Viruses that parasitize archaea have been isolated nearly exclusively from two types of aquatic systems: extreme geothermal environments with temperatures exceeding 80°C and high-saline waters with nearly saturating concentrations of sodium chloride. The number of described species, all carrying
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DNA genomes, single stranded (ss) or double stranded (ds), represents only a small percentage, hardly more than 1%, of known viruses from the two other domains, Bacteria and Eukarya. However, even this limited number of species reveals a remarkable—unprecedented in other domains— diversity of virion morphotypes (for recent reviews, see Refs. 6–8). The morphological landscape of archaeal viruses comprises a number of virus types never observed among viruses from the other two domains. These include viruses with particles resembling bottles (family Ampullaviridae),9 spindles—tail-less, tailed, and two-tailed (families Fuselloviridae and Bicaudaviridae),10 droplets (family Guttaviridae),11,12 and spirals (family Spiraviridae).13 Also specific to archaea are viruses with unique combinations of dsDNA genomes with virions of linear (families Rudiviridae and Lipothrixviridae from the order Ligamenvirales),14 bacilliform (family Clavaviridae),15 and spherical (family Globuloviridae)16 shape. In addition to these archaea-specific viruses, archaea replicate all types of dsDNA viruses known to infect bacteria, including head-tailed viruses (families Myoviridae, Siphoviridae, and Podoviridae from the order Caudovirales),17 icosahedral viruses with internal lipid envelopes (families Sphaerolipoviridae and Turriviridae in archaea; Tectiviridae and Corticoviridae in bacteria),8–18 and pleomorphic viruses (families Pleolipoviridae in archaea and Plasmaviridae in bacteria).19,20 There are reasons to believe that the bewildering morphotypical diversity of known archaeal viruses, far exceeding (and including) that of bacterial viruses, represents only the tip of an iceberg. Observations of virus-like particles in natural habitats where archaea dominate are consistent with this suggestion.21–25 Moreover, the number of archaeal virus morphotypes constantly expands with the exploration of new hosts and new habitats. By contrast, no new morphotype of bacterial virus has been found since the 1970s, despite isolation of thousands of new species.26 Virion morphogenesis and constituents of archaeal viruses The archaeal viruses with morphotypes similar to those of bacterial viruses (e.g., head-tailed and icosahedral viruses) apparently follow the same prin36
ciples of virion morphogenesis as their bacterial counterparts:27 DsDNA is packaged into a preformed capsid as a tightly wound spool, with help from a nucleoside triphosphate–dependent molecular motor.28 Moreover, the major capsid proteins (MCPs) of some archaeal and bacterial viruses are highly similar in structure, carrying Hong-Kong 79 (HK79)-like fold (head-tailed viruses) or double jelly-roll fold (icosahedral viruses with internal lipid layer).29,30 The archaeal viruses with archaea-specific virion types seem to exploit particular pathways of virion assembly, different from the translocation of the genome into the preformed capsid. For several of these viruses, distinct steps of virion morphogenesis could be postulated based on electron microscopy (EM) examination of virions in native and partially disintegrated states (Fig. 1). An essential step in virion morphogenesis appears to be the formation of a nucleoprotein filament by the interaction of DNA with multiple copies of virusencoded DNA-binding MCPs; for members of the Ampullaviridae, Spiraviridae, Bicaudaviridae, Rudiviridae, Lipothrixviridae, and Globuloviridae, the existence of such nucleoprotein filaments has been documented by EM observations (Fig. 1). Depending on the properties of the MCPs, the nucleoprotein is condensed into virion cores of different shapes, which often determine the virion morphotype. A good example showing that the manner of nucleoprotein organization shapes the virion morphotype is provided by the Ampullaviridae.9 In their virions, the dsDNA-containing nucleoprotein is folded into an unusual cone-shaped core that, after being encased in the lipid-containing envelope, determines the exceptional bottle-shaped morphotype of the mature virion (Fig. 1). Behind the exceptional coil shape of the Spiraviridae virions is another special manner of nucleoprotein organization.13 The circular nucleoprotein, formed by ssDNA and MCP copies, is folded into a structure with two levels of helical organization: the two halves of the circular nucleoprotein intertwine with each other and form a rope-like fiber, which is condensed into the helical coil spring of the virus particle (Fig. 1). The spherical and spindle-like shapes of the Globuloviridae and Bicaudaviridae virions, respectively, are likely also coupled with unusual mechanisms of condensation of their dsDNA-containing nucleoproteins.
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Figure 1. Virions of six families of archaeal viruses in native and partially degraded states (transmission and cryo-electron micrographs). For all virions, the DNA–protein filament represents a basic structural element and is highlighted by black arrows. For the Ampullaviridae and Spiraviridae, nucleoprotein organization in the native virion is schematically illustrated. Two forms of the Bicaudaviridae virion are shown, (I) immature and (M) mature two-tailed; in inset: horizontal slice through the threedimensional reconstruction of part of the mature virion. The virion of the Lipothrixviridae is shown in two states: (N) native and (Δ env) devoid of the lipid-containing envelope. The structures of the MCP of the rudivirus SIRV and two MCPs of the lipothrixvirus AFV1 are colored using a rainbow color gradient from the N-terminus (blue) to the C-terminus (red). Adapted from Refs. 9, 13, 16, 23, 34, and 47.
The manner of folding of nucleoprotein filaments in archaea-specific viruses, as mentioned earlier, is apparently controlled by the physicochemical properties of their MCPs. The MCP structures have only been resolved for members of the families Rudiviridae, Lipothrixviridae, and Bicaudaviridae.31–33 They all carry unique four-helix-bundle folds, which are highly similar for Rudiviridae and Lipothrixviridae, but different for Bicaudaviridae. The wrapping of similar MCPs of Rudiviridae and Lipothrixviridae around linear dsDNA forms helical nucleoprotein filaments of similar structure, as observed by cryoEM (Fig. 1). In the linear virions of Lipothrixviridae, the helical nucleoprotein is encased in a lipidcontaining envelope, whereas in virions of the Rudiviridae it remains nonenveloped (Fig. 1).
The role of the four-helix-bundle MCP of the Bicaudaviridae in virion morphogenesis is unknown. The spindle-shaped virion extruded from the host cell undergoes extensive changes in the course of its extracellular maturation, leading to the formation of helical appendages at both pointed ends of the immature virion.34 Observation of a nucleoprotein filament inside these appendages (Fig. 1) indicates its release, during virion maturation, from the condensed state it has in the spindleshaped virion. Polyphyletic origin of archaeal viruses from primordial ancestors The morphological distinctiveness of archaeal viruses extends to the genetic information that they
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carry and the structures of the proteins that they encode: the vast majority of their genes do not resemble any gene in the extant databases in terms of sequence,35,36 and many encode proteins that carry unusual folds.29,37 Moreover, for some cases it was shown that proteins without known homologues encode peculiar features of the infection cycle, specifically those of virion egress, not encountered in viruses of bacteria and eukaryotes.38 The available information leads to the notion that viruses that parasitize archaea form a special group in the viral world and, thus, each of the three domains of life has its own set of associated DNA viruses. Despite the pronounced differences, some members of the distinct, domain-specific groups of viruses share a few genes. For example, homologous genes encoding protein-primed DNA polymerases and replication-initiator Rep proteins have been identified in virus species from all three domains (for review, see Ref. 7). These virus species are extremely diverse in their morphotypes and genomic properties, and the occurrence of homologous genes in them could hardly be owing to close evolutionary relationships. Neither is horizontal gene transfer a probable explanation, given the large evolutionary distances between their hosts and the low probability of cross-domain spreading. The incidence of virus-specific genes that encode homologous proteins in viral species from the three domains of life is most consistent with the acquisition of these genes directly from an ancestral pool of viral genes that predated the divergence of the three domains of life, in the times of the last universal common ancestor of cellular organisms (LUCA). The notion of an ancestral pool of viral genes is consistent with the existence of viral lineages— a group of viruses with structurally similar virions and MCPs—that span all three domains of cellular life and originate from an ancestor parasitizing on the LUCA.3,4 Two such structure-based lineages of dsDNA viruses have now been defined.39 One comprises icosahedral viruses with MCPs carrying the double jelly-roll fold: archaeal Turriviridae, bacterial Tectiviridae and Corticoviridae, and eukaryal Adenoviridae and the “Megavirales.” Another includes bacterial and archaeal head-tailed viruses (Caudovirales) and eukaryal Herpesvirales, which carry MCPs with the HK97-like fold. Thus, it appears that in the time of the LUCA, at least two ancestral morphotypes—archetypes—of icosahedral viruses 38
existed, one that gave rise to the extant viruses with the double jelly-roll MCP and another that generated the viruses with the HK97 type of MCP. If ancestors of the icosahedral viruses were present in the times of the LUCA, it is reasonable to suggest that the diverse morphotypes of archaeal DNA viruses may have also had their origins in the archetypes present in the ancient virosphere,40 predating the divergence of the three cellular domains.7,41 Although possible, it is highly improbable that these viruses, with diverse architectural principles and assembly pathways of their virions, appeared specifically in extreme environmental conditions later in the evolution of the biosphere. The primordial existence of archetypes of extant archaeal viruses with fundamentally different solutions for packaging and protection of genomic material depicts the ancient virosphere as a kind of laboratory for structural and functional designs of virus particles. In this laboratory, the viral lifestyle seems to have been developed,42 and multiple efficient ways were explored for the packaging and delivery of viral genomes, using different proteins for these functions. Moreover, such a scenario implies that there must have been a certain predisposition in the biosphere for the development of the viral lifestyle, and it was not a rare or accidental event. The specific nature of the archaeal virosphere is linked with the envelope composition of host cells The origin of the differences between the virus types parasitizing archaea and those parasitizing bacteria—the former including all bacterial types— is unclear. Recently, I suggested that these differences are linked to different strategies developed in the two domains against virus infection and that these strategies concerned modifications of the cell envelope: the bacterial strategy involved increasing the complexity of the cell wall—by introduction of peptidoglycan, outer membrane, capsule, and so on—while the archaeal solution mainly involved chemical modification of the cell surface.7 Indeed, the cell wall of bacteria is much more complex in its organization compared to the cell envelope of archaea, the sole constituent of which, in many cases (specifically in hyperthermophiles—the hosts for the majority of archaeal viral morphotypes), is an S-layer, a paracrystalline protein layer that presumably is the earliest cell wall structure to have
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evolved.43 On the other hand, archaea, with their relatively simple cell envelope, have all the surfaceexposed proteins modified; the most common is N-glycosylation of S-layer proteins, a modification rarely observed in bacteria.43 Seeing the interplay between viruses and their hosts as the driving force for the emergence of extant cell envelopes of Bacteria and Archaea is in line with the hypothesis, proposed by Patrick Forterre and me, that states that the arms race between viruses and cells was the driving force behind major evolutionary novelties in the biosphere.44,45 Under the proposed scenario, the majority of ancestral virus types do not parasitize bacteria because the latter have developed a complex cell wall structure, through which only very few virus types can channel their genomic material.7 However, chemical modification of the cell surface, the strategy preferred by archaea, is apparently less restrictive, and many ancestral virus types could develop mechanisms allowing them to evade it and remain associated with archaeal hosts.7 With extremely scarce available information on the entry process of archaeal viruses,46 it is impossible to provide support for the proposed scenario. The merit of the presented attempts to rationalize the data on the morphological peculiarities of archaeal viruses, especially for the purpose of reconstructing evolutionary scenarios, is significantly constrained by our limited knowledge on the subject. Only rudimentary information is available on the structure of virions and MCPs of known archaeal virus species. Moreover, we are a long way from a full comprehension of the global viral diversity—much more remains to be known on viral diversity in different environments and in a broader range of host taxa. These are now the lines of research that promise to provide critical insights into the evolutionary history of viruses and their interactions with host cells. Acknowledgment I gratefully acknowledge the support of l’Agence Nationale de la Recherche, and stimulating discussion with Patrick Forterre and Mart Krupovic, and their critical comments on the manuscript. Conflicts of interest The author declares no conflicts of interest.
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