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Archaeal viruses and bacteriophages: comparisons and contrasts Maija K. Pietila¨, Tatiana A. Demina, Nina S. Atanasova, Hanna M. Oksanen, and Dennis H. Bamford Institute of Biotechnology and Department of Biosciences, P.O. Box 56, Viikinkaari 5, 00014 University of Helsinki, Helsinki, Finland

Isolated archaeal viruses comprise only a few percent of all known prokaryotic viruses. Thus, the study of viruses infecting archaea is still in its early stages. Here we summarize the most recent discoveries of archaeal viruses utilizing a virion-centered view. We describe the known archaeal virion morphotypes and compare them to the bacterial counterparts, if such exist. Viruses infecting archaea are morphologically diverse and present some unique morphotypes. Although limited in isolate number, archaeal viruses reveal new insights into the viral world, such as deep evolutionary relationships between viruses that infect hosts from all three domains of life. Discovery of archaeal viruses All cellular organisms are susceptible to viral infections, which makes viruses a major evolutionary force shaping cellular life. Furthermore, it has been estimated that there are more than 1031 viruses on Earth [1,2]. Because prokaryotes, comprising archaea and bacteria, outnumber eukaryotes, their viruses are thus the most abundant biological entities in the biosphere. The first bacterial viruses, that is, bacteriophages, were described in the 1910s, and since then, thousands have been discovered [3]. However, the first archaeal virus to be described was isolated decades later, in the 1970s, even before the formal establishment of Archaea as the third domain of life [4,5]. Viruses infecting archaeal hosts have gained wider attention during recent years, and the number of studied archaeal viruses is now about 100 [6,7]. However, this is only a few percent of all known prokaryotic viruses because over 6000 bacterial viruses have been studied to date [8]. The aim of this review is to define the present knowledge of archaeal viruses and compare them to bacteriophages. The domain Archaea has traditionally been divided into two major phyla, Crenarchaeota and Euryarchaeaota, including extremophiles (see Glossary) from habitats such as hot springs and salt lakes. Thermophiles and hyperthermophiles are found in both phyla whereas halophilic and methanogenic archaea are so far classified only into Corresponding author: Bamford, D.H. ([email protected]). Keywords: Archaea; bacteria; virus; virion; morphotype. 0966-842X/$ – see front matter ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tim.2014.02.007

Euryarchaeaota [9,10]. Archaea have also been cultivated from moderate environments such as seawater and soil. Consequently, an additional phylum, Thaumarchaeota, has been formed to contain mesophilic and thermophilic ammonia-oxidizing archaea [11]. However, all known archaeal viruses infect extremophiles – mainly hyperthermophiles belonging to the crenarchaeal genera Sulfolobus and Acidianus or halophiles of the euryarchaeal genera Haloarcula, Halorubrum, and Halobacterium [6,7]. Even though bacteria are also found in diverse extreme habitats such as hypersaline lakes, archaea typically dominate at extreme salinities, based on both cultivation-dependent and -independent studies [6,12–15]. Consequently, archaeal viruses do the same in hypersaline environments. About 50 prokaryotic haloviruses were recently isolated from nine globally distant locations, and only four of them infected bacteria [6,16]. In contrast to archaeal isolates, bacterial viruses have been isolated for both non-extremophiles and extremophiles, and the majority of the studied bacteriophages infect the former [8,17]. Although no archaeal viruses have yet been isolated from non-extreme niches, a putative provirus was recently recognized in the genome of a thaumarchaeon and virus-like particles (VLPs) resembling archaea-specific viruses have been detected in freshwater sediments [18,19]. To date, the isolated bacterial viruses infect hosts belonging to almost 200 different genera, whereas archaeal hosts belong to less than 20 genera [8]. In addition to virus isolates, several proviruses have been detected in archaeal genomes. These proviruses show similarity to head-tailed, tailless icosahedral, spindleshaped, and ovoid-shaped archaeal viruses [20–23]. In this review, we take a virion-centered view (Box 1) and focus on cultivated viruses (Figure 1). Taken together, archaeal viruses are morphologically more diverse than bacterial Glossary Alkaliphile: an organism that requires a high pH to grow, usually above 9. Extremophile: an organism that is dependent on extreme habitats such as hypersaline or hyperthermic. Halophile: an organism that requires at least 0.17 M [1% (w/v)] NaCl for optimal growth. Head-tailed virus: a virus with an icosahedral capsid and a helical tail. Hyperthermophile: an organism that grows optimally above 808C. Mesophile: an organism that grows optimally at 15–608C. Methanogen: an anaerobic organism that produces methane by reduction of carbon dioxide, acetic acid, or other, often simple, carbon compounds. Neutrophile: an organism that grows optimally at a pH around 7. Thermophile: an organism that grows optimally above 608C and up to 808C. Trends in Microbiology xx (2014) 1–11

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Box 1. What is a virus? Viruses are self-replicating obligatory parasites without inherent metabolism. When they exist in extracellular environment, viruses are usually biochemically inert. In addition, viruses are traditionally considered to be very small filterable agents. However, this view has been challenged after the discovery of an archaeal virus developing its tails ex vivo [59] and after realizing that viruses such as Mimivirus and Pandoravirus can be even larger than the smallest cells [114,115]. Viruses consist of particles containing a nucleic acid (either DNA or RNA), which encodes the information necessary for their replication. Furthermore, viral genomes are either circular or linear, single- or double-stranded (ss or ds), and as one molecule or segmented. In the Baltimore system, viruses are divided into seven classes of DNA, RNA, and reverse-transcribing viruses [116]. When the genetic information includes a gene (or genes) encoding a capsid protein (or capsid proteins), which is capable of forming a capsid shell, then a virus particle can be formed. The capsid-encoding

gene found in the viruses distinguishes them from other selfreplicating entities such as plasmids. A virion is defined as an infectious virus particle, which functions as both a protective shell for the genome and a vehicle for nucleic acid delivery to an appropriate cell to initiate a new reproduction cycle. To date, all known archaeal viruses have DNA genomes, whereas the known bacterial viruses have either DNA or RNA genomes including circular ssDNA, circular dsDNA, linear dsDNA, linear ssRNA, or segmented dsRNA [17]. Bacteriophages with linear dsDNA genomes form the largest group. Most archaeal viruses also have dsDNA genomes, either linear or circular, and only a few viruses with circular ssDNA have been isolated [55,78,79]. Although no RNA viruses infecting archaea have been discovered, metagenomic analyses of viral sequences in archaea-dominated hot springs indicate that they might be there waiting to be discovered [117].

1970s even though thousands of isolates have been examined [8]. According to the International Committee on Taxonomy of Viruses (ICTV), archaeal viruses are classified into 15 families or corresponding groups, while bacterial ones belong to ten families [8,17]. In addition to virion morphotypes, one more peculiar feature of archaeal viruses is their genomes. Although morphologically diverse, all

ones, although they are fundamentally underrepresented among the prokaryotic virus isolates [7,8]. So far, 16 different morphotypes have been described for archaeal viruses and many of these are unique (Figure 1 and Table 1). For bacteriophages, only nine morphotypes are known (Figure 1 and Table 1). Furthermore, no new bacterial virion morphotypes have been discovered since the

Podoviridae

Tecviridae Corcoviridae “Turriviridae” “Sphaerolipoviridae”

Microviridae Leviviridae

Cystoviridae

Myoviridae Siphoviridae Plasmaviridae “Pleolipoviridae” Globuloviridae Guaviridae APOV1

Clavaviridae

Inoviridae

Ampullaviridae

Lipothrixviridae: beta, gamma, delta

Lipothrixviridae: alpha

Rudiviridae

‘Spiraviridae’

Fuselloviridae salterprovirus TPV1, PAV1

Bicaudaviridae

STSV1, STSV2, SMV1, APSV1 Key:

Archaeal and bacterial

Bacterial

Archaeal

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Figure 1. Virion morphotypes of prokaryotic viruses. Names of viral genera or families based on International Committee on Taxonomy of Viruses (ICTV) are indicated below the schematic virus particles. If an archaeal virus has not been assigned to any genus or family, individual virus names are given. The virions are not drawn to scale. Abbreviations: APOV1, Aeropyrum pernix ovoid virus 1; APSV1, Aeropyrum pernix spindle-shaped virus 1; PAV1, Pyrococcus abyssi virus 1; SMV1, Sulfolobus monocaudavirus 1; Sulfolobus tengchongensis spindle-shaped virus 1 (STSV1); STSV2, Sulfolobus tengchongensis spindle-shaped virus 2; TPV1, Thermococcus prieurii virus 1.

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Table 1. Archaeal viruses Morphotype

Classification a

Host b

Example

Genome

Head-tailed, with a long contractile tail Head-tailed, with a long noncontractile tail Head-tailed, with a short tail Tailless icosahedral

Siphoviridae Myoviridae Podoviridae ‘‘Turriviridae’’ c ‘‘Sphaerolipoviridae’’ c

E E E C E

HVTV-1 HSTV-2 HSTV-1 STIV SH1

Droplet-shaped Bottle-shaped Spherical, with helical core Pleomorphic

Guttaviridae APOV1 Ampullaviridae Globuloviridae ‘‘Pleolipoviridae’’ c

C C C C E

SNDV – ABV PSV HRPV-1

Bacilliform Filamentous

Clavaviridae Lipothrixviridae

C C

APBV1 AFV1

dsDNA, linear dsDNA, linear dsDNA, linear dsDNA, circular dsDNA, linear/circular dsDNA, circular dsDNA, circular dsDNA, linear dsDNA, linear ssDNA/dsDNA, linear/circular dsDNA, circular dsDNA, linear

Rod-shaped Coil-shaped Spindle-shaped, with a short tail

Rudiviridae ‘‘Spiraviridae’’ c Fuselloviridae Salterprovirus

C C C E

SIRV2 ACV SSV1 His1

dsDNA, linear ssDNA, circular dsDNA, circular dsDNA, linear

TPV1, PAV1 STSV1, STSV2, SMV1, APSV1 Bicaudaviridae

E C

– –

dsDNA, circular dsDNA, circular

C

ATV

dsDNA, circular

Spindle-shaped, with a long tail Spindle-shaped, with two long tails

Lipid content has been verified

Contain lipids SH1, HHIV-2, and SNJ1 contain lipids

Contain lipids Contain lipids

Alpha-, beta-, and gammalipothrixviruses contain lipids

Contain a lipidmodified MCP STSV1 and STSV2 contain lipids

Refs [32] [32] [38] [42] [41,43, 45,48] [82] [20] [81] [39] [36,78] [54] [111]

[52] [55] [58] [61,67] [64,65] [20,60, 72,73] [59]

a

If the virus remains unclassified, its name is mentioned.

b

Abbreviations: C, crenarchaeon; E, euryarchaeon.

c

The approval of the family is pending at the ICTV.

known archaeal viruses have a DNA genome (Box 1). Moreover, the genome sequences or gene products of archaeal viruses typically only share sequence similarity with closely related viruses except for head-tailed isolates [21,24]. Morphotypes of archaeal viruses Described archaeal viruses can be divided into those infecting euryarchaea and those infecting crenarchaea, and these two groups share only two morphotypes: spindle-shaped and tailless icosahedral (Table 1). Currently, euryarchaeal viruses account for more than half of all studied archaeal viruses [6,7]. However, crenarchaeal viruses are morphologically more diverse and, consequently, they have been classified into nine viral families [8,17]. Interestingly, unusual morphotypes typical of crenarchaeal viruses have been detected also in hypersaline environments where halophilic euryarchaea thrive, indicating that euryarchaeal viruses might be more diverse than currently known [25–28]. Head-tailed viruses All head-tailed isolates infect euryarchaea, either halophilic or methanogenic [6,7]. Head-tailed VLPs have also been detected in habitats typical of hyperthermophilic crenarchaea, but no such virus has yet been isolated [29]. So far, only five viruses infecting methanogens have been isolated, and they all are either myo- or siphoviruses (Table 1) [7]. Most haloarchaeal virus isolates also represent the head-tailed type. However, electron microscopy (EM) observations propose that such particles represent the minority in

hypersaline environments, while spindle-shaped and spherical particles are the most abundant ones [6,7,25–27]. So far, about 40 head-tailed isolates have been obtained for haloarchaea, and these include all three types of head-tailed viruses: myo-, sipho-, and podoviruses (Table 1) [6,7]. VLP concentration is high in hypersaline waters, about 107–109 particles per milliliter [25–27]. This may facilitate recombination, and one such an example is provided by haloarchaeal myoviruses HF1 and HF2, which have been isolated from the same Australian saltern. Their genome sequences are 94% identical, and most sequence differences are located at the right arm of the genomes [30,31]. These viruses also show sequence similarity to another myovirus, Halorubrum sodomense tailed virus 2 (HSTV-2), which has been isolated from Israel [32]. Thus, haloarchaeal viruses are able to spread over long distances. Myoviruses wH and wCh1, which both have been isolated from laboratory cultures of haloarchaea, share significant sequence similarity. Their hosts, however, originate from different environments, because wH infects neutrophilic Halobacterium salinarum and wCh1 infects alkaliphilic Natrialba magadii [33–35]. Haloarchaeal viruses often require high salinity to be infective [35–37]. It has been observed that head-tailed viruses infecting extremely halophilic archaea are inactivated at low salinity, but regain infectivity when high salinity conditions are restored [32,38]. It has been proposed that such behavior might help viruses to survive in their natural habitats, where salinity fluctuations may occur. These stability experiments also showed that the 3

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Review capsid of HSTV-2 stays intact at low salinity enabling the determination of its 3D structure at high resolution [32]. The capsid structure of HSTV-2 revealed that the virus has enlarged its capsid by inserting a stabilizing protein in the protein lattice between the major capsid protein (MCP) subunits – a strategy not previously observed. Thus, the HSTV-2 virion can accommodate a genome, which is larger than those of other viruses with same capsid triangulation number [32]. Studies of head-tailed viruses have also revealed that wCh1 packages host RNA molecules into its virions, which may assist in the genome packaging [35]. Spherical viruses Two types of spherical archaeal viruses have been recognized: (i) those having a helical nucleoprotein core and (ii) those with an icosahedrally symmetric capsid (Table 1). The former group is represented by the viral family Globuloviridae, which includes crenarchaeal Pyrobaculum spherical virus (PSV) and Thermoproteus tenax spherical virus 1 (TTSV1) [17]. The virion consists of a lipid envelope surrounding a linear double-stranded DNA (dsDNA) genome that forms the helical nucleoprotein complex. Thus, this architecture resembles that of eukaryotic singlestranded RNA (ssRNA) paramyxoviruses [17,39]. Tailless icosahedral morphologies are represented among both crenarchaeal and euryarchaeal viruses [37,40–43]. Sulfolobus turreted icosahedral virus (STIV) and STIV2, which infect hyperthermophilic crenarchaea, form the proposed family Turriviridae [44]. These viruses are closely related having similar genome organization and several homologous genes as well as conserved capsid architecture [40,42]. Their icosahedral capsids contain an inner lipid membrane, and the capsid surface is decorated with turret-like structures at vertices [40,42]. Three closely related tailless icosahedral viruses infect a euryarchaeaon, Haloarcula hispanica [37,41,43]. The genome sequences of SH1, PH1, and Haloarcula hispanica icosahedral virus 2 (HHIV-2) are more than 50% identical [41,43]. Interestingly, SH1 and PH1 have been isolated from Australia, but HHIV-2 originates from Italy [37,41,43]. Thus, in addition to head-tailed viruses, this is yet another example of closely related haloarchaeal viruses dispersed over long distances. Similar to STIV and STIV2, SH1 and HHIV-2 have been shown to contain lipids, and typically prokaryotic tailless icosahedral viruses acquire their lipids selectively from the host cell membrane [41,45]. This is due to the geometrical constrains associated with the icosahedral capsid, which prefers lipids able to produce appropriate membrane curvature [46,47]. A temperate virus, SNJ1, which infects a haloarchaeon Natrinema sp. J7-1, has also been proposed to be icosahedrally symmetric [48]. The virion is spherical and contains lipids. Furthermore, SNJ1 encodes a putative ATPase that is conserved among tailless, membrane-containing icosahedral dsDNA viruses [48,49]. Linear viruses All characterized linear archaeal viruses infect hyperthermophilic crenarchaea (Table 1), although such VLPs have also been observed in hypersaline environments [17,27,28]. These viruses can be divided into four groups: 4

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(i) filamentous, (ii) rod-shaped, (iii) coil-shaped, and (iv) bacilliform (Table 1). Filamentous and rod-shaped viruses are classified into the family Lipothrixviridae and Rudiviridae, respectively. Lipothrixviridae is further divided into four genera: Alpha-, Beta-, Gamma-, and Deltalipothrixvirus [17]. Lipothrixviruses have typically flexible, lipid-containing virions, although no lipids were found in the virions of deltalipothrixviruses [17,50]. Gammalipothrixvirus Acidianus filamentous virus 1 (AFV1) has two MCPs, and it has been proposed that the genome wraps around one MCP and the other interacts with both the DNA and lipid envelope [51]. By contrast, Rudiviruses have a nonenveloped rigid virion [17]. Sulfolobus islandicus rod-shaped viruses 1 and 2 (SIRV1 and SIRV2) contain only one MCP, which most likely binds to the DNA forming a helical structure [52]. Lipothrix- and rudiviruses have the same MCP fold and share several homologous genes. Consequently, it has been proposed that these viral families form the order Ligamenvirales [53]. Virions of Aeropyrum pernix bacilliform virus 1 (APBV1) are stiff and bacilli-like, and the virus has been classified into a new viral family, Clavaviridae [17,54]. Aeropyrum coil-shaped virus (ACV), which is classified into the proposed family Spiraviridae, has hollow cylinder-like virions formed by a coiling nucleoprotein fiber. The genome of APBV1 (5278 bp) is one of the smallest known dsDNA genomes, whereas ACV has the largest known singlestranded DNA (ssDNA) genome (24 893 nucleotides) [54,55]. In addition to head-tailed and tailless icosahedral viruses, only a few other archaeal viruses are known to be lytic. Despite different morphologies, lytic viruses SIRV2 and STIV use the same, unique exit strategy. Both induce pyramid-like structures on the cell surface, which upon opening release progeny virions [56]. Detailed information on infection cycles of archaeal viruses is limited, and especially the entry process is poorly characterized. For SIRV2, it was recently shown that it adsorbs rapidly to its host cells and utilizes pilus structures on the cell surface. After initial binding to the tip of a pilus, SIRV2 is suggested to move along the filament to the cell surface [57]. Spindle-shaped viruses Spindle-shaped VLPs are abundant in both hypersaline and hyperthermic environments [27,29]. Such viruses have a short or long tail attached to one end of the virion or long tails attached to both ends [58–60]. Fifteen spindle-shaped viruses have been isolated (Table 1) and all of them, except for one, infect hyperthermophiles [61]. In addition, a spindle-shaped VLP, Methanococcus voltae A3 VLP (A3-VLP), has been isolated from a methanogenic euryarchaeaon [62]. The family Fuselloviridae is the biggest group of spindle-shaped viruses and includes crenarchaeal viruses with a short tail [17]. The type species is Sulfolobus spindleshaped virus 1 (SSV1). The virion is rather flexible, although the presence of a lipid membrane is unclear [17,63]. Fuselloviruses are closely related and share gene synteny as well as significant nucleotide sequence similarity [58]. Thermococcus prieurii virus 1 (TPV1) and Pyrococcus abyssi virus 1 (PAV1) resemble morphologically fuselloviruses but

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Review infect hyperthermophilic euryarchaea. However, they show no significant sequence similarity to fuselloviruses and remain unclassified [64,65]. His1 is so far the only described spindle-shaped virus infecting halophilic euryarchaea and it is classified into a floating genus Salterprovirus [17,61]. Using His1 as a model, the first DNA ejection study for archaeal viruses was performed [66]. Physical measurements showed that this ejection is unidirectional but randomly paused and incomplete, and it is thought that host factors are necessary to finish the ejection. His1 has a linear dsDNA genome encoding a putative type-B DNA polymerase for proteinprimed replication, whereas fuselloviruses have circular dsDNA genomes [58,67]. These viruses show no significant genome sequence similarity, but share many features in addition to the virion appearance [58,61,67]. Both His1 and fuselloviruses are nonlytic and cause a persistent infection resulting in host growth retardation and continuous virus production [61,68]. In addition, the MCPs of His1 and SSV1 are 47% similar at the amino acid level [61,69]. Similar to fuselloviruses, His1 has been reported to form elongated particles with varying size and this elasticity may be due to the lipid modification observed in His1 MCP [61]. Furthermore, PAV1 virions are flexible and consist of one MCP, which contains two hydrophobic motifs similar to SSV1 and His1 MCPs [61,65,70]. A recent analysis identified PAV1 MCP as a homolog of SSV1 and His1 MCPs and showed that the same homolog is present in TPV1 and A3-VLP. Thus, it was proposed that all shorttailed spindle-shaped viruses can be classified into different genera within the family Fuselloviridae [71]. Spindle-shaped viruses with one or two long tails are known to infect hyperthermophilic crenarchaea (Table 1). Acidianus two-tailed virus (ATV), the only member in the family Bicaudaviridae, has an extraordinary capability to form the tails outside the host cells [17,59]. Sulfolobus tengchongensis spindle-shaped viruses 1 and 2 (STSV1 and STSV2), Sulfolobus monocaudavirus 1 (SMV1), and Aeropyrum pernix spindle-shaped virus 1 (APSV1) typically have one long tail, but two-tailed forms have also been detected [20,60,72,73]. STSV1 and STSV2, both isolated from solfataric fields in China, are closely related sharing approximately 80% genome sequence identity [60,73]. Interestingly, the only MCP of STSV1 and STSV2 show significant similarity to one of the major structural proteins of ATV and these viruses share additional homologous genes [60,71,73]. Lipid analyses have revealed selectively acquired lipids in both STSV1 and STSV2 virions, but chloroform–methanol extraction did not release lipids from ATV virions [59,60,73]. Recently, it was proposed that STSV1 and STSV2 could be classified into the family Bicaudaviridae as a new genus. By contrast, APSV1 was suggested to belong to the group of short-tailed spindle-shaped viruses because a homolog of SSV1 and His1 MCPs was identified in APSV1 [71]. Pleomorphic viruses Recently, a worldwide distributed group of pleomorphic viruses has been described [36]. These viruses have been designated pleolipoviruses based on their lipid envelope and pleomorphic appearance (Figure 2A), and a new viral

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family, Pleolipoviridae, has been proposed [36]. Pleolipoviruses contain two or three major structural proteins, and one of them forms spike-like structures on the virion surface, whereas the other(s) are internal membrane proteins (Figure 2B,C). The spike proteins of His2 and Halogeometricum pleomorphic virus 1 (HGPV-1) are lipid modified, whereas the spike protein of Halorubrum pleomorphic virus 1 (HRPV-1) is glycosylated [36,74,75]. In addition to pleolipoviruses, bacilliform, rod-shaped, and tailless icosahedral archaeal viruses have glycosylated structural proteins [54,76,77]. For HRPV-1, this glycomodification has been shown to be important for infectivity [75]. Pleolipoviruses have five core genes, which include two genes encoding major structural proteins and one encoding a putative ATPase (Figure 2D) [78]. Core genes have also been identified in the genomes of fuselloviruses, which share 13 such genes reflecting their larger genomes compared to pleolipoviruses [58,78]. The genome of pleolipoviruses resides inside a lipid envelope without forming any ordered nucleoprotein complex [36,74]. These viruses are nonlytic, only retarding the host growth, and they acquire their lipids unselectively from the host cell membrane. Consequently, it has been proposed that pleolipoviruses use budding to exit infected cells [36,79,80]. HRPV-1, the type species of the family Pleolipoviridae, was the first described archaeal virus having an ssDNA genome [79]. In addition, there are three other ssDNA and four dsDNA viruses in this family, and one of the dsDNA genomes is linear, whereas others are circular [67,78–80]. Thus, the family Pleolipoviridae challenges the traditional view of virus classification based on genome type. Bottle- and droplet-shaped viruses Acidianus bottle-shaped virus (ABV) and Sulfolobus neozealandicus droplet-shaped virus (SNDV) infect hyperthermophilic crenarchaea and represent the viral families Ampullaviridae and Guttaviridae, respectively [17,81,82]. Recently, an ovoid virion morphotype resembling SNDV was discovered by provirus induction, and the virus was designated as Aeropyrum pernix ovoid virus 1 (APOV1) [20]. The bottle-shaped virion of ABV seems to be rather complex. The genome is most likely in a nucleoprotein filament forming a cone-like structure that is surrounded by an outer layer, and the tip of the bottle is formed by a separate structure [81]. Comparison of archaeal viruses to bacterial counterparts Studied archaeal viruses represent only a fraction of all known prokaryotic viruses [8]. Despite this, significant similarities can be recognized between archaeal and bacterial viruses, including icosahedrally symmetric and pleomorphic ones. In addition, linear viruses are found in both groups. However, there are morphotypes not shared by these viruses. In this section, we will highlight how studied archaeal viruses compare to bacteriophages. Icosahedral viruses Icosahedral viruses have been described to infect both archaea and bacteria, and in both cases the viruses can 5

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(A)

(B)

(C) KDa 150 100 70 50 40 30 20 15

Key:

VP3

4

3

5

4

2

1

5

4

4

2

4

3

10 VP4

3

29 Spike 28 proteins

Internal membrane 27 proteins Lipids

ssDNA

HR PV -1 HR PV -2 HR PV -3 HR PV -6 HG PV -1 HH PV -1 Hi s2

Lipids

(D) Key:

Pleolipovirus core genes

Internal membrane protein genes

Spike protein genes

Common to all pleolipoviruses

Putave ATPase genes

HRPV-1 HRPV-2 HRPV-3 HRPV-6

Putave DNA polymerase genes

HGPV-1 HHPV-1

His-2 TRENDS in Microbiology

Figure 2. Archaeal pleolipoviruses. (A) Tomographic slice of HRPV-1 virions studied by cryo-EM. The arrows indicate spike structures protruding from the virion surface. The inset shows an empty particle devoid of the genome. Scale bar, 50 nm. Modified, with permission, from [36]. (B) A schematic model of the HRPV-1 virion. Two major structural proteins, VP3 and VP4, are indicated in the model. (C) Protein and lipid profiles of pleolipoviruses. The major VPs are indicated on the gel, and molecular mass markers are given on the left. Modified, with permission, from [36]. (D) The conserved gene block of pleolipoviruses. Genes or ORFs are indicated according to the key. Abbreviations: cryo-EM, cryo-electron microscopy; HGPV-1, Halogeometricum pleomorphic virus 1; HHPV-1, Haloarcula hispanica pleomorphic virus 1; HRPV, Halorubrum pleomorphic virus; ORF, open reading frame; VP, virion protein.

either have a tail (head-tailed viruses) or be tailless. Archaeal head-tailed viruses (myo-, sipho-, and podoviruses) morphologically resemble such bacteriophages. Crystallographic analyses have shown that the MCP of head-tailed phages such as Hong Kong 97 (HK97) forms an L-shaped molecule consisting of two domains (A and P), an extended N-terminal arm, and an E-loop (HK97 fold; Figure 3A) [83]. The recent cryo-electron microscopy (cryo-EM) and 3D image reconstruction of Haloarcula sinaiiensis tailed virus 1 (HSTV-1) at subnanometer resolution showed that archaeal head-tailed viruses also adopt the HK97 fold (Figure 3) [38]. Interestingly, this HK97 fold is also characteristic of herpesviruses and is indicative of a common ancestry linking archaeal and bacterial headtailed viruses together with eukaryotic herpesviruses [84,85]. At the genome level, remarkable diversity can be found among the head-tailed viruses. Their linear genomes are mosaics composed of variable and conserved genomic regions, which have evolved by recombination and have been derived from a common global pool of genes [31,86,87]. 6

All described tailless icosahedral viruses infecting archaea have a membrane under the capsid shell and share their virion morphology with the bacterial counterparts without any sequence similarity. All these viruses have either a linear or circular dsDNA genome and their protein-rich membranes follow the icosahedral shape of the capsid. The best studied viral system, where the icosahedral virion possesses an internal membrane, is bacteriophage PRD1 (Tectiviridae) infecting Gram-negative bacteria such as Escherichia coli or Salmonella enterica serovar Typhimurium [17]. There is broad structural and functional information on PRD1, providing insights into assembly of complex viruses, their DNA packaging mechanism, and entry and exit of the host cells [49,88–91]. The PRD1 capsid is composed of the MCP P3 cemented together with the minor capsid protein P30 [88,92]. PRD1 P3 has the canonical upright double b-barrel fold ubiquitous among the PRD1-like viruses including also phage PM2 (Corticoviridae) [93,94]. The same MCP fold has also been found from an archaeal virus STIV [95] as well as from eukaryotic viruses such as adenovirus, vaccinia virus, and

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(A)

(B) Spine helix A domain

P domain (D)

(E)

21 0 24 0 27 0 30 0 33 0 36 0

21 0 24 0 27 0 30 0 33 0 36 0

(C)

E loop

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Figure 3. Archaeal virus HSTV-1 has the canonical HK97-like fold. (A) The HK97-like fold with axial (A) and peripheral (P) domains, the spine helix of P domain, and the E loop are indicated. Modified, with permission, from [38]. (B) Cryo-electron micrograph of HSTV-1. Scale bar, 50 nm. Modified, with permission, from [38]. (C,D) HSTV-1 capsid structures based on the icosahedral reconstruction. The isosurface presentations are shown in (C) and (D) using different thresholds. Symmetry axes are indicated by an ellipse (twofold), a triangle (threefold), and a pentagon (fivefold). Modified, with permission, from [38]. (E) The HK97-fold fitted in the asymmetric unit of the HSTV-1 capsid. The unit is viewed from the capsid interior on the left and from the exterior on the right. Modified, with permission, from [38]. Abbreviations: HK97, Hong Kong 97; HSTV-1, Haloarcula sinaiiensis tailed virus 1.

Paramecium bursaria chlorella virus 1 (PBCV-1) [96–98], and even in virophage Sputnik [99]. It has been observed that there is a PRD1-encoded ATPase that is responsible for the translocation of the genome to a preformed viral procapsid [100]. This ATPase has a signature sequence discovered in many viral ATPases and all these ATPases are involved in the genome translocation by the internal membrane-containing icosahedral viruses [49,101]. There is a subgroup in PRD1-like viruses, whose virions resemble the overall architecture of PRD1, but their capsid organization is more complex with two MCP species instead of one. These viruses include Thermus phage P23-77, Salisaeta icosahedral phage 1 (SSIP-1), and archaeal Haloarcula-infecting viruses SH1, HHIV-2, and PH1 (and most probably SNJ1 infecting Natrinema) [16,41, 43,48,102,103]. Recently, it has been proposed that at least bacteriophage P23-77 and archaeal viruses SH1, HHIV-2, PH1, and SNJ1 belong to a new virus family, Sphaerolipoviridae [104]. Structural findings have illustrated that viruses infecting hosts that belong to different domains of cellular life can be grouped into structure-based viral lineages such as the above mentioned HK97-like and PRD1-like viruses. However, within a group, they do not share any sequence similarity, but have the same MCP fold and virion architecture [84,105,106]. Pleomorphic viruses Archaeal pleolipoviruses show similarities to bacterial pleomorphic, enveloped viruses L2 and L172, which infect mycoplasma Acholeplasma laidlawii cells [107].

First, these viruses resemble each other morphologically [36,107]. Second, L2 and L172 have been observed to acquire lipids unselectively from the host cell membrane, as described for pleolipoviruses [36,74,80,108]. As seen in pleolipoviruses, L2 and L172 also have different genome types, circular dsDNA and ssDNA, respectively [107,109]. However, although pleolipoviruses show gene synteny and sequence similarity, there is no detectable DNA homology between L2 and L172 [107]. Furthermore, mycoplasma viruses have different structural protein profiles [107]. Consequently, L2 has been classified into the viral family Plasmaviridae, and L172 has been proposed to represent another virus group [17,107]. Interestingly, the structural protein profile of L172 is very close to that of pleolipoviruses, with two major structural proteins of 15 and 53 kDa [107]. Thus, mycoplasma virus L172 might be related to archaeal pleolipoviruses, and these viruses may have a common ancestor. Unfortunately, there is no genome sequence data available for L172. Linear viruses Helical viruses are found in one bacterial and four archaeal virus families (Figure 1). The bacterial virus family Inoviridae is further divided into the genera Inovirus and Plectrovirus represented by flexible filaments and rigid rods, respectively [17]. Archaeal and bacterial helical viruses share no significant sequence similarity, and there are differences between these viruses [24]. First, bacterial filamentous viruses have ssDNA genomes, whereas archaeal viruses have dsDNA genomes [17]. Second, only 7

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Review archaeal filamentous viruses contain lipids [110]. Helical viruses infecting bacteria are nonlytic, and inoviruses infecting Gram-negative hosts are known to assemble and extrude their virions at sites between the outer and inner membranes of their host cells [17]. Among helical archaeal viruses, rod-shaped virus SIRV2 is known to lyse its host cells, but filamentous lipothrixviruses might utilize budding to exit cells without lysis as they contain a lipid envelope [56,110]. The filamentous virion of phage M13, the type species of the genus Inovirus, is composed of 2700 copies of the MCP in the cylindrical protein shell as well as a few copies of minor structural proteins at each end, which function either in adsorption or assembly [17]. Such a clear picture and function of minor structural proteins is not yet available for helical archaeal viruses, although virion models for the cylindrical body have been proposed [51]. Especially, archaeal lipothrixviruses possess a variety of virion terminal structures such as short filaments or appendices resembling claws, bottle brushes, or mops [17]. Despite different virion termini, both filamentous bacterial and archaeal viruses have been observed to use pili on the cell surface to adsorb to their host cells [111]. Archaeal coil-shaped virus ACV is the only helical archaeal virus with an ssDNA genome, but its virion organization is considerably different compared to ssDNA inoviruses. In inoviruses, the circular genome forms two antiparallel strands encapsidated by a cylindrical protein shell [17]. In ACV, the capsid protein binds to the circular genome and this nucleoprotein filament forms a pseudo double-helix, which further intertwines into a cylindrical super-helix [55]. Moreover, filamentous and rod-shaped archaeal viruses have an MCP fold characterized by a four-helix bundle, but this arrangement has not been observed in other helical viruses [51,112]. Thus, helical archaeal and bacterial viruses most likely do not have a common ancestor. Viruses without counterparts in the other domains It has been proposed that the last universal common ancestor (LUCA) of cellular life was infected by a number of viruses, and then specific virus groups adapted to infect the evolving cells that deviated to form the current three domains of cellular life [7,113]. Furthermore, it has recently been suggested that bacteria and archaea are infected by such different types of viruses due to the differences in their cell envelope composition [44]. Archaeal viruses display unique morphotypes, which are not found among bacterial or eukaryotic viruses. These include all spindle-shaped viruses as well as coil-, bottle-, and dropletshaped ones. Especially, spindle-shaped viruses are abundant among the known archaeal viruses and in archaearich habitats. Spherical viruses of the family Globuloviridae have counterparts among eukaryotic viruses, namely paramyxoviruses, but not among bacterial ones. By contrast, most bacterial viruses have counterparts among archaeal ones except for tailless icosahedral viruses without a lipid membrane (microviruses and leviviruses) and those having an outer membrane (cystoviruses). Microviruses, leviviruses, and cystoviruses, however, have eukaryotic counterparts [17]. 8

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Box 2. Outstanding questions  How do different archaeal viruses enter their host cells?  What kind of exit mechanisms do nonlytic archaeal viruses use and how do they extrude through the proteinaceous surface layer of archaeal cells?  What morphologies and genome structures will be discovered in viruses infecting non-extremophilic archaea?  Are there RNA viruses infecting archaea?  How many novel morphotypes are there still to be discovered for archaeal viruses?  Are there head-tailed viruses infecting hyperthermophilic crenarchaea?  Are there any new morphotypes to be discovered for bacterial viruses?

Concluding remarks Bacterial viruses have been studied for a century, whereas archaeal ones have only been studied for about 40 years, and thus many questions still remain to be answered (Box 2). Isolated bacteriophages significantly outnumber archaeal viruses. Limited in isolate number, archaeal viruses, however, have revealed many surprises that have changed our understanding of the virosphere. These findings include extraordinary virion morphotypes (spindle-, droplet-, coil-, and bottle-shaped particles) [20,55,58,81,82], a unique virion release mechanism through pyramid-like structures [56], a remarkable virion property in developing tails outside host cells [59], and a unique capsid enlargement strategy [32]. Moreover, morphological studies of archaeal viruses have gained significant attention in recent years with the development of virion-based approaches for viral classification [84,105,106,113]. Archaeal viruses are morphologically more diverse than bacteriophages, and this diversity may originate from the ancient pool of morphotypes associated with LUCA [44]. Recent isolation of about 50 new viruses infecting halophilic archaea, however, revealed only one new morphotype supporting the hypothesis of a limited number of possible viral architectures [6,84]. One of the most intriguing questions for further research is the existence of yet unknown virion types (Box 2). So far, structural studies have mostly focused on icosahedral and helical archaeal viruses. However, more such studies, especially on unusual virion morphotypes, are necessary to understand the phylogenetic position of archaeal viruses in the virosphere. Acknowledgments The authors acknowledge support from the Academy of Finland (Academy Professor funding grants 255342 and 256518 to D.H.B.). We also thank the Academy of Finland (grants 271413 and 272853) and the University of Helsinki for support of the European Union (EU) European Strategy Forum on Research Infrastructures (ESFRI) Instruct Centre for Virus Production. T.A.D. is a University of Helsinki fellow in the Doctoral Program in Microbiology and Biotechnology.

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