The analysis of translation-related gene set boosts debates around origin and evolution of mimiviruses
The giant mimiviruses challenged the well-established concept of viruses, blurring the roots of the tree of life, mainly due to their genetic content. Along with other nucleo-cytoplasmic large DNA viruses, they compose a new proposed order—named Megavirales—whose origin and evolution generate heated debate in the scientific community. The presence of an arsenal of genes not widespread in the virosphere related to important steps of the translational process, including transfer RNAs, aminoacyl-tRNA synthetases, and translation factors for peptide synthesis, constitutes an important element of this debate. In this review, we highlight the main findings to date about the translational machinery of the mimiviruses and compare their distribution along the distinct members of the family Mimiviridae. Furthermore, we discuss how the presence and/or absence of the translation-related genes among mimiviruses raises important insights to boost the debate on their origin and evolutionary history.
Vyšlo v časopise:
The analysis of translation-related gene set boosts debates around origin and evolution of mimiviruses. PLoS Genet 13(2): e32767. doi:10.1371/journal.pgen.1006532
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Review
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https://doi.org/10.1371/journal.pgen.1006532
Souhrn
The giant mimiviruses challenged the well-established concept of viruses, blurring the roots of the tree of life, mainly due to their genetic content. Along with other nucleo-cytoplasmic large DNA viruses, they compose a new proposed order—named Megavirales—whose origin and evolution generate heated debate in the scientific community. The presence of an arsenal of genes not widespread in the virosphere related to important steps of the translational process, including transfer RNAs, aminoacyl-tRNA synthetases, and translation factors for peptide synthesis, constitutes an important element of this debate. In this review, we highlight the main findings to date about the translational machinery of the mimiviruses and compare their distribution along the distinct members of the family Mimiviridae. Furthermore, we discuss how the presence and/or absence of the translation-related genes among mimiviruses raises important insights to boost the debate on their origin and evolutionary history.
Zdroje
1. Lwoff A. The concept of virus. J Gen Microbiol. 1957; 17: 239–253. doi: 10.1099/00221287-17-2-239 13481308
2. ICTV, 2016 –Last taxonomic release: 2015 release.
3. Raoult D, La Scola B, Birtles R. The Discovery and Characterization of Mimivirus, the Largest Known Virus and Putative Pneumonia Agent. Clin Infect Dis. 2007; 45: 95–102. doi: 10.1086/518608 17554709
4. Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, et al. The 1.2-Megabase Genome Sequence of Mimivirus. Science. 2004; 306: 1344–1350. doi: 10.1126/science.1101485 15486256
5. Fischer MG, Allen MJ, Wilson WH, Suttle CA. Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci USA. 2010; 107: 19508–19513. doi: 10.1073/pnas.1007615107 20974979
6. Arslan D, Legendre M, Seltzer V, Abergel C, Claverie JM. Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci USA. 2011; 108: 17486–17491. doi: 10.1073/pnas.1110889108 21987820
7. Colson P, de Lamballerie X, Fournous G, Raoult D. Reclassification of Giant Viruses Composing a Fourth Domain of Life in the New Order Megavirales. Intervirology. 2012; 55: 321–332. doi: 10.1159/000336562 22508375
8. La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M. A giant virus in amoebae. Science. 2003; 299: 2033. doi: 10.1126/science.1081867 12663918
9. Abrahão JS, Dornas FP, Silva LC, Almeida GM, Boratto PV, Colson P, et al. Acanthamoeba polyphaga mimivirus and other giant viruses: an open field to outstanding discoveries. Virol J. 2014; 11: 120. doi: 10.1186/1743-422X-11-120 24976356
10. Colson P, Fournous G, Diene SM, Raoult D. Codon Usage, Amino Acid Usage, Transfer RNA and Amino-Acyl-tRNA Synthetases in Mimiviruses. Intervirology. 2013; 56: 364–375. doi: 10.1159/000354557 24157883
11. Klose T, Rossmann MG. Structure of large dsDNA viruses. Biol Chem. 2014; 359: 711–719.
12. Legendre M, Santini S, Rico A, Abergel C, Claverie JM. Breaking the 1000-gene barrier for Mimivirus using ultra-deep genome and transcriptome sequencing. Virol J. 2011; 8: 99. doi: 10.1186/1743-422X-8-99 21375749
13. Colson P, Yutin N, Shabalina SA, Robert C, Fournous G, La Scola B, et al. Viruses with More Than 1,000 Genes: Mamavirus, a New Acanthamoeba polyphaga mimivirus Strain, and Reannotation of Mimivirus Genes. Genome Biol Evol. 2011; 3: 737–742. doi: 10.1093/gbe/evr048 21705471
14. Campos RK, Boratto PV, Assis FL, Aguiar ER, Silva LC, Albarnaz JD, et al. Samba virus: a novel mimivirus from a giant rain forest, the Brazilian Amazon. Virol J. 2014; 11: 95. doi: 10.1186/1743-422X-11-95 24886672
15. Boratto PV, Arantes TS, Silva LC, Assis FL, Kroon EG, La Scola B, et al. Niemeyer Virus: A New Mimivirus Group A Isolate Harboring a Set of Duplicated Aminoacyl-tRNA Synthetase Genes. Front Microbiol. 2015; 6: 1256. doi: 10.3389/fmicb.2015.01256 26635738
16. Yoosuf N, Yutin N, Colson P, Shabalina SA, Pagnier I, Robert C, et al. Related giant viruses in distant locations and different habitats: Acanthamoeba polyphaga moumouvirus represents a third lineage of the Mimiviridae that is close to the Megavirus lineage. Genome Biol Evol. 2012; 4: 1324–1330. doi: 10.1093/gbe/evs109 23221609
17. Saadi H, Pagnier I, Colson P, Cherif JK, Beji M, Boughalmi M, et al. First isolation of Mimivirus in a patient with pneumonia. Clin Infec Dis. 2013; 57: e127–134.
18. Yoosuf N, Pagnier I, Fournous G, Robert C, La Scola B, Raoult D, et al. Complete genome sequence of Courdo11 virus, a member of the family Mimiviridae. Virus Genes. 2014; 48: 218–223. doi: 10.1007/s11262-013-1016-x 24293219
19. Santini S, Jeudy S, Bartoli J, Poirot O, Lescot M, Abergel C, et al. Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. Proc Natl Acad Sci USA. 2013; 110: 10800–10805. doi: 10.1073/pnas.1303251110 23754393
20. Yau S, Lauro FM, DeMaere MZ, Brown MV, Thomas T, Raftery MJ, et al. Virophage control of antarctic algal host–virus dynamics. Proc Natl Acad Sci USA. 2011; 108: 6163–6168. doi: 10.1073/pnas.1018221108 21444812
21. Piacente F, Marin M, Molinaro A, De Castro C, Seltzer V, Salis A, et al. Giant DNA virus mimivirus encodes pathway for biosynthesis of unusual sugar 4-amino-4,6-dideoxy-D-glucose (Viosamine). J Biol Chem. 2012; 287: 3009–3018. doi: 10.1074/jbc.M111.314559 22157758
22. Piacente F, Bernardi C, Marin M, Blanc G, Abergel C, Tonetti MG. Characterization of a UDP-N-acetylglucosamine biosynthetic pathway encoded by the giant DNAvirus Mimivirus. Glycobiology. 2014; 24: 51–61. doi: 10.1093/glycob/cwt089 24107487
23. Boyer M, Yutin N, Pagnier I, Barrassi L, Fournous G, Espinosa L, et al. Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. Proc Natl Acad Sci USA. 2009; 106: 21848–21853. doi: 10.1073/pnas.0911354106 20007369
24. Philippe N, Legendre M, Doutre G, Couté Y, Poirot O, Lescot M, et al. Pandoraviruses: amoebae viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science. 2013; 341: 281–286. doi: 10.1126/science.1239181 23869018
25. Reteno DG, Benamar S, Khalil JB, Andreani J, Armstrong N, Klose T, et al. Faustovirus, an asfavirus-related new lineage of giant viruses infecting amoebae. J Virol. 2015; 89: 6585–6594. doi: 10.1128/JVI.00115-15 25878099
26. Legendre M, Lartigue A, Bertaux L, Jeudy S, Bartoli J, Lescot M, et al. In-depth study of Mollivirus sibericum, a new 30,000-y-old giant virus infecting Acanthamoeba. Proc Natl Acad Sci USA. 2015; 112: E5327–5335. doi: 10.1073/pnas.1510795112 26351664
27. Ribas de Pouplana L, Schimmel P. Aminoacyl-tRNA synthetases: potential markers of genetic code development. Trends Biochem Sci. 2001; 26: 591–596. 11590011
28. Li R, Macnamara LM, Leuchter JD, Alexander RW, Cho SS. MD Simulations of tRNA and Aminoacyl-tRNA Synthetases: Dynamics, Folding, Binding, and Allostery. Int J Mol Sci. 2015; 16: 15872–15902. doi: 10.3390/ijms160715872 26184179
29. Fournier GP, Andam CP, Alm EJ, Gogarten JP. Molecular Evolution of Aminoacyl tRNA Synthetase Proteins in the Early History of Life. Orig Life Evol Biosph. 2011; 41: 621–632. doi: 10.1007/s11084-011-9261-2 22200905
30. Nasir A, Kim KM, Caetano-Anollés G. Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya. BMC Evol Biol. 2012; 12: 156. doi: 10.1186/1471-2148-12-156 22920653
31. Nasir A, Caetano-Anollés G. A phylogenomic data-driven exploration of viral origins and evolution. Sci Adv. 2015; 1: e1500527. doi: 10.1126/sciadv.1500527 26601271
32. Yutin N, Wolf YI, Koonin EV. Origin of giant viruses from smaller DNA viruses not from a fourth domain of cellular life. Virology. 2014; 466–467: 38–52. doi: 10.1016/j.virol.2014.06.032 25042053
33. Koonin EV, Krupovic M, Yutin N. Evolution of double-strand DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses. Ann N Y Acad Sci. 2015; 1341: 10–24. doi: 10.1111/nyas.12728 25727355
34. Boyer M, Madoui MA, Gimenez G, La Scola B, Raoult D. Phylogenetic and Phyletic Studies of Informational Genes in Genomes Highlight Existence of a 4th Domain of Life Including Giant Viruses. PLoS ONE. 2010; 5: e15530. doi: 10.1371/journal.pone.0015530 21151962
35. Legendre M, Audic S, Poirot O, Hingamp P, Seltzer V, Byrne D, et al. mRNA deep sequencing reveals 75 new genes and a complex transcriptional landscape in Mimivirus. Genome Res. 2010; 20: 664–674. doi: 10.1101/gr.102582.109 20360389
36. Abergel C, Chenivesse S, Byrne D, Suhre K, Arondel V, Claverie JM. Mimivirus TyrRS: preliminary structural and functional characterization of the first amino-acyl tRNA synthetase found in a virus. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2005; 61(Pt 2): 212–215. doi: 10.1107/S174430910500062X 16510997
37. Abergel C, Rudinger-Thirion J, Giegé R, Claverie JM. Virus-Encoded Aminoacyl-tRNA Synthetases: Structural and Functional Characterization of Mimivirus TyrRS and MetRS. J Virol. 2007; 81: 12406–12417. doi: 10.1128/JVI.01107-07 17855524
38. Silva LC, Almeida GM, Assis FL, Albarnaz JD, Boratto PV, Dornas FP, et al. Modulation of the expression of mimivirus-encoded translation-related genes in response to nutrient availability during Acanthamoeba castellanii infection. Front Microbiol. 2015; 6: 539. doi: 10.3389/fmicb.2015.00539 26082761
39. Filée J. Genomic comparison of closely related giant viruses supports an accordion-like model of evolution. Front Microbiol. 2015; 6: 593. doi: 10.3389/fmicb.2015.00593 26136734
40. Boyer M, Azza S, Barrassi L, Klose T, Campocasso A, Pagnier I, et al. Mimivirus shows dramatic genome reduction after intraamoebal culture. Proc Natl Acad Sci USA. 108: 10296–10301. doi: 10.1073/pnas.1101118108 21646533
41. Giegé R. The early history of tRNA recognition by aminoacyl-tRNA synthetases. J Biosci. 2006; 31: 477–488. 17206068
42. Barciszewska MZ, Perrigue PM, Barciszewski J. tRNA–the golden standard in molecular biology. Mol Biosyst. 2016; 12: 12–17. doi: 10.1039/c5mb00557d 26549858
43. Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Rüger W. Bacteriophage T4 Genome. Microbiol Mol Biol Rev. 2003; 67: 86–156. doi: 10.1128/MMBR.67.1.86-156.2003 12626685
44. Virgin HW 4th, Latreille P, Wamsley P, Hallsworth K, Weck KE, Dal Canto AJ, et al. Complete Sequence and Genomic Analysis of Murine Gammaherpesvirus 68. J Virol. 1997. 71: 5894–5904. 9223479
45. Van Etten JL, Meints RH. Giant viruses infecting algae. Annu Rev Microbiol. 1999; 53: 447–494. doi: 10.1146/annurev.micro.53.1.447 10547698
46. Assis FL, Bajrai L, Abrahao JS, Kroon EG, Dornas FP, Andrade KR, et al. Pan-Genome Analysis of Brazilian Lineage A Amoebal Mimiviruses. Viruses. 2015; 7: 3483–3499. doi: 10.3390/v7072782 26131958
47. Yoosuf N, Pagnier I, Fournous G, Robert C, Raoult D, La Scola B, et al. Draft genome sequences of Terra1 and Terra2 viruses, new members of the family Mimiviridae isolated from soil. Virology. 2014; 452–453:125–132. doi: 10.1016/j.virol.2013.12.032 24606689
48. Yutin N, Colson P, Raoult D, Koonin EV. Mimiviridae: clusters of orthologous genes, reconstruction of gene repertoire evolution and proposed expansion of the giant virus family. Virol J. 2013; 10: 106. doi: 10.1186/1743-422X-10-106 23557328
49. Claverie JM. Giant virus in the sea: Extending the realm of Megaviridae to Viridiplantae. Commum Integr Biol. 2013; 6: e25685.
50. Raoult D. TRUC or the need for a new microbial classification. Intervirology. 2013; 56: 349–353. doi: 10.1159/000354269 23867259
51. Seligmann H, Raoult D. Unifying view of stem-loop hairpin RNA as origin of current and ancient parasitic and non-parasitic RNAs, including in giant viruses. Curr Opin Microbiol. 2016; 31: 1–8. doi: 10.1016/j.mib.2015.11.004 26716728
52. Moreira D, López-García P. Comment on “The 1.2-megabase genome sequence of Mimivirus”. Science. 2005; 308: 1114. doi: 10.1126/science.1110820 15905382
53. Noble CG, Song H. Structural studies of elongation and release factors. Cell Mol Life Sci. 2008; 65: 1335–1346. doi: 10.1007/s00018-008-7495-6 18213444
54. Kyrpides NC, Woese CR. Universally conserved translation initiation factors. Proc Natl Acad Sci USA. 1998; 95: 224–228. 9419357
55. Claverie JM, Abergel C. Mimivirus: the emerging paradox of quasi-autonomous viruses. Trends Genet. 2010; 26: 431–437. doi: 10.1016/j.tig.2010.07.003 20696492
56. Moreira D, Lópes-García P. Ten reasons to exclude viruses from the tree of life. Nat Rev Microbiol. 2009; 7: 306–311. doi: 10.1038/nrmicro2108 19270719
57. Raoult D. There is no such thing as a tree of life (and of course viruses are out!). Nat Rev Microbiol. 2009. 7: 615.
58. Saini HK, Fischer D. Structural and functional insights into Mimivirus ORFans. BMC Genomics. 2007; 8: 115. doi: 10.1186/1471-2164-8-115 17490476
59. Jeudy S, Abergel C, Claverie JM, Legendre M. Translation in Giant Viruses: A Unique Mixture of Bacterial and Eukaryotic Termination Schemes. PLoS Genet. 2012; 8: e1003122. doi: 10.1371/journal.pgen.1003122 23271980
60. Raoult D. The post-Darwinist rhizome of life. Lancet. 2010; 375: 104–105. doi: 10.1016/S0140-6736(09)61958-9 20109873
61. Moreira D, Brochier-Armanet C. Giant viruses, giant chimeras: The multiple evolutionary histories of Mimivirus genes. BMC Evol Biol. 2008; 8: 12. doi: 10.1186/1471-2148-8-12 18205905
62. Khalil JY, Andreani J, La Scola B. Updating strategies for isolating and discovering giant viruses. Curr Opin Microbiol. 2016; 31: 80–87. doi: 10.1016/j.mib.2016.03.004 27039269
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