Advertisement

Archives of Virology

, Volume 160, Issue 7, pp 1851–1874 | Cite as

Past, present, and future of arenavirus taxonomy

  • Sheli R. Radoshitzky
  • Yīmíng Bào
  • Michael J. Buchmeier
  • Rémi N. Charrel
  • Anna N. Clawson
  • Christopher S. Clegg
  • Joseph L. DeRisi
  • Sébastien Emonet
  • Jean-Paul Gonzalez
  • Jens H. Kuhn
  • Igor S. Lukashevich
  • Clarence J. Peters
  • Victor Romanowski
  • Maria S. Salvato
  • Mark D. Stenglein
  • Juan Carlos de la Torre
Virology Division News

Abstract

Until recently, members of the monogeneric family Arenaviridae (arenaviruses) have been known to infect only muroid rodents and, in one case, possibly phyllostomid bats. The paradigm of arenaviruses exclusively infecting small mammals shifted dramatically when several groups independently published the detection and isolation of a divergent group of arenaviruses in captive alethinophidian snakes. Preliminary phylogenetic analyses suggest that these reptilian arenaviruses constitute a sister clade to mammalian arenaviruses. Here, the members of the International Committee on Taxonomy of Viruses (ICTV) Arenaviridae Study Group, together with other experts, outline the taxonomic reorganization of the family Arenaviridae to accommodate reptilian arenaviruses and other recently discovered mammalian arenaviruses and to improve compliance with the Rules of the International Code of Virus Classification and Nomenclature (ICVCN). PAirwise Sequence Comparison (PASC) of arenavirus genomes and NP amino acid pairwise distances support the modification of the present classification. As a result, the current genus Arenavirus is replaced by two genera, Mammarenavirus and Reptarenavirus, which are established to accommodate mammalian and reptilian arenaviruses, respectively, in the same family. The current species landscape among mammalian arenaviruses is upheld, with two new species added for Lunk and Merino Walk viruses and minor corrections to the spelling of some names. The published snake arenaviruses are distributed among three new separate reptarenavirus species. Finally, a non-Latinized binomial species name scheme is adopted for all arenavirus species. In addition, the current virus abbreviations have been evaluated, and some changes are introduced to unequivocally identify each virus in electronic databases, manuscripts, and oral proceedings.

Keywords

Arenavirid Arenaviridae Arenavirus Bat virus Bibdavirus ICTV Inclusion body disease International Committee on Taxonomy of Viruses Mammarenavirus PASC Reptarenavirus Rodent virus Snake virus TaxoProp Viral hemorrhagic fever Virus classification Virus nomenclature Virus taxonomy 

Introduction

Mammalian arenavirions are enveloped and spherical to pleomorphic in shape, ranging from 50 to 300 nm in diameter (Fig. 1; reviewed in references [28, 40, 71, 98]). The particles’ sandy appearance in electron microscopy sections, originally thought to be due to the incorporation of host cell ribosomes, earned these viruses their name (Latin arena = sand). The mammalian arenavirus genome consists of two single-stranded ambisense RNA molecules, designated L (large) and S (small). Purified arenavirion RNA is not infectious. The 5’ and 3’ ends of the L and S RNA segments have noncoding untranslated regions (UTRs) and contain conserved reverse complementary sequences of 19 to 30 nucleotides at each extremity [8]. These termini are predicted to form panhandle structures through base pairing [65, 120, 144]. The 3’ UTR of each segment contains the arenaviral genomic promoter that directs RNA replication and gene transcription (Fig. 2) [66, 107].
Fig. 1

(A) Electron micrographs of arenavirus particles emerging from an infected cell [125]; (B) Sucrose-gradient-purified and negatively stained arenavirus particles; (C, D) Ultrathin sections of arenavirus-infected Vero cells. Surface projections on arenavirus particles (panels B and C) and a budding membrane site within an arenavirus-infected cell (panel D) are indicated by arrows [88]

Fig. 2

Schematic diagrams of an arenavirus particle (A) and the organization of the bi-segmented arenavirus L and S RNA genome segments (B). The 5’ and 3’ ends of both segments are complementary at their termini, likely promoting the formation of circular RNPs within the arenavirion, as illustrated for the L RNP in panel A and in reference [144]

Each mammalian arenaviral genomic segment encodes two different proteins in two nonoverlapping open reading frames (ORF) of opposite polarities (ambisense coding arrangement) [9]. The L segment (≈7,200 nt) encodes a viral RNA-dependent RNA polymerase (L) and a zinc-binding matrix protein (Z) [121]. The S segment (≈3,500 nt) encodes a nucleoprotein (NP) and an envelope glycoprotein precursor (GPC) [26, 79, 83]. The two ORFs in each segment are separated by an intergenic noncoding region (IGR) that could form one or more energetically stable stem-loop (hairpin) structures [9, 143]. The IGR functions in structure-dependent transcription termination [96, 97, 132] and in virus assembly and/or budding [111].

Mammalian arenavirus mRNAs are capped and not polyadenylated [96, 126, 127]. The 5’ ends of viral mRNAs contain several nontemplated bases, resembling the mRNAs of influenza A viruses and bunyaviruses [62, 96, 112]. The mammalian arenaviral transcription-initiation mechanism resembles the cap-snatching mechanism of influenza A viruses and bunyaviruses and involves cleavage of the caps and associated bases by an endonuclease activity associated with the L polymerase [112]. The cap leader is subsequently used to prime transcription of the arenavirus genome.

NP is the mammalian arenaviral major structural protein. The protein is a component of nucleocapsids and is associated with viral RNA in the form of bead-like structures. NP is essential for both transcription and replication [107, 110]. Like other RNA-dependent RNA polymerases, L carries out two different processes: transcription and replication [61, 62, 63, 77, 85]. The matrix protein Z contains a zinc-binding RING motif [121, 122, 123] and is the main driving force for mammalian arenavirus budding [54, 107, 130]. Z also inhibits RNA synthesis in a dose-dependent manner [44, 45, 46, 64, 76, 87]. GP1 and GP2, the two envelope glycoproteins, are derived from posttranslational cleavage of GPC. GP1 and GP2 together with a stable signal peptide (SSP), cleaved off during GPC synthesis, form the virion spike that mediates attachment and fusion with host membranes.

During infection, mammalian arenaviruses attach to cell-surface receptors and are internalized by endocytosis [16, 90, 136]. pH-dependent fusion with late endosomes releases the virus ribonucleoprotein (RNP) complex containing NP, L, and viral genomic RNA into the cytoplasm, where the RNP directs both RNA genome replication and gene transcription [98]. During replication, L reads through the IGR transcription-termination signal and generates uncapped antigenomic and genomic RNAs [84]. These RNAs contain a single nontemplated G at the 5’ end [62, 112]. Consequently, replication initiation might involve a slippage mechanism of L on the nascent RNA [63]. Transcription of GPC and Z mRNAs occurs only after one round of virus replication, during which S and L antigenomes are produced. The GPC polyprotein is synthesized into the lumen of the endoplasmic reticulum (ER), where it is extensively N-glycosylated, and where it is thought to oligomerize prior to proteolytic processing by the subtilisin kexin-isozyme-1/site-1 protease (SKI-1/S1P). Proteolytic maturation of GPC, as well as its trafficking from the ER to the cell surface, is dependent on the SSP [112]. Virion budding occurs from the cellular plasma membrane, thereby providing the virion envelope [48, 54, 107, 130].

Past developments in arenavirus taxonomy

In 1933, Armstrong and Lillie discovered the “virus of experimental lymphocytic choriomeningitis” [7], today known as lymphocytic choriomeningitis virus (LCMV). In 1935, Traub identified the house mouse (Mus musculus) as LCMV’s natural reservoir host [134]. Around the same time, Rivers and McNair Scott demonstrated that LCMV is the cause of an aseptic meningitis in humans that today is called lymphocytic choriomeningitis [93, 114, 115]. In 1956, a novel agent later called Tacaribe virus (TCRV) was isolated from Jamaican fruit-eating bats (Artibeus jamaicensis trinitatis) in Trinidad and Tobago, but the virus was not associated with overt human disease [52] (anecdotal reports suggest a single human infection that resulted in a mild febrile illness). In 1959, Junín virus (JUNV), maintained in nature by drylands lauchas (Calomys musculinus), was identified as the cause of Junín/Argentinian hemorrhagic fever [105, 106].

In 1963, Mettler et al. established the “Tacaribe antigenic group” after demonstrating a serological relationship between TCRV and JUNV using the complement fixation test and differences between the viruses using a neutralization assay [94]. Machupo virus (MACV), isolated from a patient with Machupo/Bolivian hemorrhagic fever in 1963 [72], was also found to be antigenically closely related to JUNV by complement fixation tests [140]. In nature, MACV was found to be carried by big lauchas (Calomys callosus) [73]. In the following years, the “Tacaribe antigenic group” expanded to include additional newly discovered viruses: Amaparí (AMAV) [109], Latino (LATV, first mentioned in reference [101]), Paraná (PARV) [139], Pichindé (PICV) [133], and Tamiami viruses (TAMV) [36]. None of these viruses are known to cause human disease (although there are anecdotal reports of two severe PICV infections in humans), but all of them were found to be maintained in nature by specific rodent hosts.

Next, LCMV and the Tacaribe complex viruses were proposed to constitute a new taxonomic group of viruses, tentatively named “Arenoviruses” (later corrected to “Arenaviruses”) [117]. This proposal was based on the similar morphology and morphogenesis of LCMV and the Tacaribe complex viruses [100, 101] and cross-serological reactivity between them in indirect immunofluorescence assays [118]. In 1969, a novel arenavirus later named Lassa virus (LASV) was recovered from Lassa fever patients in Nigeria [58]. Soon after, in 1970, LASV was demonstrated to be antigenically related to LCMV and to some of the Tacaribe complex viruses [30], and LASV’s morphology was found to resemble that observed for LCMV [128]. Taken together, the morphological, physicochemical, and serological properties of all of these viruses became the basis for a formal proposal and the definition of the “arenavirus group,” with LCMV as the (proto)type virus.

In addition to the morphological and serological criteria for the grouping, several of the viruses were noted to have similar limited geographical distributions, ecological associations with specific rodent hosts (with the exception of TCRV), and abilities to induce clinically similar infectious diseases with fever and/or hemorrhagic manifestations. In 1971, the taxon Arenavirus (at the time not italicized) was approved at the genus level by the International Committee on Nomenclature of Viruses (ICNV) [141], the predecessor of the International Committee on Taxonomy of Viruses (ICTV). In 1976, the family Arenaviridae (at the time not italicized) was established to include the genus Arenavirus (not italicized) with LCMV and Tacaribe complexes recognized [56]. Further developments and highlights of arenavirus taxonomy as accepted by the ICTV throughout the years are summarized in Table 1.
Table 1

History of arenavirus taxonomy (typography as used in the ICTV Reports)

Years

Highlights and developments

Newly recognized arenaviruses/arenavirus species

Until 1971 (prior to 1st ICTVa Report) [117, 118]

Morphological similarities between lymphocytic choriomeningitis, Junín, and Machupo virions led to the establishment of the taxonomic “LCM group”, later renamed “arenoviruses”

 

1971-1976 (1st ICTVa Report) [141]

• Spelling of “arenoviruses” corrected to “arenaviruses,” and genus Arenavirus established

• Lymphocytic choriomeningitis virus or “Arenavirus m-1” selected as “type species”

• Virion morphology characterized

• Taxon inclusion criteria: serology-based group-specific antigen recognition by immunofluorescence/complement fixation

Amapari virus [sic]

Junin virus [sic]

Lassa virus

Latino virus

lymphocytic choriomeningitis virus

Machupo virus

Parana virus [sic]

Pichinde virus [sic]

Pistillo virusb

Tacaribe virus

Tamiani virus [sic]

1976-1979 (2nd ICTV Report) [56]

Family Arenaviridae established

• Tacaribe complex recognized and separated from Lassa virus

• Spelling of “Tamiani virus” corrected to Tamiami virus

• “Species” Pistillo virus deleted

• Nature of genomic material described

• Recognition of specific rodent hosts with persistent infection for each arenavirus

None

1979-1982 (3rd ICTV Report) [91]

• Genus name now italicized (Arenavirus)

• Description of physiochemical properties and virion properties (virus nucleic acids and proteomics)

• Some information on the arenavirus lifecycle elucidated

• Description of antigenic properties used for classification and definition of species and complexes

• Introduction of the terms “Old World arenaviruses” (for the LCMV-LASV complex) and “New World arenaviruses” (for the Tacaribe complex)

• Characterization of host range and mode of transmission

None

Tentative: Mozambique virus, Flescal virus [sic]

1982-1991 (4th ICTV Report) [92]

• Family name now italicized (Arenaviridae)

• Incorporation of further details on arenavirus lifecycle and arenavirion properties

• Spelling of “Flescal virus” corrected to “Flexal virus”

None

1991-1995 (5th ICTV Report) [59]

• Clear division into two separate serogroups: LCMV-LASV complex and Tacaribe complex

• Mozambique virus absorbed in “species” Mopeia virus

• “Machupo virus” misspelled as “Macupo virus”

Flexal virus

Ippy virus

Mobala virus

Mopeia virus

1995-2000 (6th ICTV Report) [27]

• “Species” name abbreviations are assigned

• GenBank sequence accession numbers are included, and taxonomic structure of the genus is based on both serology- and sequence-based analyses

• “Species” Latino virus is removed

Guanarito virus

SPH 114202 virus

Tentative: Sabio virus [sic]

2000-2005 (7th ICTV Report) [43]

• Species names now italicized (all virus names introduced previously were copied and introduced as species names)c

• Species (and virus name) corrections: Junin virus→Junín virus; Parana virus→Paraná virus

• SPH 114202 virus and “Sabio virus” combined, and “Sabio virus” corrected to “Sabiá virus”

• New World arenaviruses subdivided into Clades A-C

• Virus strains and serotypes associated with genomic sequence information

• Indication of natural hosts and their geographic distribution

• Phylogenetic relationships within the family are based on the nucleic acid sequence of the N gene

• Species demarcation criteria are based on association with a specific host, geographic distribution, ability to cause human disease, differences in antigenic cross-reactivity, and amino acid sequence divergence

Latino virus

Oliveros virus

Pirital virus

Sabiá virus

Whitewater Arroyo virus

Tentative: Pampa virus

2005-2011 (8th ICTV Report) [55]

• Viruses and species now differentiated

• Genome sequencing of Bear Canyon, Tamiami, and Whitewater Arroyo viruses sparks discussion whether they are recombinants of ancestral arenaviruses from different lineages

Allpaahuayo virus [sic] (species Allpaahuayo virus [sic])

Bear Canyon virus (species Bear Canyon virus)

Cupixi virus (species Cupixi virus)

Tentative: Rio Cacarana virus [sic]d

2011-present (9th ICTV Report and ICTV updates) [1, 2, 74]

• Pampa virus absorbed in Oliveros virus (species Oliveros virus)

• “Allpaahuayo virus” and “Allpaahuayo virus” corrected to “Allpahuayo virus” and “Allpahuayo virus,” respectively

• Species demarcation criterion is specified to at least 12 % in the NP amino acid sequence

Chapare virus (species Chapare virus)

Lujo virus (species Lujo virus)

Luna virus (species Luna virus)

Tentative: Dandenong virus, Kodoko virus, Merino Walk virus

aAt the time called the International Committee on Nomenclature of Viruses (ICNV)

bThe origin of this name is unclear

cNote that, from that moment on, species (concepts of the mind) and viruses (physical entities) were clearly distinguished conceptually by the ICTV but not necessarily by ICTV study groups. This distinction is still not widely understood. Hence, in the 7th ICTV Report, species are listed as viruses rather than as taxa and therefore erroneously received abbreviations

dThe sequence of the Río Carcarañá virus S RNA was determined, but virus could not be isolated and the sample was lost. Consequently, this virus was dropped from the list of classifiable arenaviruses (Victor Romanowski, personal communication)

Current arenavirus taxonomy

As of January 21, 2014, the family Arenaviridae includes a single genus, Arenavirus, which includes 25 approved species (Table 2) [1, 124]. Historically, based on antigenic properties and geographical distribution (with the exception of LCMV ubiquity), the 30 members of these 25 species were divided into two distinct groups. Old World arenaviruses (“Lassa–lymphocytic choriomeningitis serocomplex”) include viruses indigenous to Africa, and the ubiquitous LCMV, and New World arenaviruses (“Tacaribe serocomplex”) include viruses indigenous to the Americas [17, 31, 42, 118]. Subsequent phylogenetic analysis based on sequences of the NP genes of all arenaviruses has provided support for the previously defined antigenic grouping and further defines virus relationships. Sequence data derived from other regions of arenavirus genomes, if available, are largely consistent with this analysis. The 30 member viruses of the 25 species represent four to five phylogenetic groups. The Old World arenaviruses form one monophyletic group that is deeply rooted to three or four New World arenavirus groups [4, 18, 19, 138]. Among the Old World viruses, LASV, Mobala virus (MOBV), and Mopeia virus (MOPV) are monophyletic, while Ippy virus (IPPYV) and LCMV are more distantly related. The recently discovered Lujo virus (LUJV), most likely endemic in Zambia, is most closely related to Old World viruses but contains elements of New World sequences in its GP gene [25].
Table 2

Current arenavirus classification (ICTV-approved and ratified species names) [1, 2, 29, 32, 37, 40, 41, 42, 49, 71, 74, 82, 102, 119, 124]

Virus species name

Species member(s): virus (virus abbreviation)

Geographic virus distribution

Natural host reservoir (species name)

OLD WORLD ARENAVIRUSES

Ippy virus

Ippy virus (IPPYV)

Central African Republic

unstriped grass rats ( Arvicanthis spp. Lesson, 1842) a; soft-furred mice (Praomys spp. Thomas, 1915)

Lassa virus

Lassa virus (LASV)

Western Africa

Natal mastomys (Mastomys natalensis b Smith, 1834)

Lujo virus

Lujo virus (LUJV)

Zambia

unknown

Luna virus

Luna virus (LUNV)

Southern Africa, Zambia

Natal mastomys (Mastomys natalensis b Smith, 1834)

Lymphocytic choriomeningitis virus

lymphocytic choriomeningitis virus (LCMV)

worldwide

house mice ( Mus ( Mus ) musculus Linnaeus, 1758); long-tailed field mice (Apodemus sylvaticus Linnaeus, 1758)

Mobala virus

Mobala virus (MOBV)

Central African Republic

soft-furred mice (Praomys spp. Thomas, 1915)

Mopeia virus

Mopeia virus (MOPV)

Mozambique, Zimbabwe

Natal mastomys (Mastomys natalensis b Smith, 1834)

Morogoro virus (MORV)

Tanzania

Natal mastomys (Mastomys natalensis b Smith, 1834)

NEW WORLD ARENAVIRUSES, CLADE A

Allpahuayo virus

Allpahuayo virus (ALLV)

Peru

Brazilian oecomys (Oecomys paricola Thomas, 1904); white-bellied oecomys (Oecomys bicolor Tomes, 1860)

Flexal virus

Flexal virus (FLEV)

Brazil

Unidentified member of the oryzomyini

Paraná virus

Paraná virus (PARV)

Paraguay

Angouya oryzomys (Oryzomys angouya c Fischer, 1814)

Pichinde virus [sic]

Pichindé virus (PICV)

Colombia

white-throated oryzomys (Oryzomys albigularis Tomes, 1860)

Pirital virus

Pirital virus (PIRV)

Venezuela

Alston’s cotton rats ( Sigmodon ( Sigmomys ) alstoni Thomas, 1880); short-tailed zygodonts (Zygodontomys brevicauda Allen and Chapman, 1893)

NEW WORLD ARENAVIRUSES, CLADE B

Amapari virus [sic]

Amaparí virus (AMAV)

Brazil

Guianan neacomys (Neacomys guianae Thomas, 1905)d

Chapare virus

Chapare virus (CHPV)

Bolivia

unknown

Cupixi virus

Cupixi virus (CPXV)

Brazil

Azara’s broad-headed oryzomys (Oryzomys megacephalus Fischer, 1814)

Guanarito virus

Guanarito virus (GTOVe)

Venezuela

short-tailed zygodonts ( Zygodontomys brevicauda Allen and Chapman, 1893); Alston’s cotton rats (Sigmodon (Sigmomys) alstoni Thomas, 1880);

Junín virus

Junín virus (JUNV)

Argentina

drylands lauchas ( Calomys musculinus Thomas, 1913); Azara’s akodonts (Akodon (Akodon) azarae Fischer, 1829); little lauchas (Calomys laucha Fischer, 1814)

Machupo virus

Machupo virus (MACV)

Bolivia

big lauchas (Calomys callosus Rengger, 1830)f

Sabiá virus

Sabiá virus (SABV)

Brazil

?

Tacaribe virus

Tacaribe virus (TCRVg)

Trinidad

Jamaican fruit-eating bats (Artibeus (Artibeus) jamaicensis trinitatis Anderson, 1906)

NEW WORLD ARENAVIRUSES, CLADE C

Latino virus

Latino virus (LATV)

Bolivia

big lauchas (Calomys callosus Rengger, 1830)h

Oliveros virus

Oliveros virus (OLVV)

Argentina

Argentine akodonts (Necromys benefactus Thomas, 1919)i

NEW WORLD ARENAVIRUSES, TENTATIVE CLADE D

Bear Canyon virus

Bear Canyon virus (BCNV)

California, USA

big-eared woodrats ( Neotoma ( Neotoma ) macrotis Thomas, 1893); California deermice ( Peromyscus californicus Gambel, 1848)

Tamiami virus

Tamiami virus (TAMV)

Florida, USA

Alston’s cotton rats ( Sigmodon (Sigmomys) alstoni Thomas, 1880); marsh oryzomys (Oryzomys palustris Harlan, 1837)

Whitewater Arroyo virus

Big Brushy Tank virus (BBTV)

southwestern USA

white-throated woodrats (Neotoma (Neotoma) albigula Hartley, 1894)

Catarina virus (CTNV)

 

southern plains woodrats (Neotoma (Neotoma) micropus Baird, 1855)

Skinner Tank virus (SKTV)

 

Mexican woodrats (Neotoma (Neotoma) mexicana Baird, 1855)

Tonto Creek virus (TTCV)

 

white-throated woodrats (Neotoma (Neotoma) albigula Hartley, 1894)

Whitewater Arroyo virus (WWAV)

 

white-throated woodrats (Neotoma (Neotoma) albigula Hartley, 1894)

aPredominant/main hosts are in printed bold

bAlso sometimes referred to as Praomys natalensis

cAlso sometimes referred to as Sooretamys angouya Fischer, 1814

dInitial studies reported members of Oryzomys sp. as possible hosts [119]

ePreviously also abbreviated GUAV [27]

fMembers of Calomys cf. callosus have been reported to be the actual reservoir of MACV [119]. These lauchas are morphologically indistinguishable from members of Calomys callosus (s.s.) but may comprise a separate species

gPreviously also abbreviated TACV [27]

hThe proper species name for this reservoir rodent is Calomys callosus (s.s.) [119]

iMembers of Necromys benefactus Waterhouse, 1837 were previously thought to be the hosts [119]

New World arenaviruses are subdivided into three or four phylogenetic groups, A, B, C, and possibly D. Group A includes Allpahuayo virus (ALLV), Flexal virus (FLEV), PARV, PICV, and Pirital virus (PIRV) from South America. Group B contains the human pathogenic viruses Chapare virus (CHPV), Guanarito virus (GTOV), JUNV, MACV, and Sabiá virus (SABV), as well as the nonpathogenic AMAV, Cupixi virus (CPXV), and TCRV. Group C is composed of LATV and Oliveros virus (OLVV).

Recombination may have influenced the evolution of some arenaviruses. The NP and GP genes of Bear Canyon virus (BCNV), TAMV, and Whitewater Arroyo virus (WWAV) from North America have divergent phylogenetic histories. Separate analyses of full-length amino acid sequences revealed that the NPs of these three viruses are related to those of New World Group A viruses, while the GPCs are more closely related to those of New World Group B viruses [6, 38, 39, 60]. Together, these viruses are currently regarded as a tentative Group D of New World viruses.

Current family and genus inclusion criteria

Since the family Arenaviridae is currently monogeneric, the inclusion criteria for both family and genus are identical. According to the latest 9th ICTV Report [74], the current polythetic parameters to define an arenavirus (i.e., a member of the family Arenaviridae and the genus Arenavirus) are:
  1. 1)

    enveloped spherical or pleomorphic virions;

     
  2. 2)

    bisegmented single-stranded, ambisense RNA genome without polyadenylated tracts at the 3’ termini;

     
  3. 3)

    5’- and 3’-end sequence complementarity;

     
  4. 4)

    nucleotide sequences that could form one or more hairpin configurations within the intergenic regions of both genomic RNA molecules;

     
  5. 5)

    capped but not polyadenylated viral mRNAs;

     
  6. 6)

    induction of a persistent and frequently asymptomatic infection in reservoir hosts, in which chronic viremia and viruria occur.

     

Current species demarcation criteria

According to the latest 9th ICTV Report, “[t]he parameters used to define a species in the genus are:
  1. 1)

    an association with a specific host species [sic] or group of species [sic];

     
  2. 2)

    presence in a defined geographical area;

     
  3. 3)

    etiological agent (or not) of disease in humans;

     
  4. 4)

    significant differences in antigenic cross-reactivity, including lack of cross-neutralization activity where applicable;

     
  5. 5)

    significant amino acid sequence difference from other species [sic] in the genus (i.e., showing a divergence between species of at least 12 % in the nucleoprotein amino acid sequence)“ [124].

     

Not all criteria need to be fulfilled for a novel virus to define a new species (polythetic principle). For example, although PIRV and GTOV are endemic in the same region of Venezuela, they have been assigned to two different species (Pirital virus and Guanarito virus, respectively) because the viruses are maintained in different rodent hosts (Table 2), their titers differ by at least 64-fold using ELISA, and partial NP sequences are less than 55 % similar at the amino acid level. In another example, LASV and MOPV share common rodent hosts (Table 2), yet are distinguished by their different geographical range, profiles of reactivity with panels of monoclonal antibodies, and by NP amino acid sequence divergence of about 26 %. Also, LASV causes viral hemorrhagic fever in humans, whereas MOPV has not been found to be associated with human disease. Consequently, these two viruses have also been assigned to two different species (Lassa virus and Mopeia virus, respectively) in the past.

Current challenges in arenavirus taxonomy

Classification: discovery of novel arenaviruses

The number of sequenced coding-complete or complete genomes (for the sequencing nomenclature used see reference [80]) of viral pathogens has increased dramatically in recent years. Newly developed “next-generation” sequencing (NGS) technologies allow the rapid and cost-effective acquisition of thousands to millions of short sequence reads from a single sample and provide unprecedented possibilities for the large-scale sequencing of virus genomes [50, 68, 89, 95]. These technological advances promise an even richer haul of genomic data for arenaviruses in the near future, mainly due to their generally small genomes. Furthermore, NGS enables sequencing of viral genomes directly from clinical samples without the manipulation and adaptation often associated with culture prior to PCR-based methodologies.

Most virological science today is focused on the study of a relatively small number of pathogens. These viruses are studied either because of their easy propagation in the laboratory or their association with human or animal disease. However, many viruses cannot be cultured under standard laboratory conditions. The lack of knowledge of the size and characteristics of the global virome and the diversity of viral genomes are critical issues in the field of viral ecology that remain to be examined in detail [23]. Such knowledge would contribute to a better understanding of important issues, such as the origin of emerging pathogens and the extent of gene exchange among viruses.

Recently, NGS has been applied to direct whole genome sequencing of uncultured viral assemblages in a process termed “viral metagenomics,” and this advance has dramatically expanded our understanding of viral diversity. Researchers are now using this approach to explore viral communities in various biological and environmental matrices, including human samples from feces [21, 24, 57, 113, 145], blood [22], and the respiratory tract [142], as well as bat [51, 53, 86] and rodent [108, 137] samples. Metagenomic approaches present a fascinating opportunity to identify previously uncultured viruses and to understand the biodiversity, function, interactions, adaptation, and evolution of these viruses in different environments [5, 13, 20, 21, 23, 50, 116].

An example of how NGS and viral metagenomics studies can bring about such advances in arenavirology can be found in a recent study by Stenglein et al. [129]. Three novel arenaviruses, CAS virus, Golden Gate virus, and Collierville virus were identified in sick boid snakes as possible etiological agents of snake inclusion body disease (IBD). This discovery was made possible by unbiased high-throughput metagenomic analysis of RNA extracted directly from IBD-positive and –negative snake tissues. In fact, isolation attempts using common reptile cell lines or the mammalian arenavirus-permissive grivet-derived Vero cell line failed to detect productive replication of Golden Gate virus. Only a continuous cell line generated from a female boa constrictor, the alethinophidian host of Golden Gate virus, supported efficient virus replication. Thus, this study exemplifies the potential of NGS and viral metagenomics studies in advancing discovery and characterization of novel arenaviruses, which might be difficult or impossible to culture under standard laboratory conditions.

Recently, two other studies used similar approaches and identified two additional snake viruses that have genomes with the typical organization of arenaviruses [14, 67]. All of these newly discovered snake arenaviruses differ from all other known arenaviruses in several key aspects:
  • they infect alethinophidian snakes, rather than mammals [14, 67, 129];

  • their genes and genomes do not cluster with either Old World or New World arenaviruses in sequence alignments but together form a monophyletic sister group to both clusters [14, 67, 129];

  • their GPC genes encode a GP2 subunit highly reminiscent of that of Ebola virus (family Filoviridae) [67, 75, 129];

  • their Z proteins do not possess N-terminal glycine residues but have transmembrane domains at the N-termini; they do not contain known late budding motifs [129];

  • putative late budding motifs are found at the C-termini of their NP proteins [129].

At the time of writing, most published alethinophidian arenaviruses were isolated in culture. Together with the data summarized above, these snake arenaviruses will have to be classified, but they cannot be included in any of the established mammalian arenavirus species [67].

In addition to the alethinophidian arenaviruses, several novel mammalian Old and New World arenaviruses have been described in recent years. A summary list of all currently unclassified arenaviruses is presented in Table 3. Most of the unclassified mammalian arenaviruses would not be recognized as members of new species under the current species demarcation criteria. Such an example is Dandenong virus, the NP amino acid sequence of which is only 3 % different from that of LCMV, suggesting it is a member of the species Lymphocytic choriomeningitis virus. However, some viruses do comply with all or most of the species demarcation criteria. One example is the newly discovered Merino Walk virus, the NP amino acid sequence of which is more than 31 % different from that of MOPV, the most closely related arenavirus.
Table 3

Currently unclassified arenaviruses

Suggested virus name (suggested abbreviation)

Genomic sequence availability and amino acid sequence divergence to closely related virus homologs

Serology

Isolation in culture

Natural host reservoir (species name)

Reference and GenBank accession numbers

OLD WORLD MAMMALIAN ARENAVIRUSES

Dandenong virus (DANV)

GP, NP, L, Z. LCMV: GPC (6 %) and NP (3 %)

yes (IgG and IgM)

yes (confirmed by CPE, RT-PCR, IFA-α OWA, EM)

unknown

[103]

S: EU136038

L: EU136039

Gbagroube virus (none)

complete S segment, partial L segment. LASV: GPC (9.8 %) and NP (14.1 %)

yes (α OWA IgG)

no

Peters’s mice (Mus (Nannomys) setulosus Peters, 1876)

[47]

S: GU830848

Jirandogo virus (none)

partial GP, NP, L. LASV: NP (18 %)

no

no

Baoule’s mice (Mus (Nannomys) baoulei Vermeiren and Verheyen, 1980)

[78]

Only partial sequencess

Kodoko virus (KODV)

partial NP, partial L. LCMV: NP (24.6 %), and L (7.2 %)

no

no

African pygmy mice (Mus (Nannomys) minutoides Smith, 1834)

[82]

Only partial sequences

Lunk virus (LNKV)

complete S and L segments. LCMV: NP (17.7 %)

no

yes

African pygmy mice (Mus (Nannomys) minutoides Smith, 1834)

[70]

S: AB693150

L: AB693151

Menekre virus (none)

complete S segment, partial L segment. MOPV: GPC (21.5 %), LASV: NP (24.7 %)

yes (α OWA IgG)

no

African wood mice (Hylomyscus sp. Thomas, 1926)

[47]

S: GU830862

Merino Walk virus (MWV)

complete genome. MOPV: NP (31.4 %)

CF testing: related to MOPV, MOBV, and IPPYV, but unrelated to LCMV

yes (confirmed by EM)

Bush Ka(r)roo rats (Myotomys unisulcatus Cuvier, 1829)

[104]

S: GU078660

L: GU078661

NEW WORLD MAMMALIAN ARENAVIRUSES

“[New World] arenavirus 96010025”

complete S segment. AV 96010151: NP (8.2 %)

no

?

bushy-tailed woodrats (Neotoma (Teonoma) cinerea Ord, 1815)

Unpublished

S: EU486820

“[New World] arenavirus H0380005”

complete S segment. AV 96010151: NP (6.8 %)

no

yes?

southern plains woodrats (Neotoma (Neotoma) micropus Baird, 1855)

Unpublished

S: EU910959

“North American arenavirus 96010024”

complete S segment. AV 96010151: NP (7.3 %)

no

?

Mexican woodrats (Neotoma (Neotoma) mexicana Baird, 1855)

[35]

S: EU123331

“North American arenavirus 96010151”

complete S segment. WWAV: NP (5.7 %)

no

?

Mexican woodrats (Neotoma (Neotoma) mexicana Baird, 1855)

[35]

S: EU123330

“North American arenavirus D1240007”

complete S segment.

AV 96010151: NP (7.3 %)

no

?

Mexican woodrats (Neotoma (Neotoma) mexicana Baird, 1855)

[35]

S: EU123329

Black Mesa virus (none)

complete GP, N, and partial L gene. AV 96010151: NP (7.7 % and 7.9 %)*

no

no

white-throated woodrats (Neotoma (Neotoma) albigula Hartley, 1894)

unpublished (FJ719106, FJ032026, FJ719107, FJ032027, EU938670)

Middle Pease River virus (MPRV)

GP, NP.

CTNV: NP (11-12 %)

yes (ELISA: WWAV)

Yes (confirmed by IFA-αWWAV)

southern plains woodrats (Neotoma (Neotoma) micropus Baird, 1855)

[34]

S: JX560798, JX560799

Ocozocoautla de Espinosa virus (OCEV)

complete S segment. JUNV: NP (16.1 %), TCRV: GPC (24.7 %)

yes

no

Mexican deermice (Peromyscus mexicanus Saussure, 1860)

[33]

S: JN897398

Orogrande virus (none)

partial L gene

no

no

southern plains woodrats (Neotoma (Neotoma) micropus Baird, 1855)

unpublished (EU938669)

Pinhal virus (none)

partial N gene

no

no

delicate lauchas (Calomys tener Winge, 1887)

unpublished (EU280546, EU280547, EU280545, EU220740, EU329718)

Real de Catorce virus (none)

complete S segment. CTNV: NP (11.6 %), SKTV: GPC (28.3 %)

WWAV: GPC (32 %), NP (13.7 %)

yes (ELISA: WWAV)

no

white-toothed woodrats (Neotoma (Neotoma) leucodon Merriam, 1894)

[69]

S: GQ903697

REPTILIAN ARENAVIRUSES

Boa Av NL B3 virus (none)

near-complete genome;

UHV: GPC (38 %), NP (16 %), Z (11 %), L (8 %)

no

no

captive boa constrictors (Boa constrictor Linnaeus, 1758) and emerald tree boas (Corallus caninus Linnaeus, 1758) with inclusion body disease

[14, 15]

S: KC508669

L: KC508670

CAS virus (CASV)

complete genome. Boa Av NL B3 virus: NP (43.9 %), GPC (41.6 %), L (48.9 %), Z (48.6 %)

TCRV: NP (74.2 %), L (80.8 %)

no

no

captive annulated tree boas (Corallus annulatus Cope, 1875) with inclusion body disease

[129]

S: JQ717262

L: JQ717261

Collierville virus (CVV)

no

no

no

captive boa constrictors (Boa constrictor Linnaeus, 1758) with inclusion body disease

[129]

Golden Gate virus (GGV)

complete genome

Boa Av NL B3 virus: NP (33.7 %), GPC (15.2 %), L (20.9 %)

UHV: Z (9.2 %)

LASV: NP (74.9 %), TCRV: L (81.5 %)

no

yes

captive boa constrictors (Boa constrictor Linnaeus, 1758) with inclusion body disease

[129]

S: JQ717264

L: JQ717263

University of Helsinki virus (UHV)

near-coding-complete genome. Boa Av NL B3 virus: GPC (38 %), NP (16 %), L (8 %), GGV: Z (5 %)

no

yes

captive boa constrictors (Boa constrictor Linnaeus, 1758), annulated tree boas (Corallus annulatus Cope, 1875), common tree boas (Corallus hortulanus Linnaeus, 1758) with inclusion body disease

[67]

S: KF297880

L: KF297881

CF, complement fixation; IFA, immunofluorescence assay; αOWA, anti-Old World arenavirus antibody; αWWAV, anti-WWAV antibody; EM, electron microscopy; CPE, cytopathic effect; ELISA, enzyme-linked immunosorbent assay; RT-PCR, reverse transcription polymerase chain reaction; * The two values are for the two strains of Black Mesa virus

Nomenclature: spelling of arenavirus species names

Arenavirus names and arenaviral species names are traditionally derived from geographic locations, such as towns, regions, or rivers. Since many mammalian New World arenaviruses were discovered in South America, their names are derived from South American locations, which are spelled using the Spanish alphabet. The ICTV Arenaviridae Study Groups of the past have already corrected several arenavirus and arenaviral species names by incorporating correct diacritical marks (Table 1). However, at least two species names still contain incorrectly spelled word stems (Amapari [sic] and Pichinde [sic]).

Communication among virologists and database searches are crucially dependent on virus name abbreviations being unique to avoid confusion. Several abbreviations for classified arenaviruses do not fulfill this condition:
  • CHPV as the abbreviation for Chandipura virus (a vesiculovirus) and chicken parvovirus preceded the use of CHPV as the abbreviation for Chapare virus;

  • CPXV as the abbreviation for cowpox virus (an orthopoxvirus) preceded the use of CPXV for Cupixi virus;

  • LUNV as the abbreviation for Lundy virus (an orbivirus) preceded the use of LUNV as the abbreviation for the recently discovered Luna virus;

  • PARV as the abbreviation for Paraná virus is not ideal because the abbreviations PARV4 and ParV-3 are in use for the unclassified parvovirus PARV4 virus and the unclassified potexvirus parsnip virus 3, respectively;

  • PICV as the abbreviation for Pichindé virus is not ideal, as PiCV is in use for pigeon circovirus;

  • SABV as the abbreviation for Sabiá virus is problematic, as SABV also stands for Saboya virus (a flavivirus); and

  • TAMV as the abbreviation for Tamiami virus is not ideal, as TaMV is in use for Tulare apple mosaic virus (an ilarvirus).

Several abbreviations suggested for unclassified arenaviruses are also not unique:
  • BBTV should not be used as an abbreviation for Big Brushy Tank virus, as BBTV is already in use for banana bunchy top virus (a babuvirus);

  • CVV should not be used as an abbreviation for Collierville virus as it is already in use for citrus variegation virus (an ilarvirus);

  • GGV as the abbreviation for Golden Gate virus is problematic as GgV is in use for Gaeumannomyces graminis virus (a partitivirus);

  • MPRV as the abbreviation for Middle Pease River virus is problematic as MpRV is in use for Micromonas pusilla reovirus; and

  • MWV as the abbreviation for Merino Walk virus is problematic as MwV has been suggested for the unclassified alphanodavirus Manawatu virus.

In addition, several unclassified arenavirus names do not have abbreviations: Black Mesa virus, Gbagroube virus, Jirandogo virus, Menekre virus, Orogrande virus, Pinhal virus, and Real de Catorce virus (RDCV has been suggested in one publication [10]). Finally, “Boa Av NL B3 virus” and several North American arenaviruses lack proper virus names and abbreviations.

Problems related to the International Code of Virus Classification and Nomenclature

Classification and nomenclature of viruses are subject to Rules formalized in a Code, the International Code of Classification and Nomenclature (ICVCN) [74]. At the moment, arenavirus names and arenaviral species names are spelled identically and only differ by the absence or presence of italics (e.g., Junín virus is a member of the species Junín virus). This is a problem in particular for electronic databases, which often cannot differentiate between Roman and italicized text. Second, the genus name Arenavirus and the family name Arenaviridae are only differentiated by their specific suffixes (“-virus” vs. “-viridae”) but contain the same word stem (“arena”). The members of the family are therefore called arenaviruses, while the members of the genus are also called arenaviruses. At present, this lack of precision is unproblematic, as the family currently includes only a single genus. However, the establishment of a second genus for alethinophidian arenaviruses will make “arenavirus” an ambiguous term, as it will not be clear whether, upon its use, all members of the family are meant or only those of one of the two genera. Together, current arenavirus taxonomy is therefore at odds with ICVCN
  • Rule 2.1(ii): “The essential principles of virus nomenclature are…to avoid or reject the use of names which might cause error or confusion”;

  • Rule 3.14: “New names shall not duplicate approved names. New names shall be chosen such that they are not closely similar to names that are in use currently or have been in use in the recent past”;

  • Rule 3.21: “A species name shall consist of as few words as practicable but be distinct from names of other taxa”; and

  • Rule 3.22: “A species name must provide an appropriately unambiguous identification of the species” [3, 74].

Solutions to current challenges in arenavirus taxonomy

New family and taxon inclusion criteria

Due to the recognition of the widely expanding diversity of arenaviruses, we base arenavirus classification on objective criteria based on coding-complete genomic segment sequences [80]. Based on consensus voting of ICTV Arenaviridae Study Group members, arenaviruses are now classifiable if:
  1. 1)

    coding-complete genomic sequences are available for both S and L segments even in the absence of a culturable isolate; or

     
  2. 2)

    a coding-complete genomic sequence is available for the S segment together with a culturable isolate.

     

Based on these criteria, all currently classified arenaviruses (Table 2) should remain classified. Boa AV NL B3, CAS virus, Dandenong virus, Golden Gate virus, Lunk virus, Merino Walk virus, Middle Pease River virus, Tonto Creek virus, and University of Helsinki virus should be classified. Black Mesa virus, Collierville virus, Gbagroube virus, Jirandogo virus, Kodoko virus, Ocozocoautla de Espinosa virus, Orogrande virus, Pinhal virus, Real de Catorce virus, and the unnamed North American arenaviruses (Table 3) should be considered tentative members of the family until more data become available.

The PAirwise Sequence Comparison (PASC) tool, accessible at the National Center for Biotechnology Information (NCBI) website (http://www.ncbi.nlm.nih.gov/sutils/pasc/viridty.cgi?textpage=overview) and/or alternatives such as DivErsity pArtitioning by hieRarchical Clustering (DeMARC) [81] or the Species Demarcation Tool (SDT) [99] should be used for preliminary classification of novel, classifiable arenaviruses. PASC analysis creates histograms to visualize the distances between pairs of virus sequences, resulting in peaks that may represent different taxon levels. The percentages of the lowest points of the valleys between the peaks can guide taxon demarcation criteria (for more information on PASC, see references [11, 12]). Ideally, these percentages cutoffs are concordant with the arenavirus diversity deduced from other phylogenetic analyses and are not contradicted by known biological characteristics of individual arenaviruses. Such characteristics include: differences in host specificity and thereby geographic distribution, serological cross-reactions between virions, and the ability to cause human disease. If individual analyses do not come to the same conclusions in regard to classification, the ICTV Arenaviridae Study Group will have to resolve them by criterion weighing and establishment of compromises.

The results of the arenavirus PASC analysis can be accessed on the PASC webpage (S segments: http://www.ncbi.nlm.nih.gov/sutils/pasc/viridty.cgi?cmdresult=main&id=448; L segment: http://www.ncbi.nlm.nih.gov/sutils/pasc/viridty.cgi?cmdresult=main&id=446).

PASC analysis and determination of NP amino acid pairwise distances (Fig. 3) were therefore performed to evaluate whether the various possible outcomes would match the current arenavirus classification and possibly accommodate novel viruses that are thought to require the establishment of novel taxa. Indeed, both analyses substantiate that the family Arenaviridae contains at least two genera, one for mammalian and one for reptilian arenaviruses. For the S segment, the pairwise nucleotide sequence identities within the same proposed genus are higher than 40 %, while those from different proposed genera are lower than 29 %. The genus separation cutoff in PASC was therefore set to 29-40 % for the S segment, and to 30-35 % for the L segment.
Fig. 3

Pairwise Sequence Comparison (PASC) analysis of L segment sequences and amino acid distance analysis of NP sequences. (A) Distribution of pairwise identities among 87 complete sequences of the L segments of members of the family Arenaviridae. Regions A, B and C represent virus pairs from the same species (100 %-76 %), different species but the same genus (76 %-35 %), and different genera (16 %-30 %), respectively, based on the proposed identity values indicated in parentheses. The x-axis shows percent identity, and the y-axis shows the number of L segment sequence pairs. (B) Amino acid sequence distances were compared using the pairwise-distance algorithm in the MEGA 6 software package and shown as frequency histograms. This analysis was done based on a multiple alignment generated using the ClustalW algorithm implemented in MEGA 6 [131]

Depending on the various valleys-between-peaks in PASC, several alternative sequence cutoffs could be chosen for arenavirus species demarcation. The members of the ICTV Arenaviridae Study Group agreed that the most conservative approach be taken, i.e. that these values should be chosen in a way that introduces the fewest changes and causes the least disruption of the current arenavirus classification scheme. Accordingly, >80 % nucleotide sequence identity in the S segment and >76 % identity in the L segment were chosen as values for arenaviruses that should belong to the same species. The ICTV Arenaviridae Study Group agreed that PASC or similar methods alone cannot necessarily justify species classification and that, whenever possible, other criteria should be considered to confirm or reject analysis outcomes. These species classification criteria include:
  1. 1)

    association of the arenavirus with a main host or a group of sympatric hosts;

     
  2. 2)

    dispersion of the arenavirus in a defined geographical area;

     
  3. 3)

    significant differences in antigenic cross-reactivity, including lack of cross-neutralization activity;

     
  4. 4)

    significant protein amino acid sequence differences compared to the homologous proteins of viruses from other species in the same genus (e.g., showing a divergence between members of different species of at least 12 % in the nucleoprotein amino acid sequence);

     
  5. 5)

    association (or not) with human disease.

     

Revised classification of previously classified arenaviruses and inclusion of newly discovered classifiable arenaviruses

The results obtained by PASC analyses for preliminary arenavirus classification are outlined in Table 4. This classification is largely in accordance with the current classification of mammalian arenaviruses, which was largely based on biological criteria. The only modification that PASC analyses suggests to the current arenavirus classification is the establishment of nine new species (for Big Brushy Tank virus, Catarina virus, Dandenong virus, Lunk virus, Merino Walk virus, Middle Pease River virus, Morogoro virus, Skinner Tank virus, and Tonto Creek virus) and that the current species for LASV, LCMV, MOPV, PIRV, and WWAV have to be split.
Table 4

Preliminary classification of arenaviruses based on PASC resultsa

Family

Genus

Species

Virus

Notes and GenBank accession numbers

Arenaviridae (members: arenaviruses)

    
 

Genus 1 (members: mammalian arenaviruses)

   

OLD WORLD ARENAVIRUSES

  

Species 1

Dandenong virus

also includes “LCMV M2” (AB261990), “LCMV BRC” (AB627953)

  

Species 2

Ippy virus

 
  

Species 3

Lassa virus

“LASV Josiah” (J04324)

  

Species 4

“Lassa virus”

“LASV 11620” (AF181853), “LASV Pinneo” (AY628207)

  

Species 5

“Lassa virus”

“LASV 803213” (AF181854), Nig08-04 (GU481068), Nig08-A47 (GU481078), Nig08-A37 (GU481074), Nig08-A41 (GU481076)

  

Species 6

“Lassa virus”

“LASV GA391” (X52400), “LASV Weller” (AY628206), Nig08-A18 (GU481070), Nig08-A19 (GU481072)

  

Species 7

“Lassa virus”

“LASV CSF” (AF333969)

  

Species 8

“Lassa virus”

“LASV AV” (AF246121, FR832711), “LASV Soromba-R” (KF478765), “LASV Bamba-R114” (KF478766), “LASV Komina-R16” (KF478767), “LASV Ouoma-R123” (KF478768), “LASV Soromba-R30” (KF478769)

  

Species 9

Lujo virus

 
  

Species 10

Luna virus

 
  

Species 11

Lunk virus

 
  

Species 12

lymphocytic choriomeningitis virus

“LCMV Armstrong 53b” (M20869)

  

Species 13

“lymphocytic choriomeningitis virus”

“LCMV Bulgaria” (GQ862982)

  

Species 14

“lymphocytic choriomeningitis virus”

“LCMV GR01” (FJ895883)

  

Species 15

“lymphocytic choriomeningitis virus”

“LCMV CABN” (FJ895882), “LCMV SN05” FJ895884)

  

Species 16

“lymphocytic choriomeningitis virus”

“LCMV 810935” (FJ607029)

  

Species 17

Merino Walk virus

 
  

Species 18

Mobala virus

 
  

Species 19

Mopeia virus

“MOPV AN 21366” (M33879)

  

Species 20

“Mopeia virus”

“MOPV” (DQ328874) (= Mozambique virus)

  

Species 21

Morogoro virus

 

NEW WORLD ARENAVIRUSES

  

Species 22

Allpahuayo virus

 
  

Species 23

Flexal virus

 
  

Species 24

Paraná virus

 
  

Species 25

Pichindé virus

 
  

Species 26

Pirital virus 1

“PIRV VAV-488” (AF485262)

  

Species 27

Pirital virus 2

“PIRV VAV-1743” (AY575850)

  

Species 28

Pirital virus 3

“PIRV 1645” (AY573921)

  

Species 29

Pirital virus 4

“PIRV 97021016” (AY573923), “PIRV 97020912” (AY574571)

  

Species 30

Amaparí virus

 
  

Species 31

Chapare virus

 
  

Species 32

Cupixi virus

 
  

Species 33

Guanarito virus

 
  

Species 34

Junín virus

 
  

Species 35

Machupo virus

 
  

Species 36

Sabiá virus

 
  

Species 37

Tacaribe virus

 
  

Species 38

Latino virus

 
  

Species 39

Oliveros virus

 
  

Species 40

Bear Canyon virus

 
  

Species 41

Big Brushy Tank virus

 
  

Species 42

Middle Pease River virus

 
  

Species 43

Catarina virus

 
  

Species 44

Skinner Tank virus

 
  

Species 45

Tamiami virus

 
  

Species 46

Tonto Creek virus

 
  

Species 47

Whitewater Arroyo virus

Includes “North American arenaviruses” deposited under EU123330, EU123331

  

Species 48

“[New World] arenavirus H0380005”

EU910959

  

Species 49

“North American arenavirus D1240007”

EU123329

  

Species 50

“[New World] arenavirus 96010025”

EU486820

 

Genus 2 (members: reptilian arenaviruses)

   
  

Species 1

Golden Gate virus

 
  

Species 2

University of Helsinki virus, Boa AV NLB3

 
  

Species 3

CAS virus

 

aThis table summarizes the combined results of PASC analysis of arenaviral S segments. The classification is consistent with that for L segments for almost all viruses for which coding-complete S and L segments are available. Viruses were deemed suitable for analysis if a) the complete sequence of the S segment and an isolate in culture were available or b) if the complete S and L segment sequences were available

The ICTV Arenaviridae Study Group determines the taxonomic status of individual arenaviruses using the current ICTV definition of species (ICVCN Rule 3.20: “A species is the lowest taxonomic level in the hierarchy approved by the ICTV. A species is a monophyletic group of viruses whose properties can be distinguished from those of other species by multiple criteria”) [3, 74]. The set of six polythetic criteria outlined in this article is sufficient to determine the taxonomic status of an arenavirus isolate; however, each criterion by itself is not necessarily sufficient for accurate classification. Several species criteria are directly or distantly related to phylogenetic relationships, and by extension, to monophyly. The genetic proximity of viruses is determined either by PASC analysis or by NP amino acid differences. Even differences in antigenic cross-reactivity could be related to the genetic proximity of the NP and GPC amino acid sequences of the viruses. Other criteria are related to the relationships between the virus and its environment (i.e., the “ecological niche”), such as the association with a host, the geographic area, and the ability to cause human disease.

As mentioned above, based solely on PASC analysis, several arenavirus species would have to be “split” even if the most conservative cutoffs are chosen. However, such a “split” would be in contradiction to the polythetic nature of virus species (i.e., in contradiction to the other biological demarcation criteria described above). Furthermore, in some cases, PASC analysis alone may not provide consistent results for the S and L segments (e.g., the S segment of LCMV isolate 810366 [FJ607028] shares >80 % sequence identity with those of other LCMV isolates, whereas its L segment [FJ607019] shares less than 76 % identity with others). This inconsistency is not surprising considering that members of virus species constantly replicate and evolve and, therefore, form fuzzy sets with hazy boundaries.

In general, virus species can be viewed as biological continua, with members from both extremes differing significantly from each other when considering one or several parameters but are still related through multiple members with intermediate variance values. This concept is especially true for genetic distances: divergence of two isolates could be higher than the cutoff value, but these isolates could still be linked together through other intermediate isolates. For example, the NP amino acid distance between Skinner Tank virus and “arenavirus AV 96010025” is 15.65 %, i.e., above the chosen 12 % criterion. However, they form a biological continuum with Big Brushy Tank virus and “North American arenavirus AV 96010151” with inter-NP distances below 11 %.

After discussing these issues, the ICTV Arenaviridae Study Group decided (i) not to address the species splits suggested by PASC analysis at this point and (ii) to postpone the possibly necessary establishment of novel species for Big Brushy Tank virus, Catarina virus, Dandenong virus, Middle Pease River virus, Morogoro virus, Skinner Tank virus, and Tonto Creek virus until further biological data are reviewed and additional comparative sequence analyses are performed. However, the group has decided to establish new species for Lunk virus and Merino Walk virus as suggested by PASC. Also, until further analyses are performed, the group considers Morogoro virus a member of the species already established for MOPV, and Big Brushy Tank virus, Catarina virus, Skinner Tank virus, and Tonto Creek virus members of the species already established for WWAV. The group decided to postpone any decisions on the taxonomic status of Dandenong virus and Middle Pease River virus until further phylogenetic and biological analyses are performed and isolates are obtained. These viruses are therefore considered unclassified mammalian arenaviruses at the time of writing.

Changes of genus and species names to correct spelling mistakes and to comply with ICVCN Rules

The ICTV Arenaviridae Study Group voted to name the genus for mammalian arenaviruses Mammarenavirus, and that for reptilian arenaviruses Reptarenavirus. To bring arenavirus taxonomy in compliance with the ICVCN, non-Latinized binomial species names [135] are introduced for species of both genera. Since most virologists work with actual viruses, do not need to address species frequently, and are accustomed to the established virus names, it is unlikely that the non-Latinized binomial species names would still be used accidentally for viruses. Furthermore, the species name parts “Pichinde” and “Amapari” are corrected to “Pichindé” and “Amaparí,” respectively. Unique abbreviations are assigned to all viruses (as judged by screening of the 9th ICTV Report [74]). After communication with the discoverers, “Boa AV NL B3” was renamed ROUT virus (ROUTV) (Rogier Bodewes et al., personal communication). A summary of all currently changes can be found in Table 5.
Table 5

Updated and corrected taxonomy of the family Arenaviridae

Family

Genus

Species

Virus (Abbreviation)

Arenaviridae (members: arenaviruses)

   
 

Mammarenavirus (members: mammarenaviruses)

  

OLD WORLD ARENAVIRUSES

  

Ippy mammarenavirus

Ippy virus (IPPYV)

  

Lassa mammarenavirus

Lassa virus (LASV)

  

Lujo mammarenavirus

Lujo virus (LUJV)

  

Luna mammarenavirus

Luna virus (LUAV)

  

Lunk mammarenavirus

Lunk virus (LNKV)

  

Lymphocytic choriomeningitis mammarenavirus

lymphocytic choriomeningitis virus (LCMV)

  

Merino Walk mammarenavirus

Merino Walk virus (MRWV)

  

Mobala mammarenavirus

Mobala virus (MOBV)

  

Mopeia mammarenavirus

Mopeia virus (MPOV), Morogoro virus (MORV)

NEW WORLD ARENAVIRUSES

  

Allpahuayo mammarenavirus

Allpahuayo virus (ALLV)

  

Flexal mammarenavirus

Flexal virus (FLEV)

  

Paraná mammarenavirus

Paraná virus (PRAV)

  

Pichindé mammarenavirus

Pichindé virus (PICHV)

  

Pirital mammarenavirus

Pirital virus (PIRV)

  

Amaparí mammarenavirus

Amaparí virus (AMAV)

  

Chapare mammarenavirus

Chapare virus CHAPV)

  

Cupixi mammarenavirus

Cupixi virus (CUPXV)

  

Guanarito mammarenavirus

Guanarito virus (GTOV)

  

Junín mammarenavirus

Junín virus (JUNV)

  

Machupo mammarenavirus

Machupo virus (MACV)

  

Sabiá mammarenavirus

Sabiá virus (SBAV)

  

Tacaribe mammarenavirus

Tacaribe virus (TCRV)

  

Latino mammarenavirus

Latino virus (LATV)

  

Oliveros mammarenavirus

Oliveros virus (OLVV)

  

Bear Canyon mammarenavirus

Bear Canyon virus (BCNV)

  

Tamiami mammarenavirus

Tamiami virus (TMMV)

  

Whitewater Arroyo mammarenavirus

Catarina virus (CTNV), Big Brushy Tank virus (BBRTV), Skinner Tank virus (SKTV), Tonto Creek virus (TTCV), Whitewater Arroyo virus (WWAV)

 

Reptarenavirus (members: reptarenaviruses)

  
  

Alethinophid 1 reptarenavirus

Golden Gate virus (GOGV)

  

Alethinophid 2 reptarenavirus

ROUT virus (ROUTV), University of Helsinki virus (UHV)

  

Alethinophid 3 reptarenavirus

CAS virus (CASV)

Pronunciation guidelines for arenavirus and arenavirus taxon names

Arenavirus names and arenavirus taxon names are traditionally derived from geographic locations. Table 6 provides guidance for their correct pronunciation using the International Phonetic Alphabet (IPA) and an English phonetic notation.
Table 6

Pronunciation of arenavirus names and taxon names

Arenavirus namea

International Phonetic Alphabet (IPA)

English phonetic notationb

Allpahuayo virus

[ˌɑlpɑ’wɑjɔ ˈvaɪrəs] or [ˌælpæ’wæjoʊ ˈvaɪrəs]c

ahl-pah-wah-yaw (al-pa-wa-yoh) vahy-ruhsd

Alethinophid reptarenavirus

[ˌæləthinˈoʊfɪd rɛptəˈrinəˌvaɪrəs] or [ˌæləthinˈoʊfɪd rɛptˌerənə’vaɪrəs]

al-uh-theen-oh-phid rept-uh-ree-nuh-vahy-ruhs (rept-er-uh-nuh-vahy-ruhs)

Amaparí virus

[ˌɑmɑpɑ’ri ˈvaɪrəs] or [ˌæmæpə’ri ˈvaɪrəs]

ah-mah-pah-ree (a-ma-puh-ree) vahy-ruhs

arenavirid

[əˈrinəˌvirɨd] or [ˌerənə’virɨd]

uh-ree-nuh-vee-rid (er-uh-nuh-vee-rid)

Arenaviridae

[əˈrinəˌvirɨdi or [ˌerənə’virɨdi]

uh-ree-nuh-vee-ri-dee (er-uh-nuh-vee-ri-dee)

arenavirus

[əˈrinəˌvaɪrəs] or [ˌerənəˈvaɪrəs]

uh-ree-nuh-vahy-ruhs (er-uh-nuh-vahy-ruhs)

Bear Canyon virus

[bɛər ˈkænyən ˈvaɪrəs]

bair kan-yuhn vahy-ruhs

Big Brushy Tank virus

[bɪg ˈbrʌʃi tæŋk ˈvaɪrəs]

big bruhsh-ee tangk vahy-ruhs

Black Mesa virus

[ˈblæk ˈmeɪsə ˈvaɪrəs]

blak mey-suh vahy-ruhs

CAS virus

[kæs ˈvaɪrəs]

kas vahy-ruhs

Catarina virus

[ˌkætə’rinə ˈvaɪrəs]

ka-tuh-ree-nuh vahy-ruhs

Chapare virus

[tʃɑ’pɑrɛ ˈvaɪrəs] or [tʃɑ’pɑreɪ ˈvaɪrəs]

chah-pahr-eh (chah-pahr-ey) vahy-ruhs

Collierville virus

[ˈkɒlyərˌvɪl ˈvaɪrəs]

kol-yer-vil vahy-ruhs

Cupixi virus

[kʊ’piʃ ˈvaɪrəs]

koo-peesh vahy-ruhs

Dandenong virus

[‘dændiˌnoŋ ˈvaɪrəs]

dan-dee-nong vahy-ruhs

Flexal virus

[flɛ’ʃɑl ˈvaɪrəs] or [flɛ’ʃɑʊ ˈvaɪrəs]

fle-shahl (fle-show) vahy-ruhs

Gbagroube virus

[bɑ’rʊbɛ ˈvaɪrəs] or [bɑ’rʊbeɪ ˈvaɪrəs]

bah-roo-beh (bah-roo-bey) vahy-ruhs

Golden Gate virus

[ˈgoʊldən geɪt ˈvaɪrəs]

gohl-duhn geyt vahy-ruhs

Guanarito virus

[ˌgwɑnɑ’ritɔ ˈvaɪrəs] or [ˌgwænə’ritoʊ ˈvaɪrəs]

gwah-nah-ree-taw (gwa-nuh -ree-toh) vahy-ruhs

Ippy virus

[‘ɪpi ˈvaɪrəs]

ip-ee vahy-ruhs

Jirandogo virus

[ˌdʒirən’dɔgɔ ‘vaɪrəs] or [ˌdʒirən’dɒgoʊ ‘vaɪrəs]

jee-ruhn-daw-gaw (jee-ruhn-dog-oh) vahy-ruhs

Junín virus

[hʊ’nin ˈvaɪrəs]

hoo -nin vahy-ruhs

Kodoko virus

[kɔ’dɔkɔ ˈvaɪrəs] or [kə’doʊkoʊ ˈvaɪrəs]

kaw-daw-kaw (kuh -doh-koh) vahy-ruhs

Lassa virus

[‘lɑsɑ ˈvaɪrəs] or [‘lɑsə ˈvaɪrəs]

lah-sah (lah-suh) vahy-ruhs

Latino virus

[lə’tinoʊ ˈvaɪrəs] or [læ’tinoʊ ˈvaɪrəs]

luh-tee-noh (la-tee-noh) vahy-ruhs

Lujo virus

[‘lʊdʒoʊ ˈvaɪrəs]

l oo-joh vahy-ruhs

Luna virus

[‘lʊnə ˈvaɪrəs]

loo-nuh vahy-ruhs

Lunk virus

[‘lʊŋk ˈvaɪrəs]

loongk vahy-ruhs

lymphocytic choriomeningitis virus

[ˌlɪmfəˈsɪtɪk ˈkɔrioʊˌmɛnɪnˈdʒaɪtɪs ˈvaɪrəs]

lim-fuh-sit-ik kawr-ee-oh-men-in-jahy-tis vahy-ruhs

Machupo virus

[mɑ’tʃʊpɔ ˈvaɪrəs] or [mə’tʃʊpoʊ ˈvaɪrəs]

mah-ch oo-paw (muh-ch oo-poh) vahy-ruhs

mammarenavirus

[mæməˈrinəˌvaɪrəs] or [mæmˌerənə’vaɪrəs]

mam-uh-ree-nuh-vahy-ruhs (mam-er-uh-nuh-vahy-ruhs)

Menekre virus

[mɛ’nɛkrɛ ˈvaɪrəs] or [mə’nɛkreɪ ˈvaɪrəs]

meh-nek-reh (muh-nek-rey) vahy-ruhs

Merino Walk virus

[məˈrinoʊ wɔk ˈvaɪrəs]

muh-ree-noh wawk vahy-ruhs

Middle Pease River virus

[‘mɪdl piz ˈrivər ˈvaɪrəs]

mid-l peez riv-er vahy-ruhs

Mobala virus

[mɔ’bɑlɑ ˈvaɪrəs] or [mə’bɑlə ˈvaɪrəs]

maw-bah-lah (muh-bah-luh) vahy-ruhs

Mopeia virus

[mɔ’peɪɑ ˈvaɪrəs] or [mə’peɪə ˈvaɪrəs]

maw-pey-ah (muh-pey-uh) vahy-ruhs

Morogoro virus

[mɔrɔ’gɔrɔ ˈvaɪrəs] or [mərə’goʊroʊ ˈvaɪrəs]

maw-raw-gaw-raw (muh-ruh-goh-roh) vahy-ruhs

Ocozocoautla de Espinosa virus

[ɔˌkɔsɔkɔ’aʊtlɑ dɛ ˌɛspəˈnɔsɑ ˈvaɪrəs] or [ɔˌkɔsɔkɔ’aʊtlɑ ˌdiəspəˈnoʊzə ˈvaɪrəs]

aw-kaw-saw-kaw-out-lah deh es-puh-naw-sah (dee-uhs-puh-noh-zuh) vahy-ruhs

Oliveros virus

[ɔli’vɛrɔs ˈvaɪrəs] or [ɒli’vɛəroʊz ˈvaɪrəs]

aw-lee-veh-raws (o-lee-vair-ohz) vahy-ruhs

Orogrande virus

[ˌɔrɔ’grændi ‘vaɪrəs] or [ˌɔrɔ’grɑndeɪ ˈvaɪrəs]

aw-raw-gran-dee (aw-raw-grahn-dey) vahy-ruhs

Paraná virus

[ˌpærəˈnɑ ˈvaɪrəs]

par-uh-nah vahy-ruhs

Pichindé virus

[ˌpitʃin’dɛ ˈvaɪrəs] or [ˌpitʃin’deɪ ˈvaɪrəs]

pee-cheen-deh (pee-cheen-dey) vahy-ruhs

Pinhal virus

[pin’yɑl ‘vaɪrəs] or [pi’nyɑʊ ˈvaɪrəs]

peen-yahl (pee-nyow) vahy-ruhs

Pirital virus

[piri’tɑl ˈvaɪrəs]

pee-ree-tahl vahy-ruhs

Real de Catorce virus

[rɛ’ɑl dɛ kə’tɔrsə ˈvaɪrəs] or [reɪ’ɑl deɪ kə’tɔrzeɪ ˈvaɪrəs]

reh-ahl deh kuh-tawrs-uh (rey-ahl dey kuh-tawrz-ey) vahy-ruhs

reptarenavirus

[rɛptəˈrinəˌvaɪrəs] or [rɛptˌerənə’vaɪrəs]

rept-uh-ree-nuh-vahy-ruhs (rept-er-uh-nuh-vahy-ruhs)

Río Carcarañá virus

[ˈrioʊ ˌkɑrkɑran’yɑ ‘vaɪrəs]

ree-oh kahr-kahr-ahn-yah vahy-ruhs

ROUT virus

[raʊt ‘vaɪrəs]

rout vahy-ruhs

Sabiá virus

[ˌsɑbi’jɑ ˈvaɪrəs] or [ˌsəbi’ja ˈvaɪrəs]

sah-bee-yah (suh-bee-yah) vahy-ruhs

Skinner Tank virus

[ˈskɪnər tæŋk ˈvaɪrəs]

skin-er tangk vahy-ruhs

Tacaribe virus

[ˌtɑkɑ’ribɛ ˈvaɪrəs] or [ˌtəkə’ribeɪ ˈvaɪrəs]

tah-kah-ree-beh (tuh-kuh-ree-bey) vahy-ruhs

Tamiami virus

[ˈtæmiˌæmi ˈvaɪrəs]

ta-mee-a-mee vahy-ruhs

Tonto Creek virus

[‘tɔntoʊ krik ˈvaɪrəs] or [‘tɒntoʊ ˈvaɪrəs]

tawn-toh (ton-toh) kreek vahy-ruhs

University of Helsinki virus

[ˌyunəˈvɜrsɪti ʌv ‘hɛlsɪŋkɪ ‘vaɪrəs]

yoo-nuh-vur-si-tee uhv hel-sing-kee vahy-ruhs

Whitewater Arroyo virus

[ˈʰwaɪtˌwɒtər ə’rɔɪoʊ ˈvaɪrəs]

hwahyt-wot-er uh-roi-oh vahy-ruhs

aThe pronunciations of the word stems depicted here for virus names are to be used for species names as well

bConventions of http://dictionary.reference.com/

cTwo variants are included for words of foreign origin that do not have an established pronunciation in English. The first variant is closer to the pronunciation in the original language, and the second one is more anglicized

dIn the English respelling system, the italics signify a slightly different vowel, e.g., uh vs. uh is equivalent to [ə], as in virus vs. [ʌ] as in brush; oo vs. oo is equivalent to [uː] as in boot vs. [ʊ] as in put

Notes

Acknowledgments

We would like to thank Laura Bollinger and Jiro Wada of the IRF-Frederick for critically editing the manuscript and creating/editing figures.

References

  1. 1.
    Adams MJ, Carstens EB (2012) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2012). Arch Virol 157:1411–1422PubMedGoogle Scholar
  2. 2.
    Adams MJ, King AMQ, Carstens EB (2013) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses. Arch Virol 158:2023–2030PubMedGoogle Scholar
  3. 3.
    Adams MJ, Lefkowitz EJ, King AM, Carstens EB (2013) Recently agreed changes to the International Code of Virus Classification and Nomenclature. Arch Virol 158:2633–2639PubMedGoogle Scholar
  4. 4.
    Albariño CG, Posik DM, Ghiringhelli PD, Lozano ME, Romanowski V (1998) Arenavirus phylogeny: a new insight. Virus Genes 16:39–46PubMedGoogle Scholar
  5. 5.
    Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C, Chan AM, Haynes M, Kelley S, Liu H, Mahaffy JM, Mueller JE, Nulton J, Olson R, Parsons R, Rayhawk S, Suttle CA, Rohwer F (2006) The marine viromes of four oceanic regions. PLoS Biol 4:e368PubMedCentralPubMedGoogle Scholar
  6. 6.
    Archer AM, Rico-Hesse R (2002) High genetic divergence and recombination in arenaviruses from the Americas. Virology 304:274–281PubMedCentralPubMedGoogle Scholar
  7. 7.
    Armstrong C, Lillie RD (1934) Experimental lymphocytic choriomeningitis of monkeys and mice produced by a virus encountered in studies of the 1933 St. Louis encephalitis epidemic. Public Health Rep 49:1019–1027Google Scholar
  8. 8.
    Auperin DD, Compans RW, Bishop DH (1982) Nucleotide sequence conservation at the 3’ termini of the virion RNA species of New World and Old World arenaviruses. Virology 121:200–203PubMedGoogle Scholar
  9. 9.
    Auperin DD, Galinski M, Bishop DH (1984) The sequences of the N protein gene and intergenic region of the S RNA of Pichinde arenavirus. Virology 134:208–219PubMedGoogle Scholar
  10. 10.
    Ayers SB, Bradley RD (2011) Genetic Diversity in the Transferrin Receptor 1 (TfR1) Among Natural Hosts of the North American Arenaviruses. Museum of Texas Tech University Occasional Papers No 304. http://www.nsrlttuedu/publications/opapers/ops/OP304pdf
  11. 11.
    Bao Y, Kapustin Y, Tatusova T (2008) Virus classification by Pairwise Sequence Comparison (PASC). In: Mahy BWJ, Regenmortel MHV (eds) Encyclopedia of virology, 3rd edn. Academic Press, Oxford, pp 342–348Google Scholar
  12. 12.
    Bao Y, Chetvernin V, Tatusova T (2014) Improvements to pairwise sequence comparison (PASC), a genome-based web tool for virus classification. Arch Virol 159:3293–3304PubMedCentralPubMedGoogle Scholar
  13. 13.
    Beerenwinkel N, Gunthard HF, Roth V, Metzner KJ (2012) Challenges and opportunities in estimating viral genetic diversity from next-generation sequencing data. Front Microbiol 3:329PubMedCentralPubMedGoogle Scholar
  14. 14.
    Bodewes R, Kik MJ, Raj VS, Schapendonk CM, Haagmans BL, Smits SL, Osterhaus AD (2013) Detection of novel divergent arenaviruses in boid snakes with inclusion body disease in The Netherlands. J Gen Virol 94:1206–1210PubMedGoogle Scholar
  15. 15.
    Bodewes R, Raj VS, Kik MJ, Schapendonk CM, Haagmans BL, Smits SL, Osterhaus AD (2014) Updated phylogenetic analysis of arenaviruses detected in boid snakes. J Virol 88:1399–1400PubMedCentralPubMedGoogle Scholar
  16. 16.
    Borrow P, Oldstone MB (1994) Mechanism of lymphocytic choriomeningitis virus entry into cells. Virology 198:1–9PubMedGoogle Scholar
  17. 17.
    Bowen MD, Peters CJ, Nichol ST (1996) The phylogeny of New World (Tacaribe complex) arenaviruses. Virology 219:285–290PubMedGoogle Scholar
  18. 18.
    Bowen MD, Peters CJ, Nichol ST (1997) Phylogenetic analysis of the Arenaviridae: patterns of virus evolution and evidence for cospeciation between arenaviruses and their rodent hosts. Mol Phylogenet Evol 8:301–316PubMedGoogle Scholar
  19. 19.
    Bowen MD, Rollin PE, Ksiazek TG, Hustad HL, Bausch DG, Demby AH, Bajani MD, Peters CJ, Nichol ST (2000) Genetic diversity among Lassa virus strains. J Virol 74:6992–7004PubMedCentralPubMedGoogle Scholar
  20. 20.
    Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, Azam F, Rohwer F (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99:14250–14255PubMedCentralPubMedGoogle Scholar
  21. 21.
    Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J, Salamon P, Rohwer F (2003) Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185:6220–6223PubMedCentralPubMedGoogle Scholar
  22. 22.
    Breitbart M, Rohwer F (2005) Method for discovering novel DNA viruses in blood using viral particle selection and shotgun sequencing. BioTechniques 39:729–736PubMedGoogle Scholar
  23. 23.
    Breitbart M, Rohwer F (2005) Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13:278–284PubMedGoogle Scholar
  24. 24.
    Breitbart M, Haynes M, Kelley S, Angly F, Edwards RA, Felts B, Mahaffy JM, Mueller J, Nulton J, Rayhawk S, Rodriguez-Brito B, Salamon P, Rohwer F (2008) Viral diversity and dynamics in an infant gut. Res Microbiol 159:367–373PubMedGoogle Scholar
  25. 25.
    Briese T, Paweska JT, McMullan LK, Hutchison SK, Street C, Palacios G, Khristova ML, Weyer J, Swanepoel R, Egholm M, Nichol ST, Lipkin WI (2009) Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathog 5:e1000455PubMedCentralPubMedGoogle Scholar
  26. 26.
    Buchmeier MJ, Southern PJ, Parekh BS, Wooddell MK, Oldstone MB (1987) Site-specific antibodies define a cleavage site conserved among arenavirus GP-C glycoproteins. J Virol 61:982–985PubMedCentralPubMedGoogle Scholar
  27. 27.
    Buchmeier MJ, Clegg JCS, Franze-Fernandez MT, Kolakofsky D, Peters CJ, Southern PJ (1995) Family Arenaviridae. In: Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD (eds) Virus taxonomy—Sixth Report of the International Committee on Taxonomy of Viruses Archives of Virology Supplement, vol 10., SpringerVienna, Austria, pp 319–323Google Scholar
  28. 28.
    Buchmeier MJ (2002) Arenaviruses: protein structure and function. Curr Top Microbiol Immunol 262:159–173PubMedGoogle Scholar
  29. 29.
    Buchmeier MJ, de La Torre JC, Peters CJ (2006) Arenaviridae: the viruses and their replication. In: Knipe DM, Howley PM (eds) Fields virology, 5th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1791–1827Google Scholar
  30. 30.
    Buckley SM, Casals J (1970) Lassa fever, a new virus disease of man from West Africa. 3. Isolation and characterization of the virus. Am J Trop Med Hyg 19:680–691PubMedGoogle Scholar
  31. 31.
    Cajimat MN, Fulhorst CF (2004) Phylogeny of the Venezuelan arenaviruses. Virus Res 102:199–206PubMedGoogle Scholar
  32. 32.
    Cajimat MN, Milazzo ML, Hess BD, Rood MP, Fulhorst CF (2007) Principal host relationships and evolutionary history of the North American arenaviruses. Virology 367:235–243PubMedCentralPubMedGoogle Scholar
  33. 33.
    Cajimat MN, Milazzo ML, Bradley RD, Fulhorst CF (2012) Ocozocoautla de espinosa virus and hemorrhagic fever, Mexico. Emerg Infect Dis 18:401–405PubMedCentralPubMedGoogle Scholar
  34. 34.
    Cajimat MN, Milazzo ML, Mauldin MR, Bradley RD, Fulhorst CF (2013) Diversity among Tacaribe serocomplex viruses (Family Arenaviridae) associated with the southern plains woodrat (Neotoma micropus). Virus Res 178:486–494PubMedCentralPubMedGoogle Scholar
  35. 35.
    Cajimat MNB, Milazzo ML, Borchert JN, Abbott KD, Bradley RD, Fulhorst CF (2008) Diversity among Tacaribe serocomplex viruses (family Arenaviridae) naturally associated with the Mexican woodrat (Neotoma mexicana). Virus Res 133:211–217PubMedCentralPubMedGoogle Scholar
  36. 36.
    Calisher CH, TzianaboT Lord RD, Coleman PH (1970) Tamiami virus, a new member of Tacaribe group. Am J Trop Med Hyg 19:520PubMedGoogle Scholar
  37. 37.
    Carrion R Jr, Brasky K, Mansfield K, Johnson C, Gonzales M, Ticer A, Lukashevich I, Tardif S, Patterson J (2007) Lassa virus infection in experimentally infected marmosets: liver pathology and immunophenotypic alterations in target tissues. J Virol 81:6482–6490PubMedCentralPubMedGoogle Scholar
  38. 38.
    Charrel RN, de Lamballerie X, Fulhorst CF (2001) The Whitewater Arroyo virus: natural evidence for genetic recombination among Tacaribe serocomplex viruses (family Arenaviridae). Virology 283:161–166PubMedGoogle Scholar
  39. 39.
    Charrel RN, Feldmann H, Fulhorst CF, Khelifa R, de Chesse R, de Lamballerie X (2002) Phylogeny of New World arenaviruses based on the complete coding sequences of the small genomic segment identified an evolutionary lineage produced by intrasegmental recombination. Biochem Biophys Res Commun 296:1118–1124PubMedGoogle Scholar
  40. 40.
    Charrel RN, de Lamballerie X (2003) Arenaviruses other than Lassa virus. Antiviral Res 57:89–100PubMedGoogle Scholar
  41. 41.
    Charrel RN, Lemasson JJ, Garbutt M, Khelifa R, De Micco P, Feldmann H, de Lamballerie X (2003) New insights into the evolutionary relationships between arenaviruses provided by comparative analysis of small and large segment sequences. Virology 317:191–196PubMedGoogle Scholar
  42. 42.
    Clegg JC (2002) Molecular phylogeny of the arenaviruses. Curr Top Microbiol Immunol 262:1–24PubMedGoogle Scholar
  43. 43.
    Clegg JCS, Bowen MD, Buchmeier MJ, Gonzalez JP, Lukashevich IS, Peters CJ, Rico-Hesse R, Romanowski V (2000) Family Arenaviridae. In: van Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB (eds) Virus taxonomy—seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, pp 633–640Google Scholar
  44. 44.
    Cornu TI, de la Torre JC (2001) RING finger Z protein of lymphocytic choriomeningitis virus (LCMV) inhibits transcription and RNA replication of an LCMV S-segment minigenome. J Virol 75:9415–9426PubMedCentralPubMedGoogle Scholar
  45. 45.
    Cornu TI, de la Torre JC (2002) Characterization of the arenavirus RING finger Z protein regions required for Z-mediated inhibition of viral RNA synthesis. J Virol 76:6678–6688PubMedCentralPubMedGoogle Scholar
  46. 46.
    Cornu TI, Feldmann H, de la Torre JC (2004) Cells expressing the RING finger Z protein are resistant to arenavirus infection. J Virol 78:2979–2983PubMedCentralPubMedGoogle Scholar
  47. 47.
    Coulibaly-N’Golo D, Allali B, Kouassi SK, Fichet-Calvet E, Becker-Ziaja B, Rieger T, Olschlager S, Dosso H, Denys C, Ter Meulen J, Akoua-Koffi C, Günther S (2011) Novel arenavirus sequences in Hylomyscus sp. and Mus (Nannomys) setulosus from Côte d’Ivoire: implications for evolution of arenaviruses in Africa. PLoS ONE 6:e20893PubMedCentralPubMedGoogle Scholar
  48. 48.
    Dalton AJ, Rowe WP, Smith GH, Wilsnack RE, Pugh WE (1968) Morphological and cytochemical studies on lymphocytic choriomeningitis virus. J Virol 2:1465–1478PubMedCentralPubMedGoogle Scholar
  49. 49.
    Delgado S, Erickson BR, Agudo R, Blair PJ, Vallejo E, Albariño CG, Vargas J, Comer JA, Rollin PE, Ksiazek TG, Olson JG, Nichol ST (2008) Chapare virus, a newly discovered arenavirus isolated from a fatal hemorrhagic fever case in Bolivia. PLoS Pathog 4:e1000047PubMedCentralPubMedGoogle Scholar
  50. 50.
    Djikeng A, Spiro D (2008) Advancing full length genome sequencing for human RNA viral pathogens. Future Virol 4:47–53Google Scholar
  51. 51.
    Donaldson EF, Haskew AN, Gates JE, Huynh J, Moore CJ, Frieman MB (2010) Metagenomic analysis of the viromes of three North American bat species: viral diversity among different bat species that share a common habitat. J Virol 84:13004–13018PubMedCentralPubMedGoogle Scholar
  52. 52.
    Downs WG, Anderson CR, Spence L, Aitken TH, Greenhall AH (1963) Tacaribe virus, a new agent isolated from Artibeus bats and mosquitoes in Trinidad, West Indies. Am J Trop Med Hyg 12:640–646PubMedGoogle Scholar
  53. 53.
    Drexler JF, Corman VM, Muller MA, Maganga GD, Vallo P, Binger T, Gloza-Rausch F, Rasche A, Yordanov S, Seebens A, Oppong S, Adu Sarkodie Y, Pongombo C, Lukashev AN, Schmidt-Chanasit J, Stocker A, Carneiro AJ, Erbar S, Maisner A, Fronhoffs F, Buettner R, Kalko EK, Kruppa T, Franke CR, Kallies R, Yandoko ER, Herrler G, Reusken C, Hassanin A, Kruger DH, Matthee S, Ulrich RG, Leroy EM, Drosten C (2012) Bats host major mammalian paramyxoviruses. Nat Commun 3:796PubMedCentralPubMedGoogle Scholar
  54. 54.
    Eichler R, Strecker T, Kolesnikova L, ter Meulen J, Weissenhorn W, Becker S, Klenk HD, Garten W, Lenz O (2004) Characterization of the Lassa virus matrix protein Z: electron microscopic study of virus-like particles and interaction with the nucleoprotein (NP). Virus Res 100:249–255PubMedGoogle Scholar
  55. 55.
    Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) (2005) Virus taxonomy—Eighth Report of the International Committee on Taxonomy of Viruses. Academic Press, San DiegoGoogle Scholar
  56. 56.
    Fenner F (1976) Classification and nomenclature of viruses. Second Report of the International Committee on Taxonomy of Viruses. Intervirology 7:1–115PubMedGoogle Scholar
  57. 57.
    Finkbeiner SR, Allred AF, Tarr PI, Klein EJ, Kirkwood CD, Wang D (2008) Metagenomic analysis of human diarrhea: viral detection and discovery. PLoS pathogens 4:e1000011PubMedCentralPubMedGoogle Scholar
  58. 58.
    Frame JD, Baldwin JM Jr, Gocke DJ, Troup JM (1970) Lassa fever, a new virus disease of man from West Africa. I. Clinical description and pathological findings. Am J Trop Med Hyg 19:670–676PubMedGoogle Scholar
  59. 59.
    Francki RIB, Fauquet CM, Knudson DL, Brown F (1991) Classification and nomenclature of viruses—Fifth Report of the International Committee on Taxonomy of Viruses. Springer, ViennaGoogle Scholar
  60. 60.
    Fulhorst CF, Bennett SG, Milazzo ML, Murray HL Jr, Webb JP Jr, Cajimat MN, Bradley RD (2002) Bear Canyon virus: an arenavirus naturally associated with the California mouse (Peromyscus californicus). Emerg Infect Dis 8:717–721PubMedCentralPubMedGoogle Scholar
  61. 61.
    Fuller-Pace FV, Southern PJ (1989) Detection of virus-specific RNA-dependent RNA polymerase activity in extracts from cells infected with lymphocytic choriomeningitis virus: in vitro synthesis of full-length viral RNA species. J Virol 63:1938–1944PubMedCentralPubMedGoogle Scholar
  62. 62.
    Garcin D, Kolakofsky D (1990) A novel mechanism for the initiation of Tacaribe arenavirus genome replication. J Virol 64:6196–6203PubMedCentralPubMedGoogle Scholar
  63. 63.
    Garcin D, Kolakofsky D (1992) Tacaribe arenavirus RNA synthesis in vitro is primer dependent and suggests an unusual model for the initiation of genome replication. J Virol 66:1370–1376PubMedCentralPubMedGoogle Scholar
  64. 64.
    Garcin D, Rochat S, Kolakofsky D (1993) The Tacaribe arenavirus small zinc finger protein is required for both mRNA synthesis and genome replication. J Virol 67:807–812PubMedCentralPubMedGoogle Scholar
  65. 65.
    Harnish DG, Polyak SJ, Rawls WE (1993) Arenavirus replication: molecular dissection of the role of protein and RNA. In: Salvato MS (ed) The Arenaviridae. Plenum Press, New York, pp 157–174Google Scholar
  66. 66.
    Hass M, Westerkofsky M, Muller S, Becker-Ziaja B, Busch C, Günther S (2006) Mutational analysis of the Lassa virus promoter. J Virol 80:12414–12419PubMedCentralPubMedGoogle Scholar
  67. 67.
    Hetzel U, Sironen T, Laurinmaki P, Liljeroos L, Patjas A, Henttonen H, Vaheri A, Artelt A, Kipar A, Butcher SJ, Vapalahti O, Hepojoki J (2013) Isolation, identification, and characterization of novel arenaviruses, the etiological agents of boid inclusion body disease. J Virol 87:10918–10935PubMedCentralPubMedGoogle Scholar
  68. 68.
    Holmes EC (2009) RNA virus genomics: a world of possibilities. J Clin Invest 119:2488–2495PubMedCentralPubMedGoogle Scholar
  69. 69.
    Inizan CC, Cajimat MN, Milazzo ML, Barragan-Gomez A, Bradley RD, Fulhorst CF (2010) Genetic evidence for a Tacaribe serocomplex virus, Mexico. Emerg Infect Dis 16:1007–1010PubMedCentralPubMedGoogle Scholar
  70. 70.
    Ishii A, Thomas Y, Moonga L, Nakamura I, Ohnuma A, Hang’ombe BM, Takada A, Mweene AS, Sawa H (2012) Molecular surveillance and phylogenetic analysis of Old World arenaviruses in Zambia. J Gen Virol 93:2247–2251PubMedGoogle Scholar
  71. 71.
    Jay MT, Glaser C, Fulhorst CF (2005) The arenaviruses. J Am Vet Med Assoc 227:904–915PubMedGoogle Scholar
  72. 72.
    Johnson KM, Wiebenga NH, Mackenzie RB, Kuns ML, Tauraso NM, Shelokov A, Webb PA, Justines G, Beye HK (1965) Virus isolations from human cases of hemorrhagic fever in Bolivia. Proc Soc Exp Biol Med 118:113–118PubMedGoogle Scholar
  73. 73.
    Johnson KM, Kuns ML, Mackenzie RB, Webb PA, Yunker CE (1966) Isolation of Machupo virus from wild rodent Calomys callosus. Am J Trop Med Hyg 15:103–106PubMedGoogle Scholar
  74. 74.
    King A, Adams M, Carstens E, Lefkowitz E (eds) (2011) The international code of virus classification and nomenclature. In: Virus taxonomy—Ninth Report of the International Committee on Taxonomy of Viruses Elsevier/Academic Press, London, pp 1273–1277Google Scholar
  75. 75.
    Koellhoffer JF, Dai Z, Malashkevich VN, Stenglein MD, Liu Y, Toro R, Harrison JS, Chandran K, DeRisi JL, Almo SC, Lai JR (2014) Structural characterization of the glycoprotein GP2 core domain from the CAS virus, a novel arenavirus-like species. J Mol Biol 426:1452–1468PubMedCentralPubMedGoogle Scholar
  76. 76.
    Kranzusch PJ, Whelan SP (2011) Arenavirus Z protein controls viral RNA synthesis by locking a polymerase-promoter complex. Proc Natl Acad Sci USA 108:19743–19748PubMedCentralPubMedGoogle Scholar
  77. 77.
    Kranzusch PJ, Whelan SP (2012) Architecture and regulation of negative-strand viral enzymatic machinery. RNA Biol 9:941–948PubMedCentralPubMedGoogle Scholar
  78. 78.
    Kronmann KC, Nimo-Paintsil S, Guirguis F, Kronmann LC, Bonney K, Obiri-Danso K, Ampofo W, Fichet-Calvet E (2013) Two novel arenaviruses detected in pygmy mice, Ghana. Emerg Infect Dis 19:1832–1835PubMedCentralPubMedGoogle Scholar
  79. 79.
    Kunz S, Edelmann KH, de la Torre JC, Gorney R, Oldstone MB (2003) Mechanisms for lymphocytic choriomeningitis virus glycoprotein cleavage, transport, and incorporation into virions. Virology 314:168–178PubMedGoogle Scholar
  80. 80.
    Ladner JT, Beitzel B, Chain PS, Davenport MG, Donaldson E, Frieman M, Kugelman J, Kuhn JH, O’Rear J, Sabeti PC, Wentworth DE, Wiley MR, Yu G-Y, The Threat Characterization Consortium, Sozhamannan S, Bradburne C, Palacios G (2014) Standards for sequencing viral genomes in the era of high-throughput sequencing. mBio 5:e01360–01314Google Scholar
  81. 81.
    Lauber C, Gorbalenya AE (2012) Partitioning the genetic diversity of a virus family: approach and evaluation through a case study of picornaviruses. J Virol 86:3890–3904PubMedCentralPubMedGoogle Scholar
  82. 82.
    Lecompte E, Ter Meulen J, Emonet S, Daffis S, Charrel RN (2007) Genetic identification of Kodoko virus, a novel arenavirus of the African pigmy mouse (Mus Nannomys minutoides) in West Africa. Virology 364:178–183PubMedGoogle Scholar
  83. 83.
    Lenz O, ter Meulen J, Klenk HD, Seidah NG, Garten W (2001) The Lassa virus glycoprotein precursor GP-C is proteolytically processed by subtilase SKI-1/S1P. Proc Natl Acad Sci USA 98:12701–12705PubMedCentralPubMedGoogle Scholar
  84. 84.
    Leung WC, Ghosh HP, Rawls WE (1977) Strandedness of Pichinde virus RNA. J Virol 22:235–237PubMedCentralPubMedGoogle Scholar
  85. 85.
    Leung WC, Leung MF, Rawls WE (1979) Distinctive RNA transcriptase, polyadenylic acid polymerase, and polyuridylic acid polymerase activities associated with Pichinde virus. J Virol 30:98–107PubMedCentralPubMedGoogle Scholar
  86. 86.
    Li L, Victoria JG, Wang C, Jones M, Fellers GM, Kunz TH, Delwart E (2010) Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84:6955–6965PubMedCentralPubMedGoogle Scholar
  87. 87.
    Lopez N, Jacamo R, Franze-Fernandez MT (2001) Transcription and RNA replication of Tacaribe virus genome and antigenome analogs require N and L proteins: Z protein is an inhibitor of these processes. J Virol 75:12241–12251PubMedCentralPubMedGoogle Scholar
  88. 88.
    Lukashevich IS, Salvato MS (2006) Lassa virus genome. Curr Genomics 7:351–379Google Scholar
  89. 89.
    Mardis ER (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24:133–141PubMedGoogle Scholar
  90. 90.
    Martinez MG, Cordo SM, Candurra NA (2007) Characterization of Junín arenavirus cell entry. J Gen Virol 88:1776–1784PubMedGoogle Scholar
  91. 91.
    Matthews RE (1979) Third report of the International Committee on Taxonomy of Viruses. Classification and nomenclature of viruses. Intervirology 12:129–296PubMedGoogle Scholar
  92. 92.
    Matthews RE (1982) Classification and nomenclature of viruses. Fourth report of the International Committee on Taxonomy of Viruses. Intervirology 17:1–199Google Scholar
  93. 93.
    McNair STF, Rivers TM (1936) Meningitis in man caused by a filterable virus—I. Two cases and the method of obtaining a virus from their spinal fluids. J Exp Med 63:397–414Google Scholar
  94. 94.
    Mettler NE, Casals J, Shope RE (1963) Study of the antigenic relationships between Junín virus, the etiological agent of Argentinian hemorrhagic fever, and other arthropod-borne viruses. Am J Trop Med Hyg 12:647–652Google Scholar
  95. 95.
    Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11:31–46PubMedGoogle Scholar
  96. 96.
    Meyer BJ, Southern PJ (1993) Concurrent sequence analysis of 5’ and 3’ RNA termini by intramolecular circularization reveals 5’ nontemplated bases and 3’ terminal heterogeneity for lymphocytic choriomeningitis virus mRNAs. J Virol 67:2621–2627PubMedCentralPubMedGoogle Scholar
  97. 97.
    Meyer BJ, Southern PJ (1994) Sequence heterogeneity in the termini of lymphocytic choriomeningitis virus genomic and antigenomic RNAs. J Virol 68:7659–7664PubMedCentralPubMedGoogle Scholar
  98. 98.
    Meyer BJ, de la Torre JC, Southern PJ (2002) Arenaviruses: genomic RNAs, transcription, and replication. Curr Top Microbiol Immunol 262:139–157PubMedGoogle Scholar
  99. 99.
    Muhire B, Martin DP, Brown JK, Navas-Castillo J, Moriones E, Zerbini FM, Rivera-Bustamante R, Malathi VG, Briddon RW, Varsani A (2013) A genome-wide pairwise-identity-based proposal for the classification of viruses in the genus Mastrevirus (family Geminiviridae). Arch Virol 158:1411–1424PubMedGoogle Scholar
  100. 100.
    Murphy FA, Webb PA, Johnson KM, Whitfield SG (1969) Morphological comparison of Machupo with lymphocytic choriomeningitis virus: basis for a new taxonomic group. J Virol 4:535–541PubMedCentralPubMedGoogle Scholar
  101. 101.
    Murphy FA, Webb PA, Johnson KM, Whitfield SG, Chappell WA (1970) Arenoviruses in Vero cells: ultrastructural studies. J Virol 6:507–518PubMedCentralPubMedGoogle Scholar
  102. 102.
    Oldstone MB (2002) Arenaviruses. I. The epidemiology molecular and cell biology of arenaviruses. Introduction. Curr Top Microbiol Immunol 262:V–XIIGoogle Scholar
  103. 103.
    Palacios G, Druce J, Du L, Tran T, Birch C, Briese T, Conlan S, Quan PL, Hui J, Marshall J, Simons JF, Egholm M, Paddock CD, Shieh WJ, Goldsmith CS, Zaki SR, Catton M, Lipkin WI (2008) A new arenavirus in a cluster of fatal transplant-associated diseases. N Engl J Med 358:991–998PubMedGoogle Scholar
  104. 104.
    Palacios G, Savji N, Hui J, Travassos da Rosa A, Popov V, Briese T, Tesh R, Lipkin WI (2010) Genomic and phylogenetic characterization of Merino Walk virus, a novel arenavirus isolated in South Africa. J Gen Virol 91:1315–1324PubMedCentralPubMedGoogle Scholar
  105. 105.
    Parodi AS, Greenway DJ, Rugiero HR, Frigerio M, De La Barrera JM, Mettler N, Garzon F, Boxaca M, Guerrero L, Nota N (1958) Concerning the epidemic outbreak in Junín. El Dia Médico 30:2300–2301PubMedGoogle Scholar
  106. 106.
    Parodi AS, Rugiero HR, Greenway DJ, Mettler N, Martinez A, Boxaca M, De La Barrera JM (1959) Isolation of the Junín virus (epidemic hemorrhagic fever) from the mites of the epidemic area (Echinolaelaps echidninus, Barlese). Prensa Médica Argentina 46:2242–2244PubMedGoogle Scholar
  107. 107.
    Perez M, Craven RC, de la Torre JC (2003) The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci USA 100:12978–12983PubMedCentralPubMedGoogle Scholar
  108. 108.
    Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL (2011) The fecal viral flora of wild rodents. PLoS Pathog 7:e1002218PubMedCentralPubMedGoogle Scholar
  109. 109.
    Pinheiro FP, Shope RE, Deandrad Ah, Bensabat G, Cacios GV, Casals J (1966) Amaparí, a new virus of the Tacaribe group from rodents and mites of Amapá Territory, Brazil. Proc Soc Exp Biol Med 122:531Google Scholar
  110. 110.
    Pinschewer DD, Perez M, de la Torre JC (2003) Role of the virus nucleoprotein in the regulation of lymphocytic choriomeningitis virus transcription and RNA replication. J Virol 77:3882–3887PubMedCentralPubMedGoogle Scholar
  111. 111.
    Pinschewer DD, Perez M, de la Torre JC (2005) Dual role of the lymphocytic choriomeningitis virus intergenic region in transcription termination and virus propagation. J Virol 79:4519–4526PubMedCentralPubMedGoogle Scholar
  112. 112.
    Raju R, Raju L, Hacker D, Garcin D, Compans R, Kolakofsky D (1990) Nontemplated bases at the 5’ ends of Tacaribe virus mRNAs. Virology 174:53–59PubMedGoogle Scholar
  113. 113.
    Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI (2010) Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466:334–338PubMedCentralPubMedGoogle Scholar
  114. 114.
    Rivers TM, McNair Scott TF (1935) Meningitis in man caused by a filterable virus. Science 81:439–440PubMedGoogle Scholar
  115. 115.
    Rivers TM, McNair STF (1936) Meningitis in man caused by a filterable virus—II. Identification of the etiological agent. J Exp Med 63:415–432PubMedCentralPubMedGoogle Scholar
  116. 116.
    Rohwer F, Prangishvili D, Lindell D (2009) Roles of viruses in the environment. Environ Microbiol 11:2771–2774PubMedGoogle Scholar
  117. 117.
    Rowe WP, Murphy FA, Bergold GH, Casals J, Hotchin J, Johnson KM, Lehmann-Grube F, Mims CA, Traub E, Webb PA (1970) Arenoviruses: proposed name for a newly defined virus group. J Virol 5:651–652PubMedCentralPubMedGoogle Scholar
  118. 118.
    Rowe WP, Pugh WE, Webb PA, Peters CJ (1970) Serological relationship of the Tacaribe complex of viruses to lymphocytic choriomeningitis virus. J Virol 5:289–292PubMedCentralPubMedGoogle Scholar
  119. 119.
    Salazar-Bravo J, Ruedas LA, Yates TL (2002) Mammalian reservoirs of arenaviruses. Curr Top Microbiol Immunol 262:25–63PubMedGoogle Scholar
  120. 120.
    Salvato M, Shimomaye E, Oldstone MB (1989) The primary structure of the lymphocytic choriomeningitis virus L gene encodes a putative RNA polymerase. Virology 169:377–384PubMedGoogle Scholar
  121. 121.
    Salvato MS, Shimomaye EM (1989) The completed sequence of lymphocytic choriomeningitis virus reveals a unique RNA structure and a gene for a zinc finger protein. Virology 173:1–10PubMedGoogle Scholar
  122. 122.
    Salvato MS, Schweighofer KJ, Burns J, Shimomaye EM (1992) Biochemical and immunological evidence that the 11 kDa zinc-binding protein of lymphocytic choriomeningitis virus is a structural component of the virus. Virus Res 22:185–198PubMedGoogle Scholar
  123. 123.
    Salvato MS (ed) (1993) Molecular biology of the prototype arenavirus, lymphocytic choriomeningitis virus. In: The Arenaviridae. Plenum Press, New York, pp 133–156Google Scholar
  124. 124.
    Salvato MS, Clegg JCS, Buchmeier MJ, Charrel RN, Gonzalez JP, Lukashevich IS, Peters CJ, Romanowski V (2011) Family Arenaviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy—Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, pp 715–723Google Scholar
  125. 125.
    Schley D, Whittaker RJ, Neuman BW (2013) Arenavirus budding resulting from viral-protein-associated cell membrane curvature. J R Soc Interface 10:20130403PubMedCentralPubMedGoogle Scholar
  126. 126.
    Singh MK, Fuller-Pace FV, Buchmeier MJ, Southern PJ (1987) Analysis of the genomic L RNA segment from lymphocytic choriomeningitis virus. Virology 161:448–456PubMedGoogle Scholar
  127. 127.
    Southern PJ, Singh MK, Riviere Y, Jacoby DR, Buchmeier MJ, Oldstone MB (1987) Molecular characterization of the genomic S RNA segment from lymphocytic choriomeningitis virus. Virology 157:145–155PubMedGoogle Scholar
  128. 128.
    Speir RW, Wood O, Liebhaber H, Buckley SM (1970) Lassa fever, a new virus disease of man from West Africa. IV. Electron microscopy of Vero cell cultures infected with Lassa virus. Am J Trop Med Hyg 19:692–694PubMedGoogle Scholar
  129. 129.
    Stenglein MD, Sanders C, Kistler AL, Ruby JG, Franco JY, Reavill DR, Dunker F, DeRisi JL (2012) Identification, characterization, and in vitro culture of highly divergent arenaviruses from boa constrictors and annulated tree boas: candidate etiological agents for snake inclusion body disease. mBio 3:e00180–00112Google Scholar
  130. 130.
    Strecker T, Eichler R, Meulen J, Weissenhorn W, Dieter Klenk H, Garten W, Lenz O (2003) Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected]. J Virol 77:10700–10705PubMedCentralPubMedGoogle Scholar
  131. 131.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729PubMedCentralPubMedGoogle Scholar
  132. 132.
    Tortorici MA, Albariño CG, Posik DM, Ghiringhelli PD, Lozano ME, Rivera Pomar R, Romanowski V (2001) Arenavirus nucleocapsid protein displays a transcriptional antitermination activity in vivo. Virus Res 73:41–55PubMedGoogle Scholar
  133. 133.
    Trapido H, Sanmartin C (1971) Pichindé virus, a new virus of the Tacaribe group from Colombia. Am J Trop Med Hyg 20:631–641PubMedGoogle Scholar
  134. 134.
    Traub E (1935) A filterable virus recovered from white mice. Science 81:298–299PubMedGoogle Scholar
  135. 135.
    Van Regenmortel MH, Burke DS, Calisher CH, Dietzgen RG, Fauquet CM, Ghabrial SA, Jahrling PB, Johnson KM, Holbrook MR, Horzinek MC, Keil GM, Kuhn JH, Mahy BW, Martelli GP, Pringle C, Rybicki EP, Skern T, Tesh RB, Wahl-Jensen V, Walker PJ, Weaver SC (2010) A proposal to change existing virus species names to non-Latinized binomials. Arch Virol 155:1909–1919PubMedGoogle Scholar
  136. 136.
    Vela EM, Zhang L, Colpitts TM, Davey RA, Aronson JF (2007) Arenavirus entry occurs through a cholesterol-dependent, non-caveolar, clathrin-mediated endocytic mechanism. Virology 369:1–11PubMedCentralPubMedGoogle Scholar
  137. 137.
    Victoria JG, Kapoor A, Dupuis K, Schnurr DP, Delwart EL (2008) Rapid identification of known and new RNA viruses from animal tissues. PLoS Pathog 4:e1000163PubMedCentralPubMedGoogle Scholar
  138. 138.
    Vieth S, Torda AE, Asper M, Schmitz H, Günther S (2004) Sequence analysis of L RNA of Lassa virus. Virology 318:153–168PubMedGoogle Scholar
  139. 139.
    Webb PA (1965) Properties of Machupo virus. Am J Trop Med Hyg 14:799–802PubMedGoogle Scholar
  140. 140.
    Wiebenga NH, Shelokov A, Gibbs CJ Jr, Mackenzie RB (1964) Epidemic hemorrhagic fever in Bolivia. II. Demonstration of complement-fixing antibody in patients’ sera with Junín virus antigen. Am J Trop Med Hyg 13:626–628PubMedGoogle Scholar
  141. 141.
    Wildy P (1971) Classification and nomenclature of viruses. First Report of the International Committee on Nomenclature of Viruses. Monographs in Virology, vol 5. S. Karger, Basel, SwitzerlandGoogle Scholar
  142. 142.
    Willner D, Furlan M, Haynes M, Schmieder R, Angly FE, Silva J, Tammadoni S, Nosrat B, Conrad D, Rohwer F (2009) Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS ONE 4:e7370PubMedCentralPubMedGoogle Scholar
  143. 143.
    Wilson SM, Clegg JC (1991) Sequence analysis of the S RNA of the African arenavirus Mopeia: an unusual secondary structure feature in the intergenic region. Virology 180:543–552PubMedGoogle Scholar
  144. 144.
    Young PR, Howard CR (1983) Fine structure analysis of Pichinde virus nucleocapsids. J Gen Virol 64(Pt 4):833–842PubMedGoogle Scholar
  145. 145.
    Zhang T, Breitbart M, Lee WH, Run JQ, Wei CL, Soh SW, Hibberd ML, Liu ET, Rohwer F, Ruan Y (2006) RNA viral community in human feces: prevalence of plant pathogenic viruses. PLoS Biol 4:e3PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Sheli R. Radoshitzky
    • 1
  • Yīmíng Bào
    • 2
  • Michael J. Buchmeier
    • 3
  • Rémi N. Charrel
    • 4
    • 18
  • Anna N. Clawson
    • 5
  • Christopher S. Clegg
    • 6
  • Joseph L. DeRisi
    • 7
    • 8
    • 9
  • Sébastien Emonet
    • 10
  • Jean-Paul Gonzalez
    • 11
  • Jens H. Kuhn
    • 5
  • Igor S. Lukashevich
    • 12
  • Clarence J. Peters
    • 13
  • Victor Romanowski
    • 14
  • Maria S. Salvato
    • 15
  • Mark D. Stenglein
    • 16
  • Juan Carlos de la Torre
    • 17
  1. 1.United States Army Medical Research Institute of Infectious DiseasesFrederickUSA
  2. 2.Information Engineering Branch, National Center for Biotechnology Information, National Library of MedicineNational Institutes of HealthBethesdaUSA
  3. 3.Department of Molecular Biology and BiochemistryUniversity of CaliforniaIrvineUSA
  4. 4.Emergence des Pathologies Virales EPV UMR_D 190, Aix Marseille Université - IRD French Institute of Research for Development - EHESP French School of Public HealthMarseilleFrance
  5. 5.Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious DiseasesNational Institutes of HealthFrederickUSA
  6. 6.Les MandinauxLe Grand MadieuFrance
  7. 7.Department of MedicineUniversity of CaliforniaSan FranciscoUSA
  8. 8.Department of Biochemistry and BiophysicsUniversity of CaliforniaSan FranciscoUSA
  9. 9.Department of MicrobiologyUniversity of CaliforniaSan FranciscoUSA
  10. 10.Unité de VirologieL’Institut de Recherche Biomedicale de Armees (IRBA), Echelon Recherche de LyonLyonFrance
  11. 11.Metabiota, Inc., Emerging Diseases and BiosecurityWashingtonUSA
  12. 12.Department of Pharmacology and Toxicology, School of Medicine, Center for Predictive Medicine for Biodefense and Emerging Infectious DiseasesUniversity of LouisvilleLouisvilleUSA
  13. 13.Galveston National LaboratoryUniversity of Texas Medical BranchGalvestonUSA
  14. 14.Instituto de Biotecnología y Biología Molecular, CCT-La Plata, CONICET-UNLPLa PlataArgentina
  15. 15.Institute of Human VirologyUniversity of Maryland School of MedicineBaltimoreUSA
  16. 16.Department of Microbiology, Immunology and PathologyColorado State UniversityFort CollinsUSA
  17. 17.Department of Immunology and Microbial Science IMM-6The Scripps Research InstituteLa JollaUSA
  18. 18.Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, APHM Public Hospitals of MarseilleMarseilleFrance

Personalised recommendations