Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses
- National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, China
- Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, China
- Charles Perkins Centre, School of Biological Sciences and Sydney Medical School, The University of Sydney, Australia
- Wuhan Center for Disease Control and Prevention, China
- Wenzhou Center for Disease Control and Prevention, China
Figures
Figure 1
Host component of each pool used in the RNA-seq library construction and sequencing.
The taxonomic units in the tree correspond to the unit samples used in the RNA extraction. Species or genus information is marked to the left of the tree.
Figure 2
Abundance level (transcripts per million—TPM) of the RdRp genes from the negative-sense RNA viruses detected in this study.
Abundance is calculated after the removal of ribosomal RNA reads. As a comparison, we show the abundance of the two well characterized (positive-sense) RNA viruses: Japanese encephalitis virus and Gill-associated virus found in the Mosquito-Hubei and Shrimp libraries, respectively, as well as the range of abundance of host mitochondrial COI genes in these same multi-host libraries.
Figure 3 with 3 supplements
Evolutionary history of negative-sense RNA viruses based on RdRp.
This is initially displayed in an unrooted maximum likelihood (ML) tree including all major groups of negative-sense RNA viruses (A). Separate and more detailed ML phylogenies are then shown for the Orthomyxoviridae-like (B), Bunya-Arenaviridae-like (C), and Mononegavirales-like viruses (D). In all the phylogenies, the RdRp sequences described here from arthropods are either shaded purple or marked with solid gray circles. The names of previously defined genera/families are labeled to the right of the phylogenies. Based on their host types, the branches are shaded red (vertebrate-specific), yellow (vertebrate and arthropod), green (plant and arthropod), blue (non-arthropod invertebrates), or black (arthropod only). For clarity, statistical supports (i.e., approximate likelihood-ratio test (aLRT) with Shimodaira–Hasegawa-like procedure/posterior probabilities) are shown for key internal nodes only.
Figure 3—figure supplement 1
A fully labeled ML phylogeny for Orthomyxoviridae-like viruses.
The phylogeny is reconstructed using RdRp alignments. Statistical support from the approximate likelihood-ratio test (aLRT) is shown on each node of the tree. The names of the viruses discovered in this study are shown in red. The names of reference sequences, which contain both the GenBank accession number and the virus species name, are shown in black. The names of previously defined genera/families are shown to the right of the phylogenies.
Figure 3—figure supplement 2
A fully labeled ML phylogeny for Bunya-Arenaviridae-like viruses.
The phylogeny is reconstructed using RdRp alignments. Statistical support from the aLRT is shown on each node of the tree. The names of the viruses discovered in this study are shown in red. The names of reference sequences, which contain both the GenBank accession number and the virus species name, are shown in black. The names of previously defined genera/families are shown to the right of the phylogenies.
Figure 3—figure supplement 3
A fully labeled ML phylogeny for Mononegavirales-like viruses.
The phylogeny is reconstructed using RdRp alignments. Statistical support from the aLRT is shown on each node of the tree. The names of the viruses discovered in this study are shown in red. The names of reference sequences, which contain both the GenBank accession number and the virus species name, are shown in black. The names of previously defined genera/families are shown to the right of the phylogenies.
Figure 4
The unrooted ML phylogeny based on RdRp showing the topological position of segmented viruses within the genetic diversity of negative-sense RNA viruses.
The segmented viruses are labeled with segment numbers and shaded red. The unsegmented viruses are shaded green. The Chuviridae, which exhibit a wide variety of genome organizations, are shaded cyan. Three major types of putative chuvirus genomes (circular, circular and segmented, and linear) are shown in the right panel and are annotated with predicted ORFs: putative RdRp genes are shaded blue, putative glycoprotein genes are shaded orange, and the remaining ORFs are shaded gray.
Figure 5
The unrooted ML phylogeny of negative-sense RNA viruses (RdRp) with the common names of the principle arthropod hosts analyzed in this study indicated.
Vertebrate-specific viruses are shaded red, those infecting both vertebrates and arthropods (or with unknown vectors) are shaded yellow, those infecting both plants and arthropods are shaded green, those infecting non-arthropod invertebrates are shaded blue, and the remainder (arthropod only) are shaded black.
Figure 6
Phylogenetic congruence between viruses (M segments) and hosts.
The comparisons include (A) Wuhan Horsefly Virus, (B) Wuhan Fly Virus 1, (C) Wuhan Mosquito Virus 2, and (D) Wuhan Mosquito Virus 1. Different host species/genera are distinguished with different colors, which are then mapped onto virus phylogeny to assess the phylogenetic congruence. ML phylogenetic trees were inferred in all cases.
Figure 7
The differing genome organizations in the Chuviridae.
(A) ML trees of three main putative proteins conserved among the chuviruses. Viruses with circular genomes (Type I) are shaded blue, while those with segmented genomes (Type II) are shaded red. (B) Structures of all complete chuvirus genomes. Circular genomes are indicated with the arrow (blue) situated at the 3′ end, and the genome is drawn in a linear form for ease of comparison only, being broken at the region of variable sequence (refer to the ‘Materials and methods’). (C) An example showing mapping of sequencing reads to the circular chuvirus genome. The template for mapping contains two genomes connected head-to-tail. The two boxes magnify the genomic region containing abundant sequence variation.
Figure 8
Genome structures of segmented negative-sense RNA viruses.
Predicted viral proteins homologous to known viral proteins are shown and colored according to their putative functions. The numbers below each ORF box give the predicted molecular mass.
Figure 9
Genome structures of unsegmented negative-sense RNA viruses.
Predicted ORFs encoding viral proteins with >10 kDa molecular mass are shown and colored according to their putative functions. The numbers below each ORF box give the predicted molecular mass.
Figure 10
Comparison of the genome structure of a potential tenui-like virus from horsefly with a prototype tenuivirus (Rice grassy stunt virus) genome.
https://doi.org/10.7554/eLife.05378.019
Figure 11
ML phylogeny of EVEs.
The phylogeny is based on the glycoprotein of chuviruses in the context of exogenous members of this family (A), with subtrees magnified for (B) the Culicidae clade and (C) the Hymenoptera clade. The EVEs used in the phylogeny covered the complete or near complete length of the glycoprotein gene and are shown in red and labeled according to host taxonomy in the overall tree. For clarity, monophyletic groups are collapsed based on the host taxonomy. Only bootstrap values >70% are shown.
Figure 12
Transmission of negative-sense RNA viruses in arthropods and non-arthropods.
Three types of transmission cycle are shown: (i) those between arthropods and plants are shaded green; (ii) those between arthropods and vertebrates are shaded yellow; and (iii) those that are vertebrate-only are shaded red. Viruses associated with each transmission type are also indicated.
Tables
Table 1
Host and geographic information and data output for each pool of arthropod samples
| Pool | No of units | Order | Species | Locations | Data generated (bases) |
|---|---|---|---|---|---|
| Mosquitoes—Hubei | 24 | Diptera | Aedes sp, Armigeres subalbatus, Anopheles sinensis, Culex quinquefasciatus, Culex tritaeniorhynchus | Hubei | 26,606,799,000 |
| Mosquitoes—Zhejiang | 26 | Diptera | Aedes albopictus, Armigeres subalbatus, Anopheles paraliae, Anopheles sinensis, Culex pipiens, Culex sp, Culex tritaeniorhynchus | Zhejiang | 7,233,954,480 |
| True flies | 24 | Diptera | Atherigona orientalis, Chrysomya megacephala, Lucilia sericata, Musca domestica, Sarcophaga dux, S. peregrina, S. sp | Hubei | 6,574,954,320 |
| Horseflies | 24 | Diptera | Unidentified Tabanidae (5 species) | Hubei | 8,721,642,060 |
| Cockroaches | 24 | Blattodea | Blattella germanica | Hubei | 6,182,028,000 |
| Water striders | 12 | Hemiptera | Unidentified Gerridae (2 species) | Hubei | 3,154,714,200 |
| Insects mix 1 | 6 | Diptera, Coleoptera, Lepidoptera, Neuroptera | Abraxas tenuisuffusa, Hermetia illucens, unidentified Chrysopidae, unidentified Coleoptera, Psychoda alternata, unidentified Diptera, unidentified Stratiomyidae | Zhejiang | 7,745,172,660 |
| Insects mix 2 | 4 | Diptera, Hemiptera | Unidentified Hippoboscidae (2 species), Cimex hemipterus | Hubei | 5,916,431,520 |
| Insects mix 3 (insect near water) | 10 | Odonata, Hemiptera, Hymenoptera, Isopoda | Pseudothemis zonata, unidentified Nepidae (2 species), Camponotus japonicus, Diplonychus sp, Asellus sp | Hubei | 11,973,368,200 |
| Insects mix 4 (insect in the mountain) | 12 | Diptera, Orthoptera, Odonata, Hymenoptera, Hemiptera | Psychoda alternata, Velarifictorus micado, Crocothemis servilia, unidentified Phoridae, unidentified Lampyridae, Aphelinus sp, Hyalopterus pruni, Aulacorthum magnolia | Hubei | 6,882,491,800 |
| Ticks | 16 | Ixodida | Dermacentor marginatus, Dermacentor sp, Haemaphysalis doenitzi, H. longicornis, H. sp, H. formosensis, Hyalomma asiaticum, Rhipicephalus microplus, Argas miniatus | Hubei, Zhejiang, Beijing, Xinjiang | 24,708,479,580 |
| Ticks Hyalomma asiaticum | 1 | Ixodida | Hyalomma asiaticum | Xinjiang | 2,006,000,100 |
| Spiders | 32 | Araneae | Neoscona nautica, Parasteatoda tepidariorum, Plexippus setipes, Pirata sp, unidentified Araneae | Hubei | 11,361,912,300 |
| Shrimps | 48 | Decapoda | Exopalaemon carinicauda, Metapenaeus sp, Solenocera crassicornis, Penaeus monodon, Litopenaeus vannamei | Zhejiang | 5,365,359,900 |
| Crabs and barnacles | 35 | Decapoda, Scalpelliformes | Capitulum mitella, Charybdis hellerii, C. japonica, Uca arcuata | Zhejiang | 5,833,269,360 |
| Millipedes | 12 | Polydesmida | Unidentified Polydesmidae (2 species) | Hubei, Beijing | 7,176,702,400 |
Table 2
Mononegavirales-related RdRp sequences discovered in this study
| Virus name | Length of RdRp | Classification | Pool | Abundance | Putative arthropod host | Closest relative (aa identity) |
|---|---|---|---|---|---|---|
| Bole Tick Virus 3 | 2155 | Chuvirus | Ticks | 202.35 | Hyalomma asiaticum | Midway virus (17.1%) |
| Changping Tick Virus 2 | 2156 | Chuvirus | Ticks | 185.73 | Dermacentor sp | Midway virus (17.6%) |
| Changping Tick Virus 3 | 2209 | Chuvirus | Ticks | 41.80 | Dermacentor sp | Midway virus (16.5%) |
| Lishi Spider Virus 1 | 2180 | Chuvirus | Spiders | 5.82 | Parasteatoda tepidariorum | Midway virus (16.9%) |
| Shayang Fly Virus 1 | 2459 | Chuvirus | True flies | 8.99 | Atherigona orientalis | Maize mosaic virus (16.8%) |
| Shuangao Fly Virus 1 | 2097 | Chuvirus | Insect mix 1 | 23.63 | Unidentified Diptera | Lettuce big-vein associated virus (16.3%) |
| Shuangao Insect Virus 5 | 2291 | Chuvirus | Insect mix 1 | 209.31 | Unidentified Diptera, Abraxas tenuisuffusa, unidentified Chrysopidae | Potato yellow dwarf virus (16.3%) |
| Shuangao Lacewing Virus | 2145 | Chuvirus | Insect mix 1 | 44.48 | Unidentified Chrysopidae | Potato yellow dwarf virus (16.8%) |
| Tacheng Tick Virus 4 | 2101 | Chuvirus | Ticks | 137.22 | Argas miniatus | Midway virus (17.5%) |
| Tacheng Tick Virus 5 | 2201 | Chuvirus | Ticks | 276.32 | Dermacentor marginatus | Midway virus (16.8%) |
| Wenzhou Crab Virus 2 | 2208 | Chuvirus | Crabs and barnacles | 4054.25 | Charybdis japonica, Charybdis lucifera, Charybdis hellerii | Midway virus (15.8%) |
| Wenzhou Crab Virus 3 | 2077 | Chuvirus | Crabs and barnacles | 169.21 | Charybdis japonica | Midway virus (16.3%) |
| Wuchang Cockroach Virus 3 | 2203 | Chuvirus | Cockroaches | 440.14 | Blattella germanica | Midway virus (16.3%) |
| Wuhan Louse Fly Virus 6 | 2182 | Chuvirus | Insect mix 2 | 4.12 | Unidentified Hippoboscidae | Midway virus (16.4%) |
| Wuhan Louse Fly Virus 7 | 2174 | Chuvirus | Insect mix 2 | 99.83 | Unidentified Hippoboscidae | Midway virus (17.2%) |
| Wuhan Mosquito Virus 8 | 2159 | Chuvirus | Mosquito Hubei | 300.33 | Culex tritaeniorhynchus, C. quinquefasciatus, Anopheles sinensis, Armigeres subalbatus | Midway virus (16.7%) |
| Wuhan Tick Virus 2 | 2189 | Chuvirus | Ticks | 154.46 | Rhipicephalus microplus | Midway virus (16.7%) |
| Culex tritaeniorhynchus rhabdovirus | 2142 | Culex tritaeniorhynchus rhabdovirus | Mosquito Hubei | 3517.32 | Culex tritaeniorhynchus, C. quinquefasciatus, Anopheles sinensis, Armigeres subalbatus, Aedes sp | Isfahan virus (38.5%) |
| Wuhan Insect Virus 4 | 2105 | Cytorhabdovirus | Insect mix 4 | 94.92 | Hyalopterus pruni OR Aphelinus sp | Lettuce necrotic yellows virus (40.6%) |
| Wuhan Insect Virus 5 | 2098 | Cytorhabdovirus | Insect mix 4 | 622.97 | Hyalopterus pruni OR Aphelinus sp | Persimmon virus A (47.9%) |
| Wuhan Insect Virus 6 | 2079 | Cytorhabdovirus | Insect mix 4 | 991.99 | Hyalopterus pruni OR Aphelinus sp | Persimmon virus A (45.2) |
| Wuhan Louse Fly Virus 5 | 2123 | Kolente virus like | Insect mix 2 | 98.92 | Unidentified Hippoboscidae | Kolente virus (54.5%) |
| Yongjia Tick Virus 2 | 2113 | Nishimuro virus like | Ticks | 13.14 | Haemaphysalis hystricis | Nishimuro virus (54.2%) |
| Shayang Fly Virus 2 | 2170 | Sigmavirus like | True flies | 36.83 | Musca domestica, Chrysomya megacephala | Isfahan virus (44.1%) |
| Wuhan Fly Virus 2 | 2134 | Sigmavirus like | True flies | 18.37 | Musca domestica, Sarcophaga sp | Vesicular stomatitis Indiana virus (43.4%) |
| Wuhan House Fly Virus 1 | 2098 | Sigmavirus like | True flies | 31.04 | Musca domestica | Isfahan virus (42.8%) |
| Wuhan Louse Fly Virus 10 | 2146 | Sigmavirus like | Insect mix 2 | 235.94 | Unidentified Hippoboscidae | Drosophila melanogaster sigmavirus (51.2%) |
| Wuhan Louse Fly Virus 8 | 2145 | Sigmavirus like | Insect mix 2 | 292.11 | Unidentified Hippoboscidae | Drosophila melanogaster sigmavirus (50.6%) |
| Wuhan Louse Fly Virus 9 | 2145 | Sigmavirus like | Insect mix 2 | 69.37 | Unidentified Hippoboscidae | Drosophila melanogaster sigmavirus (51.4%) |
| Bole Tick Virus 2 | 2171 | Unclassified dimarhabdovirus 1 | Ticks | 38.19 | Hyalomma asiaticum | Isfahan virus (38.1%) |
| Huangpi Tick Virus 3 | 2193 | Unclassified dimarhabdovirus 1 | Ticks | 15.81 | Haemaphysalis doenitzi | Eel virus European X (40%) |
| Tacheng Tick Virus 3 | 2182 | Unclassified dimarhabdovirus 1 | Ticks | 96.30 | Dermacentor marginatus | Eel virus European X (39.8%) |
| Taishun Tick Virus | 2226 | Unclassified dimarhabdovirus 1 | Ticks | 24.56 | Haemaphysalis hystricis | Vesicular stomatitis Indiana virus (36.6%) |
| Wuhan Tick Virus 1 | 2191 | Unclassified dimarhabdovirus 1 | Ticks | 119.92 | Rhipicephalus microplus | Eel virus European X (38.3%) |
| Wuhan Insect Virus 7 | 2120 | Unclassified dimarhabdovirus 2 | Insect mix 4 | 241.7 | Hyalopterus pruni OR Aphelinus sp | Isfahan virus (42.6%) |
| Lishi Spider Virus 2 | 2201 | Unclassified mononegavirus 1 | Spiders | 5.57 | Unidentified Araneae | Maize fine streak virus (19.6%) |
| Sanxia Water Strider Virus 4 | 2108 | Unclassified mononegavirus 1 | Water striders | 4767.82 | Unidentified Gerridae | Orchid fleck virus (20.5%) |
| Tacheng Tick Virus 6 | 2068 | Unclassified mononegavirus 1 | Ticks | 17.92 | Argas miniatus | Maize mosaic virus (20.6%) |
| Shuangao Fly Virus 2 | 1966 | Unclassified mononegavirus 2 | Insect mix 1 | 25.94 | Psychoda alternata | Midway virus (21.3%) |
| Xincheng Mosquito Virus | 2026 | Unclassified mononegavirus 2 | Mosquito Hubei | 400.12 | Anopheles sinensis | Midway virus (19.2%) |
| Wenzhou Crab Virus 1 | 1807 | Unclassified mononegavirus 3 | Crabs and barnacles | 382.29 | Capitulum mitella, Charybdis japonica, Charybdis lucifera | Midway virus (22.2%) |
| Tacheng Tick Virus 7 | 2215 | Unclassified rhabdovirus 1 | Ticks | 35.86 | Argas miniatus | Orchid fleck virus (24.5%) |
| Jingshan Fly Virus 2 | 1970 | Unclassified rhabdovirus 2 | True flies | 4.43 | Sarcophaga sp | Maize fine streak virus (23.4%) |
| Sanxia Water Strider Virus 5 | 2264 | Unclassified rhabdovirus 2 | Water striders | 4373.68 | Unidentified Gerridae | Northern cereal mosaic virus (22.6%) |
| Shayang Fly Virus 3 | 2231 | Unclassified rhabdovirus 2 | True flies | 27.73 | Chrysomya megacephala, Atherigona orientalis | Maize fine streak virus (22.6%) |
| Shuangao Bedbug Virus 2 | 2207 | Unclassified rhabdovirus 2 | Insect mix 2 | 16.29 | Cimex hemipterus | Maize fine streak virus (22.5%) |
| Shuangao Insect Virus 6 | 2088 | Unclassified rhabdovirus 2 | Insect mix 1 | 14.37 | Unidentified Diptera, Abraxas tenuisuffusa | Potato yellow dwarf virus (21.2%) |
| Wuhan Ant Virus | 2118 | Unclassified rhabdovirus 2 | Insect mix 3 | 169.79 | Camponotus japonicus | Lettuce necrotic yellows virus (21.4%) |
| Wuhan Fly Virus 3 | 2230 | Unclassified rhabdovirus 2 | True flies | 6.00 | Musca domestica, Sarcophaga sp | Maize fine streak virus (21.9%) |
| Wuhan House Fly Virus 2 | 2233 | Unclassified rhabdovirus 2 | True flies | 221.04 | Musca domestica | Northern cereal mosaic virus (23.4%) |
| Wuhan Mosquito Virus 9 | 2260 | Unclassified rhabdovirus 2 | Mosquito Hubei | 56.19 | Culex tritaeniorhynchus, C. quinquefasciatus, Aedes sp | Persimmon virus A (23.2%) |
| Wuhan Louse Fly Virus 11 | 2110 | Vesiculovirus like | Insect mix 2 | 6.11 | Unidentified Hippoboscidae | Vesicular stomatitis Indiana virus (52.9%) |
Table 3
Bunya-arenaviridae-related RdRp sequences discovered in this study
| Virus name | Length of RdRp | Classification | Pool | Abundance | Putative arthropod host | Closest relative (aa identity) |
|---|---|---|---|---|---|---|
| Huangpi Tick Virus 1 | 3914 | Nairovirus like | Ticks | 11.32 | Haemaphysalis doenitzi | Hazara virus (39.5%) |
| Tacheng Tick Virus 1 | 3962 | Nairovirus like | Ticks | 88.91 | Dermacentor marginatus | Hazara virus (39.6%) |
| Wenzhou Tick Virus | 3967 | Nairovirus like | Ticks | 44.30 | Haemaphysalis hystricis | Crimean-Congo hemorrhagic fever virus (39.1%) |
| Shayang Spider Virus 1 | 4403 | Nairovirus like | Spiders | 90.95 | Neoscona nautica, Parasteatoda tepidariorum, Plexippus setipes | Crimean-Congo hemorrhagic fever virus (26.2%) |
| Xinzhou Spider Virus | 4037 | Nairovirus like | Spiders | 3.79 | Neoscona nautica, Parasteatoda tepidariorum | Erve virus (22.9%) |
| Sanxia Water Strider Virus 1 | 3936 | Nairovirus like | Water striders | 26,483.38 | Unidentified Gerridae | Hazara virus (23.4%) |
| Wuhan Louse Fly Virus 1 | 2250 | Orthobunyavirus | Insect mix 2 | 67.06 | Unidentified Hippoboscoidea | La Crosse virus (57.8%) |
| Shuangao Insect Virus 1 | 2335 | Orthobunyavirus like | Insect mix 1 | 7.97 | Unidentified Chrysopidae, Psychoda alternata | Khurdun virus (29.1%) |
| Wuchang Cockroach Virus 1 | 2125 | Phasmavirus like | Cockroaches | 11,283.22 | Blattella germanica | Kigluaik phantom virus (35.9%) |
| GAQJ01007189 | 1554 | Phasmavirus like | Database | N/A | Ostrinia furnacalis | Kigluaik phantom virus (35.9%) |
| Shuangao Insect Virus 2 | 1765 | Phasmavirus like | Insect mix 1 | 36.32 | Abraxas tenuisuffusa, unidentified Diptera | Kigluaik phantom virus (31.9%) |
| Wuhan Mosquito Virus 1 | 2095 | Phasmavirus like | Mosquito Hubei, Mosquito Zhejiang | 3523.08 | Culex tritaeniorhynchus, Anopheles sinensis, Culex quinquefasciatus | Kigluaik phantom virus (39.5%) |
| Wuhan Mosquito Virus 2 | 2111 | Phasmavirus like | Mosquito Hubei, Mosquito Zhejiang | 39.66 | Culex tritaeniorhynchus, Anopheles sinensis, Culex quinquefasciatus, Aedes sp | Kigluaik phantom virus (39.6%) |
| Huangpi Tick Virus 2 | 2121 | Phlebovirus | N/A | N/A | Haemaphysalis sp | Uukuniemi virus (49.3%) |
| Bole Tick Virus 1 | 2148 | Phlebovirus | Ticks | 67.86 | Hyalomma asiaticum | Uukuniemi virus (37.9%) |
| Changping Tick Virus 1 | 2194 | Phlebovirus | Ticks | 335.25 | Dermacentor sp | Uukuniemi virus (39.7%) |
| Dabieshan Tick Virus | 2148 | Phlebovirus | Ticks | 250.62 | Haemaphysalis longicornis | Uukuniemi virus (39.2%) |
| Lihan Tick Virus | 2151 | Phlebovirus | Ticks | 60.40 | Rhipicephalus microplus | Uukuniemi virus (38.6%) |
| Tacheng Tick Virus 2 | 2189 | Phlebovirus | Ticks | 132.59 | Dermacentor marginatus | Uukuniemi virus (39.0%) |
| Yongjia Tick Virus 1 | 2138 | Phlebovirus | Ticks | 119.49 | Haemaphysalis hystricis | Uukuniemi virus (40.5%) |
| GAIX01000059 | 2151 | Phlebovirus like | Database | N/A | Pararge aegeria | Cumuto virus (24.1%) |
| GAKZ01048260 | 1583 | Phlebovirus like | Database | N/A | Procotyla fluviatilis | Cumuto virus (22.8%) |
| GAQJ01008681 | 2261 | Phlebovirus like | Database | N/A | Ostrinia furnacalis | Gouleako virus (22.0%) |
| Shuangao Insect Virus 3 | 2050 | Phlebovirus like | Insect mix 1 | 339.41 | Unidentified Chrysopidae, unidentified Diptera | Cumuto virus (23.7%) |
| Wuhan Louse Fly Virus 2 | 2327 | Phlebovirus like | Insect mix 2 | 3.57 | Unidentified Hippoboscoidea | Uukuniemi virus (25.2%) |
| Wuhan Insect Virus 1 | 2099 | Phlebovirus like | Insect mix 3 | 178.53 | Asellus sp, unidentified Nepidae, Camponotus japonicus | Cumuto virus (24.8%) |
| Huangshi Humpbacked Fly Virus | 2009 | Phlebovirus like | Insect mix 4 | 13.13 | Unidentified Phoridae | Cumuto virus (18.1%) |
| Yichang Insect Virus | 2100 | Phlebovirus like | Insect mix 4 | 71.50 | Aulacorthum magnoliae | Gouleako virus (45.3%) |
| Wuhan Millipede Virus 1 | 1854 | Phlebovirus like | Millipedes and insect mix 3 | 825.66 | Unidentified Polydesmidae | Cumuto virus (25.3%) |
| Qingnian Mosquito Virus | 2243 | Phlebovirus like | Mosquito Hubei | 17.09 | Culex quinquefasciatus | Razdan virus (21.0%) |
| Wutai Mosquito Virus | 2185 | Phlebovirus like | Mosquito Hubei | 70.72 | Culex quinquefasciatus | Rice stripe virus (26.4%) |
| Xinzhou Mosquito Virus | 2022 | Phlebovirus like | Mosquito Hubei | 98.95 | Anopheles sinensis | Cumuto virus (24.7%) |
| Zhee Mosquito Virus | 2443 | Phlebovirus like | Mosquito Hubei, Mosquito Zhejiang | 308.98 | Anopheles sinensis, Armigeres subalbatus | Cumuto virus (22.6%) |
| Wenzhou Shrimp Virus 1 | 2051 | Phlebovirus like | Shrimps | 5859.37 | Penaeus monodon | Uukuniemi virus (32.2%) |
| Wuhan Spider Virus | 2251 | Phlebovirus like | Spiders | 17.71 | Neoscona nautica, Parasteatoda tepidariorum, Plexippus setipes | Uukuniemi virus (21.7%) |
| Wuhan Fly Virus 1 | 2192 | Phlebovirus like | True flies | 68.58 | Atherigona orientalis, Chrysomya megacephala, Sarcophaga sp, Musca domestica | Grand Arbaud virus (27.8%) |
| Wuhan Horsefly Virus | 3117 | Tenuivirus like | Horseflies | 13.50 | Unidentified Tabanidae | Uukuniemi virus (28.2%) |
| Jiangxia Mosquito Virus 1 | 1889 | Unclassified segmented virus 1 | Mosquito Hubei | 11.55 | Culex tritaeniorhynchus | Gouleako virus (16.7%) |
| Shuangao Bedbug Virus 1 | 2015 | Unclassified segmented virus 2 | Insect mix 2 | 12.71 | Cimex hemipterus | Murrumbidgee virus (16.3%) |
| Jiangxia Mosquito Virus 2 | 1860 | Unclassified segmented virus 2 | Mosquito Hubei | 2.81 | Culex tritaeniorhynchus | Hantavirus (18.9%) |
| Shuangao Mosquito Virus | 1996 | Unclassified segmented virus 2 | Mosquito Zhejiang | 11.67 | Armigeres subalbatus | Hantavirus (18.7%) |
| Wenzhou Shrimp Virus 2 | 2241 | Unclassified segmented virus 3 | Shrimps | 3824.55 | Penaeus monodon, Exopalaemon carinicauda | La Crosse virus (19.0%) |
| Shayang Spider Virus 2 | 2165 | Unclassified segmented virus 4 | Spiders | 12.75 | Neoscona nautica, Pirata sp, Parasteatoda tepidariorum, unidentified Araneae | Akabane virus (16.6%) |
| Wuhan Insect Virus 2 | 2377 | Unclassified segmented virus 5 | Insect mix 4 | 223.06 | Hyalopterus pruni OR Aphelinus sp | Kigluaik phantom virus (19.2%) |
| Sanxia Water Strider Virus 2 | 2349 | Unclassified segmented virus 5 | Water striders | 707.09 | Unidentified Gerridae | Kigluaik phantom virus (19.8%) |
| Wuhan Millipede Virus 2 | 3709 | Unclassified segmented virus 6 | Millipedes | 1513.41 | Unidentified Polydesmidae | Dugbe virus (17.2%) |
| Wuhan Insect Virus 3 | 2231 | Unclassified segmented virus 7 | Insect mix 3 | 3.50 | Asellus sp | Herbert virus (17.2%) |
Table 4
Orthomyxoviridae-related RdRp sequences discovered in this study
| Virus name | Length of RdRp | Classification | Pool | Abundance | Putative arthropod host | Closest relative (aa identity) |
|---|---|---|---|---|---|---|
| Jingshan Fly Virus 1 | 795 | Quaranjavirus | True flies | 21.93 | Atherigona orientalis, Chrysomya megacephala, Sarcophaga sp, Musca domestica | Johnston Atoll virus (36.9%) |
| Jiujie Fly Virus | 653 | Quaranjavirus | Horseflies | 10.30 | Unidentified Tabanidae | Johnston Atoll virus (39.7%) |
| Sanxia Water Strider Virus 3 | 789 | Quaranjavirus | Water striders | 1101.03 | Unidentified Gerridae | Johnston Atoll virus (36.7%) |
| Shayang Spider Virus 3 | 768 | Quaranjavirus | Spiders | 1.95 | Neoscona nautica | Johnston Atoll virus (38.5%) |
| Shuangao Insect Virus 4 | 793 | Quaranjavirus | Insect mix 1 | 59.90 | Unidentified Diptera, unidentified Stratiomyidae | Johnston Atoll virus (36.9%) |
| Wuhan Louse Fly Virus 3 | 784 | Quaranjavirus | Insect mix 2 | 500.77 | Unidentified Hippoboscoidea | Johnston Atoll virus (37.7%) |
| Wuhan Louse Fly Virus 4 | 783 | Quaranjavirus | Insect mix 2 | 96.80 | Unidentified Hippoboscoidea | Johnston Atoll virus (38.2%) |
| Wuhan Mosquito Virus 3 | 801 | Quaranjavirus | Mosquito Hubei | 40.07 | Culex tritaeniorhynchus, Culex quinquefasciatus, Armigeres subalbatus | Johnston Atoll virus (35.6%) |
| Wuhan Mosquito Virus 4 | 792 | Quaranjavirus | Mosquito Hubei | 86.21 | Culex tritaeniorhynchus, Culex quinquefasciatus, Armigeres subalbatus | Johnston Atoll virus (34.8%) |
| Wuhan Mosquito Virus 5 | 806 | Quaranjavirus | Mosquito Hubei | 75.05 | Culex tritaeniorhynchus, Culex quinquefasciatus, Armigeres subalbatus | Johnston Atoll virus (35.5%) |
| Wuhan Mosquito Virus 6 | 800 | Quaranjavirus | Mosquito Hubei | 56.30 | Culex quinquefasciatus | Johnston Atoll virus (34.2%) |
| Wuhan Mosquito Virus 7 | 779 | Quaranjavirus | Mosquito Hubei | 20.74 | Anopheles sinensis, Culex quinquefasciatus | Johnston Atoll virus (34.1%) |
| Wuhan Mothfly Virus | 710 | Quaranjavirus | Insect mix 4 | 14.47 | Psychoda alternata | Johnston Atoll virus (39.7%) |
| Wuchang Cockroach Virus 2 | 671 | Unclassified orthomyxovirus 1 | Cockroaches | 4.01 | Blattella germanica | Influenza C virus (27.0%) |
Table 5
Summary of Endogenous Virus Elements (EVEs) determined here
| Host classification | Host name | Virus classification | Gene(s) present |
|---|---|---|---|
| Chelicerata | Ixodes scapularis | Chuvirus | G, N |
| Dimarhabdovirus | RdRp, N | ||
| Nairovirus like | N | ||
| Phlebovirus | RdRp, N | ||
| Quaranjavirus | RdRp | ||
| Tetranychus urticae | Dimarhabdovirus | N | |
| Crustacea | Daphnia pulex | Phlebovirus like | RdRp |
| Eurytemora affinis | Chuvirus | G | |
| Dimarhabdovirus | RdRp, N | ||
| Hyalella azteca | Chuvirus | G, N | |
| Unclassified mononegavirus 3 | RdRp, N | ||
| Lepeophtheirus salmonis | Phlebovirus like | N, G | |
| Insecta: Coleoptera | Dendroctonus ponderosae | Chuvirus | G |
| Phasmavirus | G, N | ||
| Tribolium castaneum | Chuvirus | G | |
| Insecta: Diptera | Aedes aegypti | Chuvirus | RdRp |
| Dimarhabdovirus | RdRp, N | ||
| Phasmavirus | G | ||
| Phlebovirus like | N | ||
| Quaranjavirus | RdRp | ||
| Anopheles spp. | Chuvirus | G | |
| Dimarhabdovirus | RdRp, N | ||
| Phasmavirus | G, N | ||
| Phlebovirus like | N | ||
| Quaranjavirus | RdRp | ||
| Culex quinquefasciatus | Chuvirus | G, N | |
| Dimarhabdovirus | N | ||
| Drosophila spp. | Dimarhabdovirus | RdRp, N | |
| Phasmavirus | N | ||
| Unclassified rhabdovirus 2 | RdRp, N | ||
| Insecta: Isoptera | Zootermopsis nevadensis | Chuvirus | N |
| Insecta: Hemiptera | Acyrthosiphon pisum | Chuvirus | G, N |
| Dimarhabdovirus | N | ||
| Phlebovirus like | N | ||
| Quaranjavirus | RdRp | ||
| Unclassified mononegavirus 1 | RdRp, N | ||
| Rhodnius prolixus | Chuvirus | G | |
| Phasmavirus | G | ||
| Insecta: Hymenoptera | Atta cephalotes | Unclassified mononegavirus 2 | RdRp |
| Acromyrmex echinatior | Chuvirus | G | |
| Unclassified mononegavirus 2 | RdRp | ||
| Camponotus floridanus | Chuvirus | G | |
| Unclassified mononegavirus 1 | N | ||
| Unclassified mononegavirus 3 | RdRp | ||
| Unclassified rhabdovirus 2 | RdRp | ||
| Harpegnathos saltator | Chuvirus | G | |
| Linepithema humile | Chuvirus | G | |
| Nasonia spp. | Chuvirus | G | |
| Pogonomyrmex barbatus | Chuvirus | G | |
| Solenopsis invicta | Chuvirus | G | |
| Unclassified mononegavirus 1 | N | ||
| Unclassified mononegavirus 3 | RdRp, N | ||
| Insecta: Lepidoptera | Bombyx mori | Chuvirus | RdRp, G |
| Quaranjavirus | RdRp | ||
| Unclassified rhabdovirus 2 | RdRp | ||
| Melitaea cinxia | Dimarhabdovirus | N | |
| Quaranjavirus | RdRp | ||
| Plutella xylostella | Dimarhabdovirus | N, G | |
| Spodoptera frugiperda | Phlebovirus like | G | |
| Myriapoda | Strigamia maritima | Chuvirus | N |
| Phlebovirus like | G |
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Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses
eLife 4:e05378.
https://doi.org/10.7554/eLife.05378
