Available online at www.sciencedirect.com

ScienceDirect Haloviruses of archaea, bacteria, and eukaryotes Nina S Atanasova, Hanna M Oksanen and Dennis H Bamford Hypersaline environments up to near saturation are rich reservoirs of extremophilic viruses. One milliliter of salt water may contain up to 109 viruses which can also be trapped inside salt crystals. To date, most of the 100 known halovirus isolates infect extremely halophilic archaea, although a few bacterial and eukaryotic viruses have also been described. These isolates comprise tailed and tailless icosahedral, pleomorphic, and lemon-shaped viruses which have been classified according to features such as host range, genome type, and replication. Recent studies have revealed that viruses can be grouped into a few structure-based viral lineages derived from a common ancestor based on conserved virion architectural principles and the major capsid protein fold. Address Department of Biosciences and Institute of Biotechnology, University of Helsinki, Helsinki, Finland Corresponding author: Bamford, Dennis H ([email protected])

Current Opinion in Microbiology 2015, 25:40–48 This review comes from a themed issue on Extremophiles Edited by Haruyuki Atomi and Elizaveta Bonch-Osolovskay

http://dx.doi.org/10.1016/j.mib.2015.04.001 1369-5274/# 2015 Elsevier Ltd. All rights reserved.

Introduction: viruses in high salt Hypersaline environments are distributed all over the world as different salt lakes, salterns, salt plains, and deposits. Extremely halophilic archaea dominate these environments, but different types of bacteria and a few eukaryotes have also been reported [1]. With only a few cellular predators around, halophilic microorganisms are in a constant interplay with viruses that outnumber the cells from ten to hundred fold [2,3]. To date, around 90 viruses have been described for extremely halophilic archaea (Halobacteriaceae family) while only approximately ten viruses are known to infect bacterial halophiles (Figure 1) [Atanasova, Bamford, Oksanen, submitted for publication]. Myoviruses, siphoviruses, and podoviruses, as well as icosahedral internal membrane-containing virus morphotypes are represented by both archaeal and bacterial haloviruses, while pleomorphic and lemon-shaped haloviruses have only been isolated for archaeal hosts (Figure 2). Current information about viruses infecting halophilic eukaryotes is scarce. No viruses have been Current Opinion in Microbiology 2015, 25:40–48

described for halophilic fungi or the green algae Dunaliella salina [1]. The five Marseillevirus-like or Mimiviruslike isolates recently obtained from Tunisian hypersaline environments using laboratory cultures of Acanthamoeba polyphaga, probably represent the only known eukaryotic virus isolates from high salt, albeit the host in this case is halotolerant instead of halophilic (Figures 1,2) [4]. In addition, high numbers of phycodnaviruses of phototrophic algae, as well as virophages attacking these viruses, have been reported from Antarctic hypersaline lakes by metagenomic studies [5]. Perhaps due to the low number of isolates, the genes of the described haloviruses are rarely detected in metaviromes of different hypersaline environments [6] and vice versa, the sequenced haloviral genomes contain numerous orphan genes [7,8]. Although observations based on transmission electron microscopy (TEM) suggest that lemon-shaped virus-like particles are abundant in high salt, until now such viruses have been rarely isolated [9]. Although archaeal haloviruses are currently the most described viruses of extremophiles, very little is known about them compared to all of the known bacterial and eukaryotic viruses [10]. Current estimations predict that the Earth’s oceans contain 1031 virus particles [11]. However, due to physical constraints of protein fold space, only certain folds are capable of making an infectious virion [12]. This suggests that despite the high number of viruses on Earth, and the enormous diversity of viral sequences, the distribution of different virus morphotypes would be relatively narrow. Thus, viruses could be grouped into a few structure-based lineages based on conserved coat protein folds [13,14]. Viruses belonging to a certain lineage represent similar morphotypes and are considered to have a common ancestor [13]. Inspired by the uniqueness of some archaeal viruses, extreme environments are now seen as potential sources for discovering novel virion morphotypes. Taken into account the challenging circumstances of these environments, viruses of extremophiles might give us insights into the limits of life. The conditions of some extreme environments are considered to resemble those of the early Earth suggesting that viruses of extremophiles could be ‘remnants’ of ancient viruses. Here, we summarize the latest knowledge about haloviruses of archaea, bacteria, or eukaryotes in the context of virion morphotypes and structure-based viral lineages.

Haloviruses of archaea To date, close to 130 archaeal viruses, of which 90 (Figure 1a) infect halophilic archaea, have been described www.sciencedirect.com

Viruses of hypersaline environments Atanasova, Oksanen and Bamford 41

Figure 1

Archaeal haloviruses

(a)

Myoviruses (52) Siphoviruses (20) Podoviruses (1) Icosahedral viruses (5) Pleomorphic viruses (11) Lemon-shaped viruses (1)

Bacterial haloviruses

(b) Virus

Origin

Host

Morphology

DNA genome size Reference (bp)

F9-11

Halomonas halophila (Lysogen) Saltern, Canada Alicante, Spain

Halomonas halophila

Siphovirus

ND

Calvo et al., 1988

Pseudomonas sp. G3 Salinivibrio costicola sp. B1 Halomonas sp.

Myovirus Myovirus

ND 80,000

Kauri et al., 1991 Goel et al., 1996

Myovirus

340,000

Seaman and Day, 2007

Salicola sp.

Siphovirus

ND

Salicola sp.

Myovirus

ND

Salicola sp. s3-1

Myovirus

ND

Kukkaro and Bamford, 2009 Kukkaro and Bamford, 2009 Atanasova et al., 2012

Salisaeta sp. SP9-1

Icosahedral with an internal membrane

43,788

Salinivibrio sp. SA50

Podovirus

40,547

Ps-G3 UTAK ΦgspC

SCTP-I SCTP-2 SCTP-3

SSIP-I

CW02

Saline soil, The Great Salt Plains National Wildlife Refuge, USA Salt water, Trapani, Italy Salt water, Trapani, Italy Salt water, Margherita di Savoia, Italy Salt water, Sedom Ponds, Israel The Great Salt Lake, USA

(c)

Atanasova et al., 2012; Aalto et al., 2012 Shen et al., 2012

Eukaryotic haloviruses

Virus

Origin

Host

Morphology

DNA genome size Reference (bp)

Bougl

Salt lake water, Tunisia Salt lake water, Tunisia Saline soil, Tunisia Saline soil, Tunisia Saline soil, Tunisia

A. polyphaga

Mimivirus-like

ND

A. polyphaga

Marseillevirus-like

ND

A. polyphaga

Marseillevirus-like

ND

A. polyphaga

Marseillevirus-like

ND

A. polyphaga

Marseillevirus-like

ND

Sebleau Seblsol Seb2sol Seb6sol

Boughalmi et aI., 2013 Boughalmi et aI., 2013 Boughalmi et aI., 2013 Boughalmi et aI., 2013 Boughalmi et aI., 2013 Current Opinion in Microbiology

The described haloviruses infecting (a) archaea [16] [Atanasova, Bamford, Oksanen, submitted], (b) bacteria [19,37–42], and (c) eukaryotes [4]. (a) Numbers of described archaeal halovirus isolates are shown in the brackets and in the pie chart as percentages of the total number (90) of halovirus isolates. The updated list of archaeal haloviruses can be found from [Atanasova, Bamford, Oksanen, submitted] and [16]. ND, not determined.

(reviewed in [15,16,17,18a]). Most of these viruses resemble bacteriophages of the Caudovirales order having either contractile (myoviruses) or non-contractile tails www.sciencedirect.com

(siphoviruses and podoviruses) and linear double-stranded (ds) DNA genomes (Figure 2) [8,10,18b]. The myovirus morphotype is especially abundant among the Current Opinion in Microbiology 2015, 25:40–48

42 Extremophiles

Figure 2

SH1

HSTV-1 HRPV-1 HSTV-2

100 nm

SCTP-2 SCTP-1 SSIP-1

Boug1

100 nm Seb1sol

ct

us

Ba

es

100 nm

His1

Archaeal viruses

CW02

HVTV-1

s HK97-like

Eu

se

Miscellaneous 2

ka

iru

ryo

lv

tic

ia

vir

er

Miscellaneous 1

PRD1-like Current Opinion in Microbiology

Schematic presentation of the tree of life showing the division of haloviruses based on their morphotypes and hosts in the three domains of life. The large baskets represent the two well-established major structure-based viral lineages (HK97-like and PRD1-like) which include viruses of bacteria, archaea, and eukaryotes (see Figure 3) (Abrescia et al., 2012). The small baskets (Miscellaneous 1 and 2) represent two proposed viral lineages of lemon-shaped and pleomorphic (archaeal) viruses (see Figure 4). Viruses with the HK97 fold (HK97-like) are colored yellow and those with vertical beta barrel fold (PRD1-like) in green. Viruses in the tree are drawn in scale (bar = 100 nm). For space limitation, only part of the halophilic Mimivirus-like, Boug1 (particle diameter = 519 nm), is shown (pointed by an arrow). The position of lipids in the virions is indicated by blue color. (Archaeal head-tailed viruses have only been isolated for euryarchaeal hosts.)

archaeal halovirus isolates. These viruses often have exceptionally broad host ranges covering haloarchaea from different species and genera [18a,19]. Like bacteriophages, Current Opinion in Microbiology 2015, 25:40–48

genomes of the sequenced haloarchaeal tailed viruses are mosaics [8,20]. Interestingly, archaeal icosahedral tailed viruses have only been isolated for haloarchaea or www.sciencedirect.com

Viruses of hypersaline environments Atanasova, Oksanen and Bamford 43

methanogens and none of the known crenarchaea [15,17,18a]. Recent data indicate that in addition to icosahedral tailed viruses, pleomorphic archaeal viruses might be abundant in hypersaline environments (Figure 1). To date, eleven such viruses have been described and eight of them have been characterized in detail [18a,21–23]. Based on these studies, pleomorphic viruses have nonlytic life cycles and are specific to their isolation hosts. HRPV-1, the type virus of the recently proposed virus family ‘Pleolipoviridae’ was the first described archaeal virus with a single-stranded (ss) DNA genome [24]. Most of the archaeal viruses have dsDNA genomes while archaeal RNA viruses are not known [15,17]. The well described eight viruses share a group of genes including those encoding the major structural proteins with gene synteny and amino acid sequence similarity. Interestingly, these viruses have either circular singlestranded, or circular or linear double-stranded DNA genomes challenging the current virus classification (ICTV) [22,25]. In addition, mobile genetic elements related to pleomorphic viruses have been identified in the genomes of several haloarchaea [22]. Pleomorphic viruses have not been described for crenarchaea, but they do resemble certain phages of mycoplasmas as well as membrane vesicles produced by microorganisms [26,27]. Icosahedral prokaryotic viruses with an internal membrane were considered to be rare for a long time. Currently, five such viruses (SH1, PH1, HHIV-2, SNJ1 and HCIV-1) that infect halophilic archaea have been isolated from different parts of the world indicating that these viruses are much more common than previously expected (Figure 1) [18a,28–30]. SH1, PH1, and HHIV2 have a virulent life cycle and their linear dsDNA genomes are related to each other [29,30]. SNJ1 is a temperate virus that is capable of replicating as a plasmid in the cytoplasm of the host [31]. This virus is structurally similar to the other halophilic tailless icosahedral viruses, but does not have significant sequence similarity with the other viruses and due to the circular genome, has different replication and assembly mechanisms [31]. Although several lemon-shaped viruses with variable tail structures have been described for the crenarchaeal hyperthermophiles, His1 is the only known halovirus with this morphology (Figure 1) [32]. The virus does not contain a lipid membrane, but the single major capsid protein (MCP), VP21, is lipid modified [33]. His1 virions are flexible and variable in size [34]. In addition, the virus encodes its own DNA polymerase [32]. It has been suggested, that His1 belongs to the same virus family Fuselloviridae, with the short-tailed crenarchaeal lemonshaped viruses [35]. www.sciencedirect.com

Haloviruses of bacteria It is considered, that halophilic or highly halotolerant bacteria may consist up to 20% of the microbiota in a typical hypersaline environment, such as a solar saltern [36]. Little is known about these bacteria and their viruses are even less studied. To date, less than ten viruses infecting halophilic bacteria from the genera Halomonas, Pseudomonas, Salinivibrio, Salicola, and Salisaeta, have been isolated (Figures 1,2). Morphologically, most of these isolates are myoviruses, but siphoviruses as well as one podovirus and one icosahedral virus with an internal lipid membrane, have also been described (Figures 1,2) [19,37–42]. SCTP-2 is the largest known prokaryotic halovirus with a head diameter of 125 nm and a contractile tail of 145 nm in length. Unfortunately, no information about the genome of this potential jumbo phage [43] is currently available. Both, SCTP-2 as well as the siphovirus SCTP-1 isolated from the same environment, are able to retain more than 50% of the infectivity at salinities ranging from 0 to 4.5 M illustrating the broad salt tolerance of halophilic bacteriophages [40]. The temperate halovirus FgspC was isolated from the Great Salt Plains National Wildlife Refuge approximately a decade ago [38]. With a genome size of 340 kbp, this phage definitely can be classified as a jumbo phage which in addition to the large size, are known for their genomes that encode a high number of proteins with unknown functions [43]. The head diameter of this myovirus is 90 nm which is smaller than that of SCTP-2. It remains to be seen whether this type of phages are common in the high salt. The genome of FgspC may encode genes that improve host (Halomonas salina) fitness at elevated salinity indicating the important role of viruses in extreme environments. The virus itself rapidly loses infectivity at low NaCl concentration [38]. On the contrary, another myovirus, UTAK, isolated from the saltern of Alicante, Spain, remains infective even in the absence of salt [39]. However, the burst size and adsorption are the highest at 1 M salinity while decreasing both below and above this value [39]. The icosahedral internal-membrane containing SSIP-1 and the podovirus CW02 are the only known halophilic bacterial viruses for which detailed structural characterization has been performed by cryo-EM [7,37]. Interestingly, turret structures typical for extremophilic viruses were visualized on the surface of CW02 capsid [37]. SSIP1 is the largest known prokaryotic tailless icosahedral virus [44]. SSIP-1 life cycle is lytic and a gene for putative integrase was identified in the 43.8 kbp circular dsDNA genome [7].

Haloviruses of eukaryotes It is widely considered, that the environments with close to saturated NaCl concentrations are dominated by prokaryotes. However, in the environment, the salinity is Current Opinion in Microbiology 2015, 25:40–48

44 Extremophiles

known to vary a lot even within one niche and the number of eukaryotes increases up on reduction of the salinity. To date very little is known about the abundance and diversity of halophilic or highly halotolerant eukaryotes. Furthermore, up to date no viruses of such microorganisms were known. To the best of our knowledge, the first reported eukaryotic virus isolates from hypersaline aquatic and soil samples were described by Boughalmi et al., in 2013 [4]. All these five virus isolates are giant viruses obtained from Tunisian hypersaline environments. One of them, Boug1, is related to Mimivirus. The virion is 519 nm in diameter and has a dense layer of fibrils attached to the capsid. The other four viruses are Marseillevirus-like with 200 nm particle diameter [4]. The morphology of these viruses was studied by TEM and their similarity to the type viruses was confirmed by analysis of the B type DNA polymerase gene (Mimivirus-like) or MCP gene (Marseillevirus-like) [4]. These viruses were isolated using laboratory cultures of A. polyphaga, which is a halotolerant amoeba. Very little is known about amoebae in hypersaline environments, but they have been commonly observed around the world [45]. It remains to be seen whether more such viruses will be found and whether Dunaliella algae might have viruses such as the phycodnaviruses.

Structural classification of haloviruses To date, four structure-based viral lineages have been established of which the lineages of HK97-like and PRD1-like viruses include viruses that infect hosts residing in all three domains of life [14]. In addition, these two lineages comprise the described haloviruses with icosahedral symmetry. The other two lineages, Picornalike and Blue tongue virus-like, are RNA virus lineages and such viruses have not been described for extremophiles to date [14]. The lambda-like bacteriophage HK97 is the ‘prototype’ member of the HK97-lineage since the canonical HK97 MCP fold (Figure 3a) was initially recognized in this phage [46]. However, it is considered that all icosahedral tailed viruses infecting bacteria and archaea (order Caudovirales) share the same MCP fold indicating common ancestry [18b,47]. During recent years, this canonical fold was identified in the eukaryotic herpes viruses [48] connecting eukaryotic viruses to the HK97-lineage. Comparative genomic analyses about nine archaeal proviruses provided strong support that the fold would be present also in archaeal icosahedral tailed viruses [47]. In 2013, this was proved by the cryo-EM reconstruction of haloarchaeal podovirus HSTV-1 [49]. At the same time, cryo-EM and three-dimensional image reconstruction revealed that also the halophilic bacterial podovirus CW02 capsid uses the HK97 fold [37]. Like CW02, also HSTV-1 capsid includes large turrets. Icosahedral internal membrane-containing viruses of the PRD1-lineage can be divided into two subclasses Current Opinion in Microbiology 2015, 25:40–48

according to the number of MCP species (one or two) the virus uses to build the capsid (Figure 3b,c). All the known archaeal and bacterial haloviruses with this architecture contain two MCP species with a single vertical beta barrel fold. However, currently the only crystal structures of such MCPs have been solved for the Thermus phage P23-77 (Figure 3c) [50]. Mimivirus is known to have one MCP with vertical double beta barrel fold, similar to the type-virus PRD1, indicating that the Mimivirus-like and Marseillevirus-like giant eukaryotic haloviruses are most probably structurally related to PRD1 [4,51]. The asymmetric pleomorphic and lemon-shaped viruses which are considered abundant in hypersaline environments are challenging for high resolution structural studies due to the lack of virion symmetry. Based on the current information concerning these viral structures, it is possible that both virus morphotypes represent a distinct lineage based on a unique MCP fold (Figures 2,4). Pleomorphic viruses have a simple architecture consisting of a membrane vesicle decorated by spike proteins (Figure 4). These viruses also have an internal membrane protein and a genome free of nucleoproteins [21,52]. His1 has a lemon-shaped virion architecture including a uniform short tail structure with six tail spikes (Figure 4) [34]. It is considered that the virus uses the tail complex for attachment and genome release to the host cell. His1 virion size is variable and the dynamic virion can transform into a tube which possibly facilitates the DNA injection [34]. The virus is very resistant to environmental changes. The single MCP of His1 is lipid-modified and related to the MCP of fusellovirus SSV1 [33]. His1 is suggested to belong to a common lineage with the crenarchaeal short-tailed fuselloviruses.

Conclusions To date, more than 100 haloviruses have been described for mostly archaeal, but also bacterial, or eukaryotic hosts. These viruses comprise six different morphotypes, myoviruses, siphoviruses, and podoviruses, as well as icosahedral internal membrane-containing, pleomorphic, and lemon-shaped viruses. So far, the last two morphotypes are specific for archaeal viruses. The structure-based viral lineages are based on conserved virion structural principles and the MCP fold. Although sequence-based comparisons can detect relatedness between viruses that are closely related, structure-based classification aims to identify relationships between structurally similar viruses that can infect very different hosts and have little or no detectable sequence similarity. It is considered, that the viruses within a lineage have a common ancestor. For instance, MCP folds of the tailless icosahedral viruses (PRD1-like) and the icosahedral tailed viruses (HK97-like) are shared by viruses infecting cells from any of the three domains of life and www.sciencedirect.com

Viruses of hypersaline environments Atanasova, Oksanen and Bamford 45

Figure 3

(a) Lineage of HK97-like viruses

HK97 (T=7)

HK97 gp5

(b) Lineage of PRD1-like viruses: viruses with vertical double beta-barrel MCP fold (1 MCP)

PRD1 (T=25)

PBCV-1(T=169)

PRD1 P3

PBCV-1 Vp54

(c) Lineage of PRD1-like viruses: viruses with vertical single beta-barrel MCP fold (2 MCPs)

P23-77 (T=28)

P23-77 Vp16

P23-77 Vp17 Current Opinion in Microbiology

Description of the two major viral lineages that are defined by the canonical HK97 and PRD1 MCP folds and that contain icosahedrally symmetric haloviruses. Morphotypes, 3D reconstruction of the capsids, and MCP fold(s) are shown from left to right. (a) HK97-like viruses. (b) PRD1-like viruses with one MCP-encoding gene. (c) PRD1-like viruses with two MCP-encoding genes. Viruses are not in scale. The approximate sizes of the virions are indicated by the triangulation number (T) shown below the capsid. Icosahedral five-fold vertex positions are indicated by blue. The peripentonal capsomers of PBCV-1 are colored in green for clarity. Capsid 3D isosurface representations and MCP folds were constructed using UCSF Chimera 1.10.1. PDB IDs are 1OHG, 1W8X, 1M3Y, and 3ZN6 for HK97, PRD1, PBCV-1, and P23-77, respectively. EMD accession code for P23-77 is 1525. www.sciencedirect.com

Current Opinion in Microbiology 2015, 25:40–48

46 Extremophiles

Figure 4

(a)

(b)

100 nm

100 Å 40 270 350 420 Current Opinion in Microbiology

Schematic models, tomograms, and 3D representations of asymmetric haloviruses (from left to right). (a) Pleomorphic halovirus HRPV-1. Lipid membrane is indicated by blue in the schematic representation. The arrow points at the isosurface representation of a separated spike (Copyright# American Society for Microbiology, [Journal of Virology 86, pp. 5067–5079, doi: 10.1128/JVI.06915-11]). (b) Lemon-shaped halovirus His1. Lipid modification of the MCP is indicated by blue dashed line. Top and side views of the virion 3D reconstruction is shown on the right as well as the radially colored 6-fold symmetrized map (Copyright# National Academy of Sciences (USA) [PNAS, doi: 10.1073/pnas.1425008112]). Scale bar is 100 nm for both tomograms.

these lineages comprise the icosahedral haloviruses. To date, high resolution structures are available for only few haloviruses. All the prokaryotic PRD1-like haloviruses have two MCP species indicating that this type of capsid architecture may be advantageous in extremely halophilic environments. The asymmetric viruses are challenging for symmetry-based structural virus classification. More research is needed, as extremophilic viruses represent virion architectures that are infectious at the limits of life.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:  of special interest  of outstanding interest 1.

Oren A: Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Systems 2008, 4:2-13.

2.

Narasingarao P, Podell S, Ugalde JA, Brochier-Armanet C, Emerson JB, Brocks JJ, Heidelberg KB, Banfield JF, Allen EE: De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J 2012, 6:81-93.

3.

Rodrı´guez-Valera F, Martin-Cuadrado AB, Rodriguez-Brito B, Pasic´ L, Thingstad FD, Rohwer F, Mira A: Explaining microbial population genomics through phage predation. Nat Rev Microbiol 2009, 7:828-1828.

4. 

Boughalmi M, Saadi H, Pagnier I, Colson P, Fournous G, Raoult D, La Scola B: High-throughput isolation of giant viruses of the

Acknowledgements Janne J. Ravantti is thanked for the help in creating 3D isosurface representations of virus capsids. We thank Academy of Finland (grants 271413 and 272853) and University of Helsinki for the support to EU ESFRI Instruct Centre for Virus Production (ICVIR). We also wish to acknowledge Academy of Finland for support (Academy Professor funding grants 256518, 283072 and 255342 to D.H.B.). Current Opinion in Microbiology 2015, 25:40–48

www.sciencedirect.com

Viruses of hypersaline environments Atanasova, Oksanen and Bamford 47

Mimiviridae and Marseilleviridae families in the Tunisian environment. Environ Microbiol 2013, 15:2000-2007. Using a high throughput method to detect amoebae lysis on agar plates, the authors describe the isolation of 11 new Marseillevirus-like and four new Mimivirus-like isolates from 1000 Tunisian environmental samples including hypersaline samples. TEM micrographs, phylogenetic analysis, and description of the isolation method are provided. 5.

Yau S, Lauro FM, DeMaere MZ, Brown MV, Thomas T, Raftery MJ, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Gibson JA et al.: Virophage control of antarctic algal host-virus dynamics. Proc Natl Acad Sci U S A 2011, 108:6163-6168.

6.

Emerson JB, Thomas BC, Andrade K, Allen EE, Heidelberg KB, Banfield JF: Dynamic viral populations in hypersaline systems as revealed by metagenomic assembly. Appl Environ Microbiol 2012, 78:6309-6320.

7.

Aalto AP, Bitto D, Ravantti JJ, Bamford DH, Huiskonen JT, Oksanen HM: Snapshot of virus evolution in hypersaline environments from the characterization of a membranecontaining Salisaeta icosahedral phage 1. Proc Natl Acad Sci U S A 2012, 109:7079-7084.

8.

Sencˇilo A, Roine E: A glimpse of the genomic diversity of haloarchaeal tailed viruses. Front Microbiol 2014, 5:84.

9.

Sime-Ngando T, Lucas S, Robin A, Tucker KP, Colombet J, Bettarel Y, Desmond E, Gribaldo S, Forterre P, Breitbart M et al.: Diversity of virus–host systems in hypersaline Lake Retba, Senegal. Environ Microbiol 2011, 13:1956-1972.

10. Ackermann HW, Prangishvili D: Prokaryote viruses studied by electron microscopy. Arch Virol 2012, 157:1843-1849. 11. Suttle CA: Marine viruses — major players in the global ecosystem. Nat Rev Microbiol 2007, 5:801-812. 12. Krupovicˇ M, Bamford DH: Order to the viral universe. J Virol 2010, 84:12476-12479. 13. Bamford DH: Do viruses form lineages across different domains of life? Res Microbiol 2003, 154:231-236. 14. Abrescia NG, Bamford DH, Grimes JM, Stuart DI: Structure  unifies the viral universe. Annu Rev Biochem 2012, 81:795-822. The authors present a comprehensive and detailed synopsis of the structure-based viral lineage concept in which viruses are classified into lineages based on conserved architectural principles of the virion. The authors highlight future opportunities for high-throughput classification of the virosphere. 15. Prangishvili D: The wonderful world of archaeal viruses. Annu  Rev Microbiol 2013, 67:565-585. The author presents a collective review of the current knowledge on archaeal viruses in the context of new viral species and morphotypes concentrating more specifically on viruses infecting crenarchaea. 16. Luk AW, Williams TJ, Erdmann S, Papke RT, Cavicchioli R: Viruses  of haloarchaea. Life (Basel) 2014, 4:681-715. The authors present an overview of viruses infecting halophilic archaea including substantial information on virus classification, morphotypes, genetic manipulation, and virus–host interactions. The review includes collective tables and figures of the described haloviruses. 17. Pietila¨ MK, Demina TA, Atanasova NS, Oksanen HM, Bamford DH: Archaeal viruses and bacteriophages: comparisons and contrasts. Trends Microbiol 2014, 22:334-344. 18. (a). Atanasova NS, Demina TA, Buivydas A, Bamford DH, Oksanen HM: Archaeal viruses multiply: temporal screening in a solar saltern. Viruses 2015, 7:1902-1926; (b). Pietila¨ MK, Laurinma¨ki P, Russell DA, Ko CC, Jacobs-Sera D, Butcher SJ, Bamford DH, Hendrix RW: Insights into head-tailed viruses infecting extremely halophilic archaea. J Virol 2013, 87:3248-3260. 19. Atanasova NS, Roine E, Oren A, Bamford DH, Oksanen HM:  Global network of specific virus–host interactions in hypersaline environments. Environ Microbiol 2012, 14:426-440. A study describing new halovirus isolates doubling the number of previously described ones. The large scale global distribution of virus–host interactions was also introduced. In addition, the broad host ranges of haloarchaeal myoviruses were described. www.sciencedirect.com

20. Sencˇilo A, Jacobs-Sera D, Russell DA, Ko CC, Bowman CA, Atanasova NS, O¨sterlund E, Oksanen HM, Bamford DH, Hatfull GF et al.: Snapshot of haloarchaeal tailed virus genomes. RNA Biol 2013, 10:803-816. 21. Pietila¨ MK, Atanasova NS, Manole V, Liljeroos L, Butcher SJ, Oksanen HM, Bamford DH: Virion architecture unifies globally distributed pleolipoviruses infecting halophilic archaea. J Virol 2012, 86:5067-5079. 22. Sencˇilo A, Paulin L, Kellner S, Helm M, Roine E: Related haloarchaeal pleomorphic viruses contain different genome types. Nucleic Acids Res 2012, 40:5523-5534. 23. Li M, Wang R, Zhao D, Xiang H: Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process. Nucleic Acids Res 2014, 42:24832492. 24. Pietila¨ MK, Roine E, Paulin L, Kalkkinen N, Bamford DH: An ssDNA virus infecting archaea: a new lineage of viruses with a membrane envelope. Mol Microbiol 2009, 72:307-319. 25. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (Eds): Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. London: Elsevier Academic Press; 2012. 26. Soler N, Krupovicˇ M, Marguet E, Forterre P: Membrane vesicles  in natural environments: a major challenge in viral ecology. ISME J 2015, 9:793-796. The authors comment on the potential roles of extracellular membrane vesicles that are universally produced by different microorganisms in the environment. The relatedness of such vesicles to viruses or virus-like elements is discussed. 27. Atanasova NS, Sencˇilo A, Pietila¨ MK, Roine E, Oksanen HM, Bamford DH: Comparison of lipid-containing bacterial and archaeal viruses. Adv Virus Res 2015, 92:1-61. 28. Porter K, Kukkaro P, Bamford JK, Bath C, Kivela¨ HM, DyallSmith ML, Bamford DH: SH1: a novel, spherical halovirus isolated from an Australian hypersaline lake. Virology 2005, 335:22-33. 29. Jaakkola ST, Penttinen RK, Vilen ST, Jalasvuori M, Ro¨nnholm G, Bamford JK, Bamford DH, Oksanen HM: Closely related archaeal Haloarcula hispanica icosahedral viruses HHIV-2 and SH1 have nonhomologous genes encoding host recognition functions. J Virol 2012, 86:4734-4742. 30. Porter K, Tang SL, Chen CP, Chiang PW, Hong MJ, Dyall-Smith M: PH1: an archaeovirus of Haloarcula hispanica related to SH1 and HHIV-2. Archaea 2013:456318. 31. Zhang Z, Liu Y, Wang S, Yang D, Cheng Y, Hu J, Chen J, Mei Y, Shen P, Bamford DH et al.: Temperate membrane-containing halophilic archaeal virus SNJ1 has a circular dsDNA genome identical to that of plasmid pHH205. Virology 2012, 434:233-241. 32. Bath C, Cukalac T, Porter K, Dyall-Smith ML: His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus. Virology 2006, 350:228-239. 33. Pietila¨ MK, Atanasova NS, Oksanen HM, Bamford DH: Modified coat protein forms the flexible spindle-shaped virion of haloarchaeal virus His1. Environ Microbiol 2013, 15:1674-1686. 34. Hong C, Pietila¨ MK, Fu CJ, Schmid MF, Bamford DH, Chiu W:  Lemon-shaped halo archaeal virus His1 with uniform tail but variable capsid structure. Proc Natl Acad Sci U S A 2015, 112:2449-2454. The authors provide the first detailed structural characterization of the haloarchaeal lemon-shaped virus (His1) based on cryo-electron tomography, subtomogram averaging, and biochemical dissociation analyses. The virus is shown to possess a unique capacity of transforming the capsid into a tube-like structure possibly involved in DNA injection. 35. Krupovicˇ M, Quemin ER, Bamford DH, Forterre P, Prangishvili D: Unification of the globally distributed spindle-shaped viruses of the Archaea. J Virol 2014, 88:2354-2358. 36. Ghai R, Pasic´ L, Fernandez AB, Martin-Cuadrado AB, Mizuno CM, McMahon KD, Papke RT, Stepanauskas R, Rodriguez-Brito B, Rohwer F et al.: New abundant microbial groups in aquatic hypersaline environments. Sci Rep 2011, 1:135. Current Opinion in Microbiology 2015, 25:40–48

48 Extremophiles

37. Shen PS, Domek MJ, Sanz-Garcia E, Makaju A, Taylor RM, Hoggan R, Culumber MD, Oberg CJ, Breakwell DP, Prince JT et al.: Sequence and structural characterization of great salt lake bacteriophage CW02, a member of the T7-like supergroup. J Virol 2012, 86:7907-7917. 38. Seaman PF, Day MJ: Isolation and characterization of a bacteriophage with an unusually large genome from the Great Salt Plains National Wildlife Refuge, Oklahoma, USA. FEMS Microbiol Ecol 2007, 60:1-13. 39. Goel U, Kauri T, Ackermann HW, Kushner DJ: A moderately halophilic Vibrio from a Spanish saltern and its lytic bacteriophage. Can J Microbiol 1996, 42:1015-1023. 40. Kukkaro P, Bamford DH: Virus–host interactions in environments with a wide range of ionic strenghts. Environ Microbiol Rep 2009, 1:71-77. 41. Kauri T, Ackermann HW, Goel U, Kushner DJ: A bacteriophage of a moderately halophilic bacterium. Arch Microbiol 1991, 156:435-438. 42. Calvo C, Garcı´a de la Paz A, Bejar V, Quesada E, RamosCormenzana A: Isolation and characterization of phage F9-11 from a lysogenic Deleya halophila strain. Curr Microbiol 1988, 17:49-53. 43. Hendrix RW: Jumbo bacteriophages. Curr Top Microbiol Immunol 2009, 328:229-240. 44. Poranen MM, Bamford DH, Oksanen HM: Membrane-containing bacteriophages. Encyclopedia of Life Sciences (ELS). Chichester: John Wiley & Sons, Ltd.; 2015:. 10.1002/ 9780470015902.a0000779.pub3. 45. Park JS, Simpson AGB: Characterization of halotolerant Bicosoecida and Placididea (Stramenopila) that are distinct

Current Opinion in Microbiology 2015, 25:40–48

from marine forms, and the phylogenetic pattern of salinity preference in heterotrophic stramenopiles. Environ Microbiol 2010, 12:1173-1184. 46. Wikoff WR, Liljas L, Duda RL, Tsuruta H, Hendrix RW, Johnson JE: Topologically linked protein rings in the bacteriophage HK97 capsid. Science 2000, 289:2129-2133. 47. Krupovicˇ M, Forterre P, Bamford DH: Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. J Mol Biol 2010, 397:144-160. 48. Baker ML, Jiang W, Rixon FJ, Chiu W: Common ancestry of herpesviruses and tailed DNA bacteriophages. J Virol 2005, 79:14967-14970. 49. Pietila¨ MK, Laurinma¨ki P, Russell DA, Ko CC, Jacobs-Sera D, Hendrix RW, Bamford DH, Butcher SJ: Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story. Proc Natl Acad Sci U S A 2013, 110:10604-10609. 50. Rissanen I, Grimes JM, Pawlowski A, Ma¨ntynen S, Harlos K, Bamford JK, Stuart DI: Bacteriophage P23-77 capsid protein structures reveal the archetype of an ancient branch from a major virus lineage. Structure 2013, 21:718-726. 51. Xiao C, Kuznetsov YG, Sun S, Hafenstein SL, Kostyuchenko VA, Chipman PR, Suzan-Monti M, Raoult D, McPherson A, Rossmann MG: Structural studies of the giant mimivirus. PLoS Biol 2009, 7:e92. 52. Pietila¨ MK, Laurinavicˇius S, Sund J, Roine E, Bamford DH: The single-stranded DNA genome of novel archaeal virus Halorubrum pleomorphic virus 1 is enclosed in the envelope decorated with glycoprotein spikes. J Virol 2010, 84:788-798.

www.sciencedirect.com