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Archives of Virology

, Volume 163, Issue 7, pp 2005–2015 | Cite as

Smacoviridae: a new family of animal-associated single-stranded DNA viruses

  • Arvind Varsani
  • Mart Krupovic
Virology Division News

Abstract

Smacoviruses have small (∼2.3-2.9 kb), circular single-stranded DNA genomes encoding rolling circle replication-associated proteins (Rep) and unique capsid proteins. Although smacoviruses are prevalent in faecal matter of various vertebrates, including humans, none of these viruses have been cultured thus far. Smacoviruses display ∼45% genome-wide sequence diversity, which is very similar to that found within other families of circular Rep-encoding single-stranded (CRESS) DNA viruses, including members of the families Geminiviridae (46% diversity) and Genomoviridae (47% diversity). Here, we announce the creation of a new family Smacoviridae and describe a sequence-based taxonomic framework which was used to classify 83 smacovirus genomes into 43 species within six new genera, Bovismacovirus (n=3), Cosmacovirus (n=1), Dragsmacovirus (n=1), Drosmacovirus (n=3), Huchismacovirus (n=7), and Porprismacovirus (n=28). As in the case of genomoviruses, the species demarcation is based on the genome-wide pairwise identity, whereas genera are established based on the Rep amino acid sequence identity coupled with strong phylogenetic support. A similar sequence-based taxonomic framework should guide the classification of an astonishing diversity of other uncultured and currently unclassified CRESS DNA viruses discovered by metagenomic approaches.

With the advent of metagenomics approaches, a large diversity of unknown viruses has been uncovered in various environmental, plant, and animal samples [23]. Sampling of animal faecal matter has proved to be particularly efficient for the discovery of a wide variety of novel viral types, in particular those with small DNA genomes. Until recently, the circular replication-initiation protein encoding single-stranded (CRESS) DNA viruses associated with eukaryotic hosts have been classified by the International Committee on Taxonomy of Viruses (ICTV) into four families, namely Circoviridae, Genomoviridae, Geminiviridae and Nanoviridae. In 2018, the ICTV created two new families for classification of CRESS DNA viruses, Bacilladnaviridae and Smacoviridae. The family Bacilladnaviridae, which includes viruses infecting diatoms, a major group of unicellular algae widespread in aquatic habitats, has been described elsewhere [7]. Here, we introduce the family Smacoviridae (smaco- stands for small circular DNA viruses) and describe the ICTV-approved sequence-based taxonomic framework for classification of these viruses.

Smacoviruses [15, 17], previously also referred to as chipoviruses [22, 24], have been identified in faecal matter of various vertebrates, including humans, as well as in the abdomina of dragonflies of two species (Table 1). Thus far, none of these viruses have been cultured or found in animal tissue sample. Nonetheless, the viruses have been discovered using viral metagenomics approaches and for the majority of the smacoviruses, the validity of genome sequences has been verified by either PCR amplification using abutting primers followed by Sanger sequencing of these products or by amplification, cloning and Sanger sequencing of the recombinant plasmids [1, 3, 4, 9, 15, 22, 24].
Table 1

Summary of taxa that are part of the family Smacoviridae

Genus

Species

Accession #

Isolate

Isolation source

Host

Host species

Country

Reference

Bovismacovirus

Bovine associated bovismacovirus 1

JN634851

CP11-49-3

Domestic cow

Bos taurus

South Korea

[9]

 

Bovine associated bovismacovirus 2

KT862222

48_Fec5_cow

Domestic cow

Bos taurus

New Zealand

[24]

 

Dragonfly associated bovismacovirus 1

KM598409

OdasCV-21-US-1679SC3-12

Red-faced Dragonlet

Erythrodiplax fusca

USA

[4]

Drosmacovirus

Camel associated drosmacovirus 1

KM573769

DcSCV_c1359

One-humped camel

Camelus dromedarius

United Arab Emirates

[26]

 

Camel associated drosmacovirus2

KM573774

DcSCV_c1330

One-humped camel

Camelus dromedarius

United Arab Emirates

[26]

 

Bovine associated drosmacovirus 1

KT862224

48_Fec9_cow

Domestic cow

Bos taurus

New Zealand

[24]

Huchismacovirus

Bovine associated huchismacovirus 1

KT862223

48_Fec59973_cow

Domestic cow

Bos taurus

New Zealand

[24]

 

Bovine associated huchismacovirus 2

KT862229

GP3_46075_cow

Domestic cow

Bos taurus

New Zealand

[24]

 

Chicken associated huchismacovirus 1

KY086301

RS/BR/2015/2

Domestic chicken

Gallus gallus

Brazil

[13]

 

Chicken associated huchismacovirus 2

KY086300

RS/BR/2015/3

Domestic chicken

Gallus gallus

Brazil

[13]

 

Human associated huchismacovirus 1

KP233180

Oregon/6/2011/GottageGrove/5A1

Human

Homo sapiens

USA

[15]

  

KP233181

Oregon/6/2011/GottageGrove/B3

Human

Homo sapiens

USA

[15]

  

KP233182

Oregon/6/2011/GottageGrove/B45

Human

Homo sapiens

USA

[15]

  

KP233183

Oregon/8/2011/Portland/D56

Human

Homo sapiens

USA

[15]

  

KP233185

Virginia/2/2012/Albemarle/5I17

Human

Homo sapiens

USA

[15]

  

KP233186

Virginia/2/2012/Chesapeake/J23

Human

Homo sapiens

USA

[15]

  

KP233188

Virginia/12/2011/Albemarle/G16

Human

Homo sapiens

USA

[15]

  

KP233193

Orgeon/8/2011/Portland/D53

Human

Homo sapiens

USA

[15]

  

KP264964

France/2/2008/2548

Human

Homo sapiens

France

[15]

  

KP264966

France/12/2008/3454

Human

Homo sapiens

France

[15]

  

KP264969

France/6/2008/2871

Human

Homo sapiens

France

[15]

  

KY086299

RS/BR/2015/4

Domestic chicken

Gallus gallus

Brazil

[13]

 

Human associated huchismacovirus 2

KP233174

France/8/2008/2444

Human

Homo sapiens

France

[15]

  

KP233175

France/1/2008/2610

Human

Homo sapiens

France

[15]

  

KP233176

France/8/2008/2449

Human

Homo sapiens

France

[15]

  

KP233177

France/4/2009/4265

Human

Homo sapiens

France

[15]

  

KP233184

Virginia/1/2012/Mecklenburg/H19

Human

Homo sapiens

USA

[15]

  

KP233187

Virginia/2/2012/Middlesex/I22

Human

Homo sapiens

USA

[15]

  

KP264965

France/3/2008/2623

Human

Homo sapiens

France

[15]

  

KP264967

France/12/2008/3454

Human

Homo sapiens

France

[15]

 

Human associated huchismacovirus 3

KP233178

France/1/2009/3664

Human

Homo sapiens

France

[15]

  

KP233179

France/1/2009/3663

Human

Homo sapiens

France

[15]

  

KP264968

France/3/2009/4191

Human

Homo sapiens

France

[15]

Porprismacovirus

Bovine associated porprismacovirus 1

KT862218

23_Fec30587_cow

Domestic cow

Bos taurus

New Zealand

[24]

 

Camel associated porprismacovirus 1

KM573772

DcSCV_c1378

One-humped camel

Camelus dromedarius

United Arab Emirates

[26]

 

Camel associated porprismacovirus 2

KM573770

DcSCV_c1072

One-humped camel

Camelus dromedarius

United Arab Emirates

[26]

 

Camel associated porprismacovirus 3

KM573771

DcSCV_c1345

One-humped camel

Camelus dromedarius

United Arab Emirates

[26]

 

Camel associated porprismacovirus 4

KM573775

DcSCV_c1358

One-humped camel

Camelus dromedarius

United Arab Emirates

[26]

 

Chimpanzee associated porprismacovirus 1

GQ351272

DP152

Common chimpanzee

Pan troglodytes

Cameroon

[1]

  

GQ351275

GM510

Common chimpanzee

Pan troglodytes

Tanzania

[1]

 

Chimpanzee associated porprismacovirus 2

GQ351273

GM495

Common chimpanzee

Pan troglodytes

Tanzania

[1]

  

GQ351274

GM476

Common chimpanzee

Pan troglodytes

Tanzania

[1]

  

GQ351276

GM488

Common chimpanzee

Pan troglodytes

Tanzania

[1]

  

GQ351277

GM415

Common chimpanzee

Pan troglodytes

Tanzania

[1]

 

Chicken associated porprismacovirus 1

KY086298

RS/BR/2015/1

Domestic chicken

Gallus gallus

Brazil

[13]

 

Gorilla associated porprismacovirus 1

KP233191

SF3

Western gorilla

Gorilla gorilla

USA

[15]

  

KP233192

SF4

Western gorilla

Gorilla gorilla

USA

[15]

 

Howler monkey associated porprismacovirus 1

KP233189

SF1

Black howler

Alouatta caraya

USA

[15]

 

Human associated porprismacovirus 1

KT600068

SmaCV2_ID31

Human

Homo sapiens

Peru

[17]

 

Human associated porprismacovirus 2

KP233190

SF2

Common chimpanzee

Pan troglodytes

USA

[15]

  

KT600069

SmaCV3_ID16

Human

Homo sapiens

Peru

[17]

  

KX838317

BWA1115

Human

Homo sapiens

Botswana

-

  

KX838318

BWA7684

Human

Homo sapiens

Botswana

-

 

Lemur associated porprismacovirus 1

KP233194

SF5

Ring-tailed lemur

Lemur catta

USA

[15]

 

Porcine associated porprismacovirus 1

JX274036

Cass

Domestic pig

Sus scrofa domesticus

New Zealand

[22]

  

KF193403

J481

Domestic pig

Sus scrofa domesticus

South Korea

[8]

  

KT862226

56_Coc3310_hare

European hare

Lepus europaeus

New Zealand

[24]

  

KT862227

59_Coc3310_possum

Common brushtail

Trichosurus vulpecula

New Zealand

[24]

 

Porcine associated porprismacovirus 2

KC545226

f

Domestic pig

Sus scrofa domesticus

USA

[2]

  

KJ577818

TP3

Domestic pig

Sus scrofa domesticus

USA

[3]

 

Porcine associated porprismacovirus 3

KC545227

3L7

Domestic pig

Sus scrofa domesticus

USA

[2]

  

KC545228

4L13

Domestic pig

Sus scrofa domesticus

USA

[2]

  

KC545229

4L5

Domestic pig

Sus scrofa domesticus

USA

[2]

  

KC545230

L2T

Domestic pig

Sus scrofa domesticus

USA

[2]

 

Porcine associated porprismacovirus 4

KJ577810

DP2

Domestic pig

Sus scrofa domesticus

USA

[3]

 

Porcine associated porprismacovirus 5

KJ577811

DP3

Domestic pig

Sus scrofa domesticus

USA

[3]

 

Porcine associated porprismacovirus 6

KJ577819

XP1

Domestic pig

Sus scrofa domesticus

USA

[3]

 

Porcine associated porprismacovirus 7

KJ577812

EP2-A

Domestic pig

Sus scrofa domesticus

USA

[3]

  

KJ577813

EP2-B

Domestic pig

Sus scrofa domesticus

USA

[3]

  

KJ577814

EP3-C

Domestic pig

Sus scrofa domesticus

USA

[3]

  

KJ577815

EP3-D

Domestic pig

Sus scrofa domesticus

USA

[3]

 

Porcine associated porprismacovirus 8

KJ577817

GP2

Domestic pig

Sus scrofa domesticus

USA

[3]

 

Porcine associated porprismacovirus 9

KJ577816

FP1

Domestic pig

Sus scrofa domesticus

USA

[3]

 

Porcine associated porprismacovirus 10

KT862225

49_Fec25_pig

Domestic pig

Sus scrofa domesticus

New Zealand

[24]

 

Rat associated porprismacovirus 1

KP860906

KS/11/0577

Brown rat

Rattus norvegicus

Germany

[21]

  

KP860907

Mu/10/1799

Brown rat

Rattus norvegicus

Germany

[21]

  

KP860908

KS/11/0582

Brown rat

Rattus norvegicus

Germany

[21]

 

Sheep associated porprismacovirus 1

KT862220

47_Fec58729_sheep

Sheep

Ovis aries

New Zealand

[24]

 

Sheep associated porprismacovirus 2

KT862221

47_Fec60415_sheep

Sheep

Ovis aries

New Zealand

[24]

 

Sheep associated porprismacovirus 3

KT862219

47_Fec58091_sheep

Sheep

Ovis aries

New Zealand

[24]

 

Turkey associated porprismacovirus 1

KF880727

TuSCV

Wild turkey

Meleagris gallopavo

Hungary

[19]

Cosmacovirus

Bovine associated cosmacovirus 1

KT862228

GP3_45917_cow

Domestic cow

Bos taurus

New Zealand

[24]

Dragsmacovirus

Dragonfly associated dragsmacovirus 1

KM598410

OdasCV-5-US-1683LM1-12

Four-spotted skimmer

Libellula quadrimaculata

USA

[4]

The genomes of currently identified smacoviruses are ~2300-2900 nucleotides-long, contain two major open reading frames (ORF), encoding the rolling circle replication-associated protein (Rep) and capsid protein (CP; Figure 1). The two ORFs in all 83 smacovirus genomes are bidirectionally organised, separated by two intergenic regions. Similar to other CRESS DNA viruses, smacoviruses contain a conserved nonanucleotide sequence located at a putative stem-loop structure at the origin of replication (Figure 1), where nicking of the dsDNA replicative intermediate is predicted to occur. The Reps of smacoviruses are homologous but phylogenetically distinct from those of classified CRESS DNA viruses (Figure 2). Phylogenetic analysis and comparison of the conserved sequence motifs suggest a closer evolutionary relationship between the smacovirus and nanovirus Reps [7]. By contrast, although conserved among smacoviruses, the CPs do not display recognizable sequence similarity to the CPs of other known viruses.
Fig. 1

Genome organization of a representative smacovirus (chimpanzee associated porprismacovirus 1 [GQ351272]) and a WebLogo of the nonanucleotide motif found in smacoviruses

Fig. 2

Unrooted approximate maximum likelihood phylogenetic tree of Reps of CRESS DNA viruses inferred using FastTree [18]. Major groups of classified CRESS DNA viruses as well as alphasatellites associated with geminiviruses and nanoviruses are colour coded

Analysis of the genome-wide pairwise identities of the 83 smacoviruses (Figure 3) shows 45% diversity amongst these genomes, which is similar to values determined for members of the families Geminiviridae [27] and Genomoviridae [12, 25]. The plot of the distribution of pairwise identities shows a trough between 76 and 88%. Hence, for this group of viruses, 77% genome-wide pairwise identity is chosen as a species demarcation threshold. Using this approach, the 83 smacoviruses were assigned to 43 species (Table 1).
Fig. 3

Distribution of pairwise identities of the full genome (upper panel), the replication initiation protein (middle panel) and the capsid protein sequences determined using SDT v1.2 [14]. The arrows indicate the thresholds of the full genome (top panel) and Rep protein (middle panel) pairwise sequence identities used as the species and genus demarcation criteria, respectively

Maximum likelihood phylogenetic analysis of the Rep sequences of all 83 smacoviruses reveals four main clusters with >90% branch support and two singletons (Figure 4). Rep sequences within each of the four clades in general share >40% pairwise identity, whereas sequences from different phylogenetic clades show less than 40% identity to each other. We note that phylogenetic trees produced using complete genome (Figure 5) and CP (Figure 6) sequences are not congruent with the Rep phylogeny, presumably due to intra-familial recombination between different smacovirus genomes resulting in chimeric entities encoding Rep and CP with different evolutionary histories, as has been also observed for genomoviruses [25]. Given that smacovirus Reps are considerably more conserved than CPs (Figure 3) and due to the fact that Reps are the only proteins shared across all CRESS DNA viruses [11, 20], genera were established based on the phylogenetic analysis of the Rep sequences coupled with their pairwise sequence identity. Accordingly, 40% Rep amino acid sequence identity coupled with strong phylogenetic support is proposed as a genus level demarcation threshold.
Fig. 4

Maximum likelihood phylogenetic tree of the Rep amino acid sequences of the smacoviruses inferred using PhyML [6] with the LG+G+I+F substitution model. The tree is rooted with the Rep sequences of nanoviruses

Fig. 5

Maximum likelihood phylogenetic tree of the genome sequences inferred using IQ-TREE [16] with K3Pu+I+G4 substitution model. Branches with <60% bootstrap support have been collapsed and the tree is mid-point rooted

Fig. 6

Maximum likelihood phylogenetic tree of the CP amino acid sequences of the smacoviruses inferred using PhyML [6] with the LG+G+I+F substitution model. The phylogenetic tree is mid-point rooted

The naming practice for smacoviruses and other uncultivated CRESS DNA viruses, such as genomoviruses [25], typically involves adoption of the name of an organism or material from which the virus genome has been sequenced. In the absence of evidence of actual infection, the word “associated” is usually added to the potential host name to emphasize that the organism may or may not be the actual host. As a case in point, it has been recently suggested that dsRNA viruses of the family Picobirnaviridae, which for three decades were considered to infect eukaryotes [5], might instead replicate in bacteria that populate the enteric tract of animals [10]. Thus, utmost caution should be exercised when assigning viruses to potential hosts.

The following names for the six genera within the Smacoviridae have been adopted

Bovismacovirus: Bovine smacovirus

3 species (Table 1);

Drosmacovirus: Dromedary smacovirus

3 species (Table 1);

Huchismacovirus: Human and chicken smacovirus

7 species (Table 1);

Porprismacovirus: Porcine and primate smacovirus

28 species (Table 1);

Cosmacovirus: Cow smacovirus

1 species (Table 1);

Dragsmacovirus: Dragonfly smacovirus.

1 species (Table 1).

We would like to note that the species Sheep associated porprismacovirus 3, Bovine associated huchismacovirus 1 and Bovine associated huchismacovirus 2 have been tentatively assigned to genera Porprismacovirus and Huchismacovirus. It is highly likely that, as more sequences become available, new genera will have to be created for these divergent smacoviruses (Figures 4 and 5).

Sequence based taxonomic framework employed here for smacoviruses and previously applied for genomoviruses [25] should guide the classification of an astonishing diversity of other uncultured CRESS DNA viruses described by metagenomic approaches.

Notes

Compliance with ethical standards

Conflict of interest

The authors declare there are no conflicts of interest.

Research involving human participants and/or animals

The research did not involve human participants or animals.

Informed consent

The research did not involve human participants or animals.

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Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.The Biodesign Center for Fundamental and Applied Microbiomics, School of Life Sciences, Center for Evolution and MedicineArizona State UniversityTempeUSA
  2. 2.Structural Biology Research Unit, Department of Clinical Laboratory SciencesUniversity of Cape TownObservatorySouth Africa
  3. 3.Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Department of MicrobiologyInstitut PasteurParisFrance

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