Towards defining the chloroviruses: a genomic journey through a genus of large DNA viruses
详细信息 查看全文
- 作者：Adrien Jeanniard (1)
David D Dunigan (2) (3)
James R Gurnon (2)
Irina V Agarkova (2) (3)
Ming Kang (2)
Jason Vitek (2)
Garry Duncan (4)
O William McClung (4)
Megan Larsen (4) (5)
Jean-Michel Claverie (1)
James L Van Etten (2) (3)
Guillaume Blanc (1) - 刊名：BMC Genomics
- 出版年：2013
- 出版时间：December 2013
- 年：2013
- 卷：14
- 期：1
- 全文大小：396KB
- 参考文献：1. Iyer LM, Aravind L, Koonin EV: Common origin of four diverse families of large eukaryotic DNA viruses. / J Virol 2001, 75:11720-1734. CrossRef
2. Iyer LM, Balaji S, Koonin EV, Aravind L: Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. / Virus Res 2006, 117:156-84. CrossRef
3. Yutin N, Wolf YI, Raoult D, Koonin EV: Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution. / Virol J 2009, 6:223. CrossRef
4. Dunigan DD, Fitzgerald LA, Van Etten JL: Phycodnaviruses: a peek at genetic diversity. / Virus Res 2006, 117:119-32. CrossRef
5. Wilson WH, Van Etten JL, Allen MJ: The Phycodnaviridae: the story of how tiny giants rule the world. / Curr Top Microbiol Immunol 2009, 328:1-2. CrossRef
6. Fuhrman JA: Marine viruses and their biogeochemical and ecological effects. / Nature 1999, 399:541-48. CrossRef
7. Wommack KE, Colwell RR: Virioplankton: viruses in aquatic ecosystems. / Microbiol Mol Biol Rev 2000, 64:69-14. CrossRef
8. Suttle CA: Marine viruses -major players in the global ecosystem. / Nat Rev Microbiol 2007, 5:801-12. CrossRef
9. Danovaro R, Corinaldesi C, Dell’anno A, Fuhrman JA, Middelburg JJ, Noble RT, Suttle CA: Marine viruses and global climate change. / FEMS Microbiol Rev 2011, 35:993-034. CrossRef
10. Virus Taxonomy: / IXth report of the international committee on taxonomy of viruses. Amsterdam: Academic Press; 2012:261.
11. Van Etten JL, Dunigan DD: Chloroviruses: not your everyday plant virus. / Trends Plant Sci 2012, 17:1-. CrossRef
12. Pr?schold T, Darienko T, Silva PC, Reisser W, Krienitz L: The systematics of Zoochlorella revisited employing an integrative approach. / Environ Microbiol 2011, 13:350-64. CrossRef
13. Li Y, Lu Z, Sun L, Ropp S, Kutish GF, Rock DL, Van Etten JL: Analysis of 74 kb of DNA located at the right end of the 330-kb chlorella virus PBCV-1 genome. / Virology 1997, 237:360-77. CrossRef
14. Dunigan DD, Cerny RL, Bauman AT, Roach JC, Lane LC, Agarkova IV, Wulser K, Yanai-Balser GM, Gurnon JR, Vitek JC, Kronschnabel BJ, Jeanniard A, Blanc G, Upton C, Duncan GA, McClung OW, Ma F, Etten JLV: Paramecium bursaria chlorella virus 1 proteome reveals novel architectural and regulatory features of a giant virus. / J Virol 2012, 86:8821-834. CrossRef
15. Fitzgerald LA, Graves MV, Li X, Feldblyum T, Nierman WC, Van Etten JL: Sequence and annotation of the 369-kb NY-2A and the 345-kb AR158 viruses that infect Chlorella NC64A. / Virology 2007, 358:472-84. CrossRef
16. Fitzgerald LA, Graves MV, Li X, Hartigan J, Pfitzner AJP, Hoffart E, Van Etten JL: Sequence and annotation of the 288-kb ATCV-1 virus that infects an endosymbiotic chlorella strain of the heliozoon Acanthocystis turfacea. / Virology 2007, 362:350-61. CrossRef
17. Fitzgerald LA, Graves MV, Li X, Feldblyum T, Hartigan J, Van Etten JL: Sequence and annotation of the 314-kb MT325 and the 321-kb FR483 viruses that infect Chlorella Pbi. / Virology 2007, 358:459-71. CrossRef
18. Van Etten JL, Gurnon JR, Yanai-Balser GM, Dunigan DD, Graves MV: Chlorella viruses encode most, if not all, of the machinery to glycosylate their glycoproteins independent of the endoplasmic reticulum and Golgi. / Biochim Biophys Acta 1800, 2010:152-59.
19. Thiel G, Moroni A, Dunigan D, Van Etten JL: Initial Events Associated with Virus PBCV-1 Infection of Chlorella NC64A. / Prog Bot 2010, 71:169-83. CrossRef
20. Mujtaba S, Manzur KL, Gurnon JR, Kang M, Van Etten JL, Zhou M-M: Epigenetic transcriptional repression of cellular genes by a viral SET protein. / Nat Cell Biol 2008, 10:1114-122. CrossRef
21. Wei H, Zhou M-M: Dimerization of a viral SET protein endows its function. / Proc Natl Acad Sci U S A 2010, 107:18433-8438. CrossRef
22. Yamada T, Onimatsu H, Van Etten JL: Chlorella viruses. / Adv Virus Res 2006, 66:293-36. CrossRef
23. Van Etten JL: Unusual life style of giant chlorella viruses. / Annu Rev Genet 2003, 37:153-95. CrossRef
24. Derelle E, Ferraz C, Escande M-L, Eychenié S, Cooke R, Piganeau G, Desdevises Y, Bellec L, Moreau H, Grimsley N: Life-cycle and genome of OtV5, a large DNA virus of the pelagic marine unicellular green alga Ostreococcus tauri. / PLoS One 2008, 3:e2250. CrossRef
25. Weynberg KD, Allen MJ, Gilg IC, Scanlan DJ, Wilson WH: Genome sequence of Ostreococcus tauri virus OtV-2 throws light on the role of picoeukaryote niche separation in the ocean. / J Virol 2011, 85:4520-529. CrossRef
26. Moreau H, Piganeau G, Desdevises Y, Cooke R, Derelle E, Grimsley N: Marine prasinovirus genomes show low evolutionary divergence and acquisition of protein metabolism genes by horizontal gene transfer. / J Virol 2010, 84:12555-2563. CrossRef
27. Weynberg KD, Allen MJ, Ashelford K, Scanlan DJ, Wilson WH: From small hosts come big viruses: the complete genome of a second Ostreococcus tauri virus, OtV-1. / Environ Microbiol 2009, 11:2821-839. CrossRef
28. Tonetti M, Zanardi D, Gurnon JR, Fruscione F, Armirotti A, Damonte G, Sturla L, De Flora A, Van Etten JL: Paramecium bursaria Chlorella virus 1 encodes two enzymes involved in the biosynthesis of GDP-L-fucose and GDP-D-rhamnose. / J Biol Chem 2003, 278:21559-1565. CrossRef
29. Van Hellemond JJ, Tielens AG: Expression and functional properties of fumarate reductase. / Biochem J 1994,304(Pt 2):321-31.
30. Arslan D, Legendre M, Seltzer V, Abergel C, Claverie J-M: Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. / Proc Natl Acad Sci U S A 2011, 108:17486-7491. CrossRef
31. Gubser C, Hué S, Kellam P, Smith GL: Poxvirus genomes: a phylogenetic analysis. / J Gen Virol 2004, 85:105-17. CrossRef
32. Landstein D, Burbank DE, Nietfeldt JW, Van Etten JL: Large deletions in antigenic variants of the chlorella virus PBCV-1. / Virology 1995, 214:413-20. CrossRef
33. Dufraigne C, Fertil B, Lespinats S, Giron A, Deschavanne P: Detection and characterization of horizontal transfers in prokaryotes using genomic signature. / Nucl Acids Res 2005, 33:e6. CrossRef
34. McLysaght A, Baldi PF, Gaut BS: Extensive gene gain associated with adaptive evolution of poxviruses. / PNAS 2003, 100:15655-5660. CrossRef
35. Monier A, Claverie J-M, Ogata H: Horizontal gene transfer and nucleotide compositional anomaly in large DNA viruses. / BMC Genomics 2007, 8:456. CrossRef
36. Filée J: Lateral gene transfer, lineage-specific gene expansion and the evolution of Nucleo Cytoplasmic Large DNA viruses. / J Invertebr Pathol 2009, 101:169-71. CrossRef
37. Forterre P: Giant viruses: conflicts in revisiting the virus concept. / Intervirology 2010, 53:362-78. CrossRef
38. Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J, Kuo A, Lindquist E, Lucas S, Pangilinan J, Polle J, Salamov A, Terry A, Yamada T, Dunigan DD, Grigoriev IV, Claverie J-M, Van Etten JL: The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. / Plant Cell 2010, 22:2943-955. CrossRef
39. Triana-Alonso FJ, Chakraburtty K, Nierhaus KH: The Elongation Factor 3 Unique in Higher Fungi and Essential for Protein Biosynthesis Is an E Site Factor. / J Biol Chem 1995, 270:20473-0478. CrossRef
40. Delaroque N, Maier I, Knippers R, Müller DG: Persistent virus integration into the genome of its algal host, Ectocarpus siliculosus (Phaeophyceae). / J Gen Virol 1999,80(Pt 6):1367-370.
41. Yomtovian I, Teerakulkittipong N, Lee B, Moult J, Unger R: Composition bias and the origin of ORFan genes. / Bioinformatics 2010, 26:996-99. CrossRef
42. Siew N, Fischer D: Analysis of singleton ORFans in fully sequenced microbial genomes. / Proteins 2003, 53:241-51. CrossRef
43. Besemer J, Lomsadze A, Borodovsky M: GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. / Nucleic Acids Res 2001, 29:2607-618. CrossRef
44. Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. / Nucleic Acids Res 2004, 32:1792-797. CrossRef
45. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O: New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. / Syst Biol 2010, 59:307-21. CrossRef
46. Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. / Mol Biol Evol 2007, 24:1596-599. CrossRef
47. Borodovsky M, McIninch J: Recognition of genes in DNA sequence with ambiguities. / Biosystems 1993, 30:161-71. CrossRef
48. Nakamura Y, Itoh T, Matsuda H, Gojobori T: Biased biological functions of horizontally transferred genes in prokaryotic genomes. / Nat Genet 2004, 36:760-66. CrossRef - 作者单位：Adrien Jeanniard (1)
David D Dunigan (2) (3)
James R Gurnon (2)
Irina V Agarkova (2) (3)
Ming Kang (2)
Jason Vitek (2)
Garry Duncan (4)
O William McClung (4)
Megan Larsen (4) (5)
Jean-Michel Claverie (1)
James L Van Etten (2) (3)
Guillaume Blanc (1)
1. Information Génomique & Structurale, IGS UMR7256, CNRS, Aix-Marseille Université, Marseille, FR-13288, France
2. Department of Plant Pathology, University of Nebraska, Lincoln, NE, 68583-0722, USA
3. Nebraska Center for Virology, University of Nebraska, Lincoln, NE, 68583-0900, USA
4. Biology Department, Nebraska Wesleyan University, Lincoln, NE, 68504, USA
5. Department of Biology, Indiana University, Bloomington, IN, 47408, USA
文摘
Background Giant viruses in the genus Chlorovirus (family Phycodnaviridae) infect eukaryotic green microalgae. The prototype member of the genus, Paramecium bursaria chlorella virus 1, was sequenced more than 15 years ago, and to date there are only 6 fully sequenced chloroviruses in public databases. Presented here are the draft genome sequences of 35 additional chloroviruses (287 -348 Kb/319 -381 predicted protein encoding genes) collected across the globe; they infect one of three different green algal species. These new data allowed us to analyze the genomic landscape of 41 chloroviruses, which revealed some remarkable features about these viruses. Results Genome colinearity, nucleotide conservation and phylogenetic affinity were limited to chloroviruses infecting the same host, confirming the validity of the three previously known subgenera. Clues for the existence of a fourth new subgenus indicate that the boundaries of chlorovirus diversity are not completely determined. Comparison of the chlorovirus phylogeny with that of the algal hosts indicates that chloroviruses have changed hosts in their evolutionary history. Reconstruction of the ancestral genome suggests that the last common chlorovirus ancestor had a slightly more diverse protein repertoire than modern chloroviruses. However, more than half of the defined chlorovirus gene families have a potential recent origin (after Chlorovirus divergence), among which a portion shows compositional evidence for horizontal gene transfer. Only a few of the putative acquired proteins had close homologs in databases raising the question of the true donor organism(s). Phylogenomic analysis identified only seven proteins whose genes were potentially exchanged between the algal host and the chloroviruses. Conclusion The present evaluation of the genomic evolution pattern suggests that chloroviruses differ from that described in the related Poxviridae and Mimiviridae. Our study shows that the fixation of algal host genes has been anecdotal in the evolutionary history of chloroviruses. We finally discuss the incongruence between compositional evidence of horizontal gene transfer and lack of close relative sequences in the databases, which suggests that the recently acquired genes originate from a still largely un-sequenced reservoir of genomes, possibly other unknown viruses that infect the same hosts.