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Home , Bicaudaviridae, Globuloviridae, Hypovirus, Picovirinae, Sclerodarnavirus

Capsidless and noninfectious RNA are integral to the World

Valerian V. Dolja and Eugene V. Koonin DNA Viruses (DdDp; RCE; DdRp) dsDNA RNA-primed Virus Polydnaviridae Nucleo-cytplasmic large Nudivirus Protein-primed Nimaviridae DNA viruses (NCLDV) World Tectviridae Cortcoviridae Ampulaviridae Lipotrixviridae Fuseloviridae Rudiviridae Papilomaviridae Rolling-circle replicons RNA Viruses (RdRp; Rz) Inoviridae -like ssDNA +RNA Aneloviridae superfamily Narnaviridae -like Leviviridae Ourmiaviridae superfamily -like superfamily Retroid Viruses (RdDp; DdRp) Cystviridae Parttviridae Totviridae +RNA , , Reverse Picobirnaviridae Retoviridae Hepatts !" transcription Hypoviridae -RNA Arenaviridae dsRNA dsDNA Ortomyxoviridae

Ophioviridae Bunyaviridae Tenuivirus Varicosavirus Virus World is defined by viral hallmark genes

1. Jelly-roll capsid protein 3. RNA-dependent RNA 2. Superfamily 3 helicase polymerase and Reverse transcriptase

5. Viral archaeo-eukaryotic DNA primase

4. Rolling circle 6. UL9-like superfamily 2 helicase replication initiation endonuclease 7. Packaging ATPase of the FtsK family

8. ATPase subunit of terminase Genomes of RNA and RNA/DNA(RT) viruses

Viral RNA genomes (<30 kb): 1 kb

Hop stunt Hepatitis #" MS2 phage 3.6 kb (4) 1.7 kb (1) 0.3 kb (0) Hepatitis C virus 9.6 kb (10)

Citrus tristeza virus 19 kb (14)

SARS coronavirus 30 kb (14)

!!!Saccharomyces cerevisiae virus L-A 4.6 kb (3)

Colorado tick fever virus 29.2 kb; 12 segments (13)

Borna disease virus 8.9 kb (6) Ebola virus 19 kb (9) +RNA Influenza A virus 13.5 kb; 8 segments (11) -RNAzz

Cauliflower mosaic dsRNA Human immunodeficiency Hepatitis B virus 8 kb (7) virus 1 9.2 kb (9) virus +RNA RT 3.0 kb (7) dsDNA RT

Analysis of viral genome size shows the lower and upper limits of genome size for! ! RNA viruses and viroids: 0.3 – 30 kb ! Class of viruses or Replication/ Viral selfish elements expression cycle hallmark genes

Translation RdRp RdRp) mRNA Proteins Positive-strand RNA Progeny RdRp, +RNA Transcription ( Encapsidation (encapsidated +RNA) Replication (RdRp) Replication (RdRp) virions S3H, JRC -RNA +RNA

Translation Narnaviridae, RdRp, proteins Hypoviridae, +RNA RdRp , Replication (RdRp) Replication (RdRp) -RNA +RNA others

Transcription mRNA RdRp, proteins Double-strand RNA Progeny RdRp, (encapsidated dsRNA) dsRNA Encapsidation Replication (RdRp) virions JRC dsRNA

Transcription Translation Negative-strand RNA mRNA RdRp, proteins Progeny (encapsidated -RNA) -RNA Encapsidation (RdRp) Replication (RdRp) Replication (RdRp) virions +RNA -RNA

Translation mRNA RT, proteins Encapsi- Progeny +RNA Replication (RT) RT, INT (encapsidated +RNA) dsDNA dation virions Transcription (Pol II) +RNA

Group II introns; retrons; Translation RT, proteins LTR, non-LTR and Transcription (Pol II) mRNA dsDNA RT, INT Penelope-like +RNA Replication (RT) dsDNA retrotransposons; telomerase RT; others

Translation Pararetroviruses mRNA RT, proteins dsDNA Transcription (Pol II) Progeny RT (encapsidated dsDNA) Replication (RT) Encapsidation +RNA dsDNA virions Capsidless RNA viruses belong to distinct lineages of +RNA viruses

RdRp RdRp RdRp CP MP Narnaviridae BDRC-1/2; 2.0 kb; Floating genus replicons from 1 2 3 OMV-3a; 2.6 kb algal chloroplasts/ OMV; 4.9 kb mitochondria

RdRp MP MP Floating genus RdRp CP p33 Umbravirus p92 ORF4 TBSV; 4.8 kb GRV; 4.0 kb ORF2 p19 ORF1 ORF3

RdRp S2H Hypoviridae A pPro pPro n CHV-1; 12.7 kb p29 p40 p48

Potyviridae S2H RdRp CP P1-Pro HC-Pro P3 CI p6 VPg NIa NIb A TEV; 9.6 kb n

Met S2H S1H RdRp Endornaviridae Endornavirus GABrV-XL1; 10.4 kb MP Met S1H RdRp CP TMV; 6.4 kb Major lineages of +RNA viruses and capsidless +RNA elements

Picornavirus-like superfamily Fu Hypoviridae Luteoviridae Alphavirus-like superfamily Astroviridae BDRM, BDRC Fu Pl Oo Endornaviridae Flavivirus-like superfamily Virgaviridae Nidovirales Tombusviridae Umbravirus Pl SsRV-L Togaviridae ()

Ourmiaviridae Fu Narnaviridae RNA Fu Oo (Leviviridae) RNA-Protein Evolutionary scenario for World Primordial and ourmiaviruses RdRp

Leviviridae (+RNA bacteriophages) Emerging

Mitochondrial endosymbiont ancestral

loss of narnavirus- like elements Tombusviridae Narnaviridae (except fungi and (+RNA viruses) (fungal mitochondria- oomycetes) dwelling capsid-less viruses)

Extant

Mitochondrion

Ourmiaviridae (+RNA plant viruses)

Viruses constitute a minority Limited host range of bona fide among the RT viruses (vertebrates and

reverse-transcribing (DGR) ) attests to their selfish elements late arrival Chlamydomonas

Group II RT-like mitochondrial RT-like ORFs of Diversity-generating retroelements Retrons Retroplasmids introns

Gypsy LTR retro- Line non-LTR transposons () retrotranspososns Caulimoviridae (AP endonuclease)

pararetroviruses retroelements Retroid

Retroviridae and virus-like retroviruses Line non-LTR retrotransposons DIRS viruses (REL endonuclease) LTR retrotransposons (EP) non-LTR non-LTR Hepadnaviridae (TP) and RVT (TP) and RVT

retrotransposons RT-related cellular pararetroviruses genes (rvt) Copia LTR retro- transposons () Penelope-like BEL LTR retrotransposons Telomerase (PLE) RT (TERT) retro- transposons PLE and TERT (TP) Gladyshev & Arkhipova (2011) PNAS 108:20311 Fusarium oxysporum Lactococcus lactis Drosophila RD RD linear mitochondrial X/D/E RT Penelope-like Ll.LTrB group II intron RT retroplasmid pFOXC2 5r RT END ~2.5 kb +RNA retrotransposon 1.9 kb hairpin DNA ~3 kb +RNA Human LINE1 (L1) ORF1 ORF2 (ORF2p) non-LTR retrotransposon ORF1p END RT ZK 1 kb 6.0 kb +RNA

A continuity between Pseudoviridae CA encapsidated, infectious, bona Ty1-copia LTR R/ pol retrotransposons U5 gag U3/ fide viruses and capsidless and/ SceTy1V PR INT RT RH R 5.6 kb +RNA or non-infectious selfish genetic Hepadnaviridae TP P/RT RH elements is illuminated by the HBV DR1 DR2 3.2 kb PX/ reverse-transcribing entities pCore PreS circular dsDNA TA

Metaviridae Ty3-gypsy LTR C R/ pol U3/ retrotransposons U5 gag env R DmeGypV PR RT RH INT CHR 7.5 kb +RNA Retroviridae HIV-1 MA C NC 6 vif vpu R/ pol nef U3/ 9.2 kb U5 gp120 gp41 gag R +RNA PR RH INT vpr RT env tat rev decaying) occupysubstantialfraction of thegenomes Retrotransposons

Retrotransposon content (% genome) 60 80 20 40 42 Homo sapiens 36 Mus musculus andintegratedretroviruses(often 27 27 Aedes aegypti 0.6 Caenorabditis elegans 3 Saccharomyces cerevisiae Fungi

5 Magnaporthe grisea 11 Entamoeba histolytica Amoebozoa

5 Trypanosoma cruzi Excavates

6 Phaeodactylum tricornutum Stramenopiles (diatom) 4

Arabidopsis thaliana Plants

21 Brachypodium distachyon mays Zea 75

Evolutionary scenario for the evolution Retro of retroelements and the origin of World retroviruses Primordial RT

DNA World Retrons Group II intron RT

Maturase, HNH Spliceosomal endonuclease introns

Group II introns AP or REL endonucleases GYI-IYG endonuclease

Line retro- Penelope-like transposons retrotransposons TERT

Pseudoviridae Integrase (DNA transposon) Loss of Aspartic protease Metaviridae (LTR env & INT and RNase H retrotransposons) Caulimoviridae (eukaryotic genome)

Gag and Env

Retroviridae Hepadnaviridae Viruses were recently defined as capsid-encoding entities as opposed to ribosome-encoding cellular organisms

This definition excludes selfish genetic elements many of which possess viral hallmark genes and share origins with viruses

The phylogenomic analysis of a broader Virus World inclusive of all selfish genetic elements is needed to understand the entire network of virus evolution