Endogenous Bornavirus-like Elements in Bats: Evolutionary Insights from the Conserved Riboviral L-Gene in Microbats and Its Antisense Transcription in Myotis daubentonii
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bat Genome References and Gene Annotation Construction
2.2. Processing of RNA-Seq Data, Refinement of CV.10-MyoDau Annotation, and Differential Gene Expression
2.3. In Vitro Validation of EVE Candidate
2.4. Synteny Analysis to Confirm the Conservation of AMCR-MyoDau and CV.10-MyoDau
2.5. Identification and Further Investigation of the Previously Described EBLL-IG
2.6. Multiple Sequence Alignments of the Three Exons of AMCR in Various Bat Species
3. Results
3.1. A Novel EVE and Its Antisense Transcription in Myotis daubentonii: EBLL-Cultervirus.10-MyoDau and AMCR-MyoDau
3.2. AMCR-MyoDau Shows Weak but Constant Expression in a Myotis daubentonii Cell Line under Mock, Interferon-Induced, and Virus-Infected Conditions
3.3. Synteny Patterns of AMCR and CV.10-MyoDau across Various Bat Species
3.4. Comparative Genome Analysis Shows AMCR Sequence Similarities in 34 Bat Species
3.5. Partial Occurrence of AMCR across Multiple Bat Families and Evolutionary Conservation of CV.10 in Vespertilionidae
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Species | Abb. | #Con|#Chr | N50 | Size | NCBI Acc. | Year | Family |
---|---|---|---|---|---|---|---|
[Mb] | [Gb] | ||||||
Yangochiroptera | |||||||
Aeorestes cinereus | ACI | 2536|0 | 35.1 | 2.1 | GCA_011751065.1 | 2020 | Vespertilionidae |
Corynorhinus townsendii | CTO | 182|0 | 177.8 | 2.0 | GCA_026230045.1 | 2022 | Vespertilionidae |
Plecotus auritus | PAU | 5570|0 | 186.5 | 2.2 | GCA_963455325.1 | 2023 | Vespertilionidae |
Nycticeius humeralis | NHU | 1,676,240|0 | 0.015 | 2.8 | GCA_007922795.1 | 2019 | Vespertilionidae |
Ia io | IIO | 2008|0 | 105.8 | 2.1 | GCA_025583905.1 | 2022 | Vespertilionidae |
Eptesicus fuscus | EFU | 48|25 | 102.8 | 2.0 | GCF_027574615.1 * | 2023 | Vespertilionidae |
Eptesicus nilssonii | ENI | 726|0 | 102.4 | 2.0 | GCA_030846915.1 | 2023 | Vespertilionidae |
Lasiurus borealis | LBO | 518,900|0 | 0.039 | 2.9 | GCA_004026805.1 | 2019 | Vespertilionidae |
Antrozous pallidus | APA | 93|23 | 114.6 | 2.1 | GCA_027563665.1 | 2023 | Vespertilionidae |
Pipistrellus kuhlii | PKU | 202|0 | 80.2 | 1.8 | GCF_014108245.1 * | 2020 | Vespertilionidae |
Pipistrellus pipistrellus | PIP | 323|0 | 94.9 | 1.8 | GCA_903992545.1 | 2020 | Vespertilionidae |
Pipistrellus pygmaeus | PPY | 243|0 | 89.5 | 1.9 | GCA_949987585.1 | 2023 | Vespertilionidae |
Murina aurata feae | MAU | 880,177|0 | 0.026 | 2.3 | GCA_004026665.1 | 2019 | Vespertilionidae |
Myotis lucifugu | MLU | 11,654|0 | 4.3 | 2.0 | GCF_000147115.1 * | 2010 | Vespertilionidae |
Myotis brandtii | MBR | 169,750|0 | 3.2 | 2.1 | GCF_000412655.1 * | 2013 | Vespertilionidae |
Myotis vivesi | MVI | 64,503|0 | 91.8 | 2.1 | GCA_035771395.1 | 2024 | Vespertilionidae |
Myotis yumanensis | MYU | 476|0 | 99.1 | 2.0 | GCA_028538775.1 | 2023 | Vespertilionidae |
Myotis davidii | MDV | 101,769|0 | 3.5 | 2.1 | GCF_000327345.1 * | 2012 | Vespertilionidae |
Myotis ricketti | MRI | 105|0 | 80 | 2.0 | GCA_036010255.1 | 2024 | Vespertilionidae |
Myotis daubentonii | MDA | 121|23 | 102.2 | 2.1 | GCF_963259705.1 * | 2023 | Vespertilionidae |
Myotis myotis | MMY | 93|0 | 94.4 | 2.0 | GCF_014108235.1 * | 2020 | Vespertilionidae |
Molossus nigricans | MNI | 146|0 | 81.9 | 2.4 | GCA_026936385.1 | 2022 | Molossidae |
Molossus alvarezi | MAL | 187|0 | 113.9 | 2.4 | GCA_031001765.1 | 2023 | Molossidae |
Molossus molossus | MMO | 60|0 | 110.7 | 2.3 | GCF_014108415.1 * | 2020 | Molossidae |
Tadarida brasiliensis | TBR | 148|25 | 111.1 | 2.3 | GCA_030848825.1 | 2023 | Molossidae |
Rhynchonycteris naso | RNA | 50|0 | 286.1 | 2.4 | GCA_031021685.1 | 2023 | Eallonurida |
Sturnira hondurensis | SHO | 25,881|0 | 10.2 | 2.1 | GCF_014824575.3 * | 2022 | Phyllostomidae |
Tonatia saurophila | TSA | 249,810 | 0.166 | 2.1 | GCA_004024845.1 | 2019 | Phyllostomidae |
Trachops cirrhosus | TCI | 396,519 | 124.5 | 2.2 | GCA_028533065.1 | 2023 | Phyllostomidae |
Micronycteris hirsuta | MHI | 550,090|0 | 0.069 | 2.3 | GCA_004026765.1 | 2019 | Phyllostomidae |
Carollia perspicillata | CPE | 1,925,339|0 | 0.010 | 2.7 | GCA_004027735.1 | 2019 | Phyllostomidae |
Anoura caudifer | ACU | 337,255|0 | 0.143 | 2.2 | GCA_004027475.1 | 2019 | Phyllostomidae |
Desmodus rotundus | DRO | 573|14 | 160.1 | 2.1 | GCF_022682495.1 * | 2022 | Phyllostomidae |
Phyllostomus discolor | PDI | 78|17 | 171.7 | 2.1 | GCF_004126475.2 * | 2020 | Phyllostomidae |
Phyllostomus hastatus | PHA | 534|0 | 39.2 | 2.1 | GCF_019186645.2 * | 2021 | Phyllostomidae |
Macrotus californicus | MCA | 1,128,787|0 | 0.017 | 2.2 | GCA_007922815.1 | 2019 | Phyllostomidae |
Artibeus jamaicensis | AJA | 868|0 | 22.1 | 2.1 | GCF_021234435.1 * | 2021 | Phyllostomidae |
Pteronotus parnellii | PPA | 333|0 | 31.5 | 2.1 | GCF_021234165.1 * | 2021 | Mormoopidae |
Mormoops blainvillei | MBL | 205,259|0 | 0.156 | 2.1 | GCA_004026545.1 | 2019 | Mormoopidae |
Noctilio leporinus | NLE | 298,222|0 | 0.136 | 2.1 | GCA_004026585.1 | 2019 | Noctilionidae |
Miniopterus natalensis | MNA | 1269|0 | 4.3 | 1.8 | GCF_001595765.1 * | 2016 | Miniopteridae |
Miniopterus schreibersii | MSC | 177,620|0 | 0.109 | 1.8 | GCA_004026525.1 | 2019 | Miniopteridae |
Yinpterochiroptera | |||||||
Megaderma lyra | MLY | 1,902,801|0 | 0.072 | 2.6 | GCA_004026885.1 | 2019 | Megadermatidae |
Craseonycteris thonglongyai | CTH | 1,224,256|0 | 0.026 | 2.3 | GCA_004027555.1 | 2019 | Craseonycteridae |
Aselliscus stoliczkanus | AST | 191|16 | 162 | 2.2 | GCA_033961575.1 | 2023 | Hipposideridae |
Hipposideros pendleburyi | HPE | 28,685|0 | 15.4 | 2.2 | GCA_021464545.1 | 2022 | Hipposideridae |
Hipposideros armiger | HAR | 7571|0 | 2.3 | 2.2 | GCF_001890085.2 * | 2016 | Hipposideridae |
Hipposideros larvatus | HLA | 69|18 | 185.5 | 2.3 | GCA_031876335.1 | 2023 | Hipposideridae |
Rhinolophus ferrumequinum | RFE | 50|0 | 92 | 2.1 | GCA_014108255.1 | 2020 | Rhinolophidae |
Cynopterus sphinx | CSP | 181|17 | 145.2 | 1.9 | GCA_030015415.1 | 2023 | Pteropodidae |
Cynopterus brachyotis | CBR | 48,006|0 | 0.251 | 1.8 | GCA_009793145.1 | 2019 | Pteropodidae |
Macroglossus sobrinus | MSO | 171,985|0 | 0.453 | 1.9 | GCA_004027375.1 | 2019 | Pteropodidae |
Pteropus alecto | PLA | 65,598|0 | 6 | 2.0 | GCF_000325575.1 * | 2013 | Pteropodidae |
Pteropus vampyrus | PVA | 36,094|0 | 6 | 2.2 | GCF_000151845.1 * | 2014 | Pteropodidae |
Pteropus giganteus | PGI | 16,113|0 | 18.9 | 2.0 | GCF_902729225.1 * | 2020 | Pteropodidae |
Pteropus rufus | PRU | 469,091|19 | 110.5 | 2.1 | GCA_028533765.1 | 2023 | Pteropodidae |
Pteropus pselaphon | PPS | 7513|0 | 0.770 | 1.9 | GCA_014363405.1 | 2020 | Pteropodidae |
Eidolon dupreanum | EDU | 1,191,098|17 | 101.6 | 2.3 | GCA_028627145.1 | 2023 | Pteropodidae |
Eidolon helvum | EHE | 133,538|0 | 0.028 | 1.8 | GCA_000465285.1 | 2013 | Pteropodidae |
Eonycteris spelaea | ESP | 4469|0 | 8 | 2.0 | GCA_003508835.1 | 2018 | Pteropodidae |
Rousettus madagascariensis | RMA | 1,467,186|18 | 85.8 | 2.3 | GCA_028533395.1 | 2023 | Pteropodidae |
Rousettus leschenaultii | RLE | 8141|0 | 32.7 | 1.9 | GCA_015472975.1 | 2020 | Pteropodidae |
Rousettus aegyptiacus | RAE | 29|0 | 113.8 | 1.9 | GCF_014176215.1 * | 2020 | Pteropodidae |
Name EVE | Species | NCBI acc. | Start-Stop | Literature |
---|---|---|---|---|
CV.10-MyoDau | Myotis daubentonii | NC_081844.1 | 39,922,667–39,923,434 | |
CV.10-AeqCin | Aeorestes cinereus | JAAGEH010000014.1 | 12,648,154–12,648,930 | - |
CV.10-CorTow | Corynorhinus townsendii | JAPDVU010000006.1 | 98,426,944–98,427,716 | - |
CV.10-PleAur | Plecotus auritus | CAUOHH010000436.1 | 107,056–107,829 | - |
CV.10-IaIo | Ia io | JAJQQW010000006.1 | 73,804,507–73,805,270 | - |
CV.10-EptFus | Eptesicus fuscus | NC_072478.1 | 36,387,431–36,388,196 | [48,72] |
CV.10-EptNil | Eptesicus nilssonii | JAULJE010000005.1 | 36,472,464–36,473,231 | - |
CV.10-AntPal | Antrozous pallidus | CM050516.1 | 75,692,535–75,693,314 | [72] |
CV.10-PipKuh | Pipistrellus kuhlii | NW_023425584.1 | 64,293,707–64,294,472 | [72] |
CV.10-PipPip | Pipistrellus pipistrellus | LR862361.1 | 31,459,988–31,460,753 | [72] |
CV.10-PipPym | Pipistrellus pygmaeus | OX465307.1 | 64,495,766–64,496,530 | - |
CV.10-MurAur | Murina aurata feae | PVJC01025922.1 | 14,138–14,917 | [72] |
CV.10-MyoLuc | Myotis lucifugus | NW_005871049.1 | 34,243,866–34,244,427 | [48,72] |
CV.10-MyoBra | Myotis brandtii | NW_005370908.1 | 1,501,243–1,501,804 | [48,72] |
CV.10-MyoViv | Myotis vivesi | JAWPEG010000011.1 | 69,888,777–69,889,333 | - |
CV.10-MyoYum | Myotis yumanensis | JAPQVT010000005.1 | 70,588,059–70,588,617 | - |
CV.10-MyoRic | Myotis ricketti | JASKON010000005.1 | 71,087,272–71,087,392 | - |
CV.10-MyoMyo | Myotis myotis | NW_023416368.1 | 71,971,796–71,972,569 | [72] |
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© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
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Ritsch, M.; Eulenfeld, T.; Lamkiewicz, K.; Schoen, A.; Weber, F.; Hölzer, M.; Marz, M. Endogenous Bornavirus-like Elements in Bats: Evolutionary Insights from the Conserved Riboviral L-Gene in Microbats and Its Antisense Transcription in Myotis daubentonii. Viruses 2024, 16, 1210. https://doi.org/10.3390/v16081210
Ritsch M, Eulenfeld T, Lamkiewicz K, Schoen A, Weber F, Hölzer M, Marz M. Endogenous Bornavirus-like Elements in Bats: Evolutionary Insights from the Conserved Riboviral L-Gene in Microbats and Its Antisense Transcription in Myotis daubentonii. Viruses. 2024; 16(8):1210. https://doi.org/10.3390/v16081210
Chicago/Turabian StyleRitsch, Muriel, Tom Eulenfeld, Kevin Lamkiewicz, Andreas Schoen, Friedemann Weber, Martin Hölzer, and Manja Marz. 2024. "Endogenous Bornavirus-like Elements in Bats: Evolutionary Insights from the Conserved Riboviral L-Gene in Microbats and Its Antisense Transcription in Myotis daubentonii" Viruses 16, no. 8: 1210. https://doi.org/10.3390/v16081210