Skip to main content
SpringerLink
Log in

Shrinking of repeating unit length in leucine-rich repeats from double-stranded DNA viruses

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Leucine-rich repeats (LRRs) are present in over 563,000 proteins from viruses to eukaryotes. LRRs repeat in tandem and have been classified into fifteen classes in which the repeat unit lengths range from 20 to 29 residues. Most LRR proteins are involved in protein-protein or ligand interactions. The amount of genome sequence data from viruses is increasing rapidly, and although viral LRR proteins have been identified, a comprehensive sequence analysis has not yet been done, and their structures, functions, and evolution are still unknown. In the present study, we characterized viral LRRs by sequence analysis and identified over 600 LRR proteins from 89 virus species. Most of these proteins were from double-stranded DNA (dsDNA) viruses, including nucleocytoplasmic large dsDNA viruses (NCLDVs). We found that the repeating unit lengths of 11 types are one to five residues shorter than those of the seven known corresponding LRR classes. The repeating units of six types are 19 residues long and are thus the shortest among all LRRs. In addition, two of the LRR types are unique and have not been observed in bacteria, archae or eukaryotes. Conserved strongly hydrophobic residues such as Leu, Val or Ile in the consensus sequences are replaced by Cys with high frequency. Phylogenetic analysis indicated that horizontal gene transfer of some viral LRR genes had occurred between the virus and its host. We suggest that the shortening might contribute to the survival strategy of viruses. The present findings provide a new perspective on the origin and evolution of LRRs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Matsushima N, Robert H. Kretsinger (2016) Leucine rich repeats: sequences, structures, ligand-interactions and evolution. LAMBERT Academic Publishing, Saarbrücken.

  2. Kobe B, Deisenhofer J (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19(10):415–421

    Article  CAS  PubMed  Google Scholar 

  3. Bella J, Hindle KL, McEwan PA, Lovell SC (2008) The leucine-rich repeat structure. Cell Mol Life Sci 65(15):2307–2333

    Article  CAS  PubMed  Google Scholar 

  4. Koonin EV, Yutin N (2018) Multiple evolutionary origins of giant viruses. F1000Res 7

  5. Redrejo-Rodriguez M, Salas ML (2014) Repair of base damage and genome maintenance in the nucleo-cytoplasmic large DNA viruses. Virus Res 179:12–25

    Article  CAS  PubMed  Google Scholar 

  6. Colson P, de Lamballerie X, Fournous G, Raoult D (2012) Reclassification of giant viruses composing a fourth domain of life in the new order Megavirales. Intervirology 55(5):321–332

    Article  PubMed  Google Scholar 

  7. Afonso CL, Tulman ER, Lu Z, Oma E, Kutish GF, Rock DL (1999) The genome of Melanoplus sanguinipes entomopoxvirus. J Virol 73(1):533–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Mitchell AL, Attwood TK, Babbitt PC, Blum M, Bork P, Bridge A, Brown SD, Chang HY, El-Gebali S, Fraser MI et al (2019) InterPro in 2019: improving coverage, classification and access to protein sequence annotations. Nucleic Acids Res 47(D1):D351–D360

    Article  CAS  PubMed  Google Scholar 

  9. Miyashita H, Kuroki Y, Matsushima N (2014) Novel leucine-rich repeat doains in proteins from uincellular eukaryotes and bacteria. Protei Pep Lett 21(3):292–305

    Article  CAS  Google Scholar 

  10. Kobe B, Kajava AV (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11(6):725–732

    Article  CAS  PubMed  Google Scholar 

  11. Matsushima N, Miyashita H, Mikami T, Kuroki Y (2010) A nested leucine rich repeat (LRR) domain: the precursor of LRRs is a ten or eleven residue motif. BMC Microbiol 10:235

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Kajava AV, Anisimova M, Peeters N (2008) Origin and evolution of GALA-LRR, a new member of the CC-LRR subfamily: from plants to bacteria? PloS One 3(2):e1694

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Matsushima N, Takatsuka S, Miyashita H, Kretsinger RH (2019) Leucine rich repeat proteins: sequences, mutations, structures and diseases. Protein Pept Lett 26(2):108–131

    Article  CAS  PubMed  Google Scholar 

  14. O’Day DH, Suhre K, Myre MA, Chatterjee-Chakraborty M, Chavez SE (2006) Isolation, characterization, and bioinformatic analysis of calmodulin-binding protein cmbB reveals a novel tandem IP22 repeat common to many Dictyostelium and Mimivirus proteins. Biochem Biophys Res Commun 46(3):879–888

  15. Evdokimov AG, Anderson DE, Routzahn KM, Waugh DS (2001) Unusual molecular architecture of the Yersinia pestis cytotoxin YopM: A leucine-rich repeat protein with the shortest repeating unit. J Mol Biol 312(4):807–821

    Article  CAS  PubMed  Google Scholar 

  16. Batkhishig D, Enkhbayar P, Kretsinger RH, Matsushima N (2020) A strong correlation between consensus sequences and unique super secondary dtructures in leucine rich repeats. Proteins 88(7):840–852

    Article  CAS  PubMed  Google Scholar 

  17. Matsushima N, Miyashita H, Mikami T, Yamada K (2011) A new method for the identification of leucine-rich repeats by incorporating protein second structure prediction. In Bioinformatics: genome bioinformatics and computational biology. editor. NOVA Science, pp 61–88

  18. Matsushima N, Tanaka T, Enkhbayar P, Mikami T, Taga M, Yamada K, Kuroki Y (2007) Comparative sequence analysis of leucine-rich repeats (LRRs) within vertebrate toll-like receptors. BMC Genom 8:124–143

    Article  CAS  Google Scholar 

  19. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14(6):1188–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kumar S, Stecher G, Li M, Knyaz C, Tamura K, MEGA X (2018) Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Schulz F, Yutin N, Ivanova NN, Ortega DR, Lee TK, Vierheilig J, Daims H, Horn M, Wagner M, Jensen GJ et al (2017) Giant viruses with an expanded complement of translation system components. Science 356(6333):82–85

    Article  CAS  PubMed  Google Scholar 

  22. Schulz F, Alteio L, Goudeau D, Ryan EM, Yu FB, Malmstrom RR, Blanchard J, Woyke T (2018) Hidden diversity of soil giant viruses. Nat Commun 9(1):4881

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Backstrom D, Yutin N, Jorgensen SL, Dharamshi J, Homa F, Zaremba-Niedwiedzka K, Spang A, Wolf YI, Koonin EV, Ettema TJG (2019) Virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism. MBio 10(2):e02497-18

    Article  PubMed  PubMed Central  Google Scholar 

  24. Kent BN, Salichos L, Gibbons JG, Rokas A, Newton IL, Clark ME, Bordenstein SR (2011) Complete bacteriophage transfer in a bacterial endosymbiont (Wolbachia) determined by targeted genome capture. Genome Biol Evol 3:209–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Jeong GJA, Jang Y, Choe JC, Choi H (2012) Wolbachia infection in the Loxoblemmus complex (Orthoptera: Gryllidae) in Korea. J Asia Pac Entomol 15(4):563–566

    Article  Google Scholar 

  26. Urbanus ML, Quaile AT, Stogios PJ, Morar M, Rao C, Di Leo R, Evdokimova E, Lam M, Oatway C, Cuff ME et al (2016) Diverse mechanisms of metaeffector activity in an intracellular bacterial pathogen, Legionella pneumophila. Mol Syst Biol 12(12):893

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Miras I, Saul F, Nowakowski M, Weber P, Haouz A, Shepard W, Picardeau M (2015) Structural characterization of a novel subfamily of leucine-rich repeat proteins from the human pathogen Leptospira interrogans. Acta Crystallogr D Biol Crystallogr 71(6):1351–1359

    Article  CAS  PubMed  Google Scholar 

  28. Deneka D, Sawicka M, Lam AKM, Paulino C, Dutzler R (2018) Structure of a volume-regulated anion channel of the LRRC8 family. Nature 558(7709):254–259

    Article  CAS  PubMed  Google Scholar 

  29. Moreau H, Piganeau G, Desdevises Y, Cooke R, Derelle E, Grimsley N (2010) Marine prasinovirus genomes show low evolutionary divergence and acquisition of protein metabolism genes by horizontal gene transfer. J Virol 84(24):12555–12563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Yau S, Lauro FM, DeMaere MZ, Brown MV, Thomas T, Raftery MJ, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Gibson JA et al (2011) Virophage control of antarctic algal host-virus dynamics. Proc Natl Acad Sci USA 108(15):6163–6168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Philippe N, Legendre M, Doutre G, Coute Y, Poirot O, Lescot M, Arslan D, Seltzer V, Bertaux L, Bruley C et al (2013) Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341(6143):281–286.

  32. Legendre M, Fabre E, Poirot O, Jeudy S, Lartigue A, Alempic JM, Beucher L, Philippe N, Bertaux L, Christo-Foroux E et al (2018) Diversity and evolution of the emerging Pandoraviridae family. Nat Commun 9(1):2285

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Legendre M, Alempic JM, Philippe N, Lartigue A, Jeudy S, Poirot O, Ta NT, Nin S, Coute Y, Abergel C et al (2019) Pandoravirus celtis illustrates the microevolution processes at work in the giant Pandoraviridae genomes. Front Microbiol 10:430

    Article  PubMed  PubMed Central  Google Scholar 

  34. Desjardins CA, Gundersen-Rindal DE, Hostetler JB, Tallon LJ, Fuester RW, Schatz MC, Pedroni MJ, Fadrosh DW, Haas BJ, Toms BS et al (2007) Structure and evolution of a proviral locus of Glyptapanteles indiensis bracovirus. BMC Microbiol 7:61

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Mitsuhashi W, Miyamoto K, Wada S (2014) The complete genome sequence of the Alphaentomopoxvirus Anomala cuprea entomopoxvirus, including its terminal hairpin loop sequences, suggests a potentially unique mode of apoptosis inhibition and mode of DNA replication. Virology 452–453:95–116

    Article  PubMed  CAS  Google Scholar 

  36. Hirt RP, Harriman N, Kajava AV, Embley TM (2002) A novel potential surface protein in Trichomonas vaginalis contains a leucine-rich repeat shared by micro-organisms from all three domains of life. Mol Biochem Parasitol 125(1–2):195–199

    Article  CAS  PubMed  Google Scholar 

  37. Handrich MR, Garg SG, Sommerville EW, Hirt RP, Gould SB (2019) Characterization of the BspA and Pmp protein family of trichomonads. Parasit Vect 12(1):406

    Article  CAS  Google Scholar 

  38. Davis PH, Zhang Z, Chen M, Zhang X, Chakraborty S, Stanley SL Jr (2006) Identification of a family of BspA like surface proteins of Entamoeba histolytica with novel leucine rich repeats. Mol Biochem Parasitol 145(1):111–116

    Article  CAS  PubMed  Google Scholar 

  39. Ramaswamy R, Houston S, Loveless B, Cameron CE, Boulanger MJ (2019) Structural characterization of Treponema pallidum Tp0225 reveals an unexpected leucine-rich repeat architecture. Acta Crystallogr F Struct Biol Commun 75(7):489–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Needham DM, Yoshizawa S, Hosaka T, Poirier C, Choi CJ, Hehenberger E, Irwin NAT, Wilken S, Yung CM, Bachy C et al (2019) A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators. Proc Natl Acad Sci USA 116(41):20574–20583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Needham DM, Poirier C, Hehenberger E, Jimenez V, Swalwell JE, Santoro AE, Worden AZ (2019) Targeted metagenomic recovery of four divergent viruses reveals shared and distinctive characteristics of giant viruses of marine eukaryotes. Philos Trans R Soc Lond B Biol Sci 374(1786):20190086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Theze J, Takatsuka J, Li Z, Gallais J, Doucet D, Arif B, Nakai M, Herniou EA (2013) New insights into the evolution of Entomopoxvirinae from the complete genome sequences of four entomopoxviruses infecting Adoxophyes honmai, Choristoneura biennis, Choristoneura rosaceana, and Mythimna separata. J Virol 87(14):7992–8003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bawden AL, Glassberg KJ, Diggans J, Shaw R, Farmerie W, Moyer RW (2000) Complete genomic sequence of the Amsacta moorei entomopoxvirus: analysis and comparison with other poxviruses. Virology 274(1):120–139

    Article  CAS  PubMed  Google Scholar 

  44. Bublitz M, Holland C, Sabet C, Reichelt J, Cossart P, Heinz DW, Bierne H, Schubert WD (2008) Crystal structure and standardized geometric analysis of InlJ, a listerial virulence factor and leucine-rich repeat protein with a novel cysteine ladder. J Mol Biol 378(1):87–96

    Article  CAS  PubMed  Google Scholar 

  45. Batkhishig D, Bilguun K, Enkhbayar P, Miyashita H, Kretsinger RH, Matsushima N (2018) Super secondary structure consisting of a polyproline II helix and a β-turn in leucine rich repeats in bacterial type III secretion system effectors. Protein J 37(3):223–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Figueroa-Bossi N, Bossi L (1999) Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol 33(1):167–176

    Article  CAS  PubMed  Google Scholar 

  47. Figueroa-Bossi N, Uzzau S, Maloriol D, Bossi L (2001) Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol Microbiol 39(2):260–271

    Article  CAS  PubMed  Google Scholar 

  48. Tisza MJ, Pastrana DV, Welch NL, Stewart B, Peretti A, Starrett GJ, Pang YS, Krishnamurthy SR, Pesavento PA, McDermott DH et al (2020) Discovery of several thousand highly diverse circular DNA viruses. eLife 9:e51971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Katharios P, Kalatzis PG, Kokkari C, Pavlidis M, Wang Q (2019) Characterization of a highly virulent Edwardsiella anguillarum strain isolated from Greek aquaculture, and a spontaneously induced prophage therein. Front Microbiol 10:141

    Article  PubMed  PubMed Central  Google Scholar 

  50. Yasuike M, Nishiki I, Iwasaki Y, Nakamura Y, Fujiwara A, Sugaya E, Kawato Y, Nagai S, Kobayashi T, Ototake M et al (2015) Full-genome sequence of a novel myovirus, GF-2, infecting Edwardsiella tarda: comparison with other Edwardsiella myoviral genomes. Arch Virol 160(8):2129–2133

    Article  CAS  PubMed  Google Scholar 

  51. Deeg CM, Chow CT, Suttle CA (2018) The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea. eLife 7:e33014

    Article  PubMed  PubMed Central  Google Scholar 

  52. Abrahao J, Silva L, Silva LS, Khalil JYB, Rodrigues R, Arantes T, Assis F, Boratto P, Andrade M, Kroon EG et al (2018) Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat Commun 9(1):749

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Alonso-Vega P, Normand P, Bacigalupe R, Pujic P, Lajus A, Vallenet D, Carro L, Coll P, Trujillo ME (2012) Genome sequence of Micromonospora lupini Lupac 08, isolated from root nodules of Lupinus angustifolius. J Bacteriol 194(15):4135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Wilson WH, Gilg IC, Moniruzzaman M, Field EK, Koren S, LeCleir GR, Martinez Martinez J, Poulton NJ, Swan BK, Stepanauskas R et al (2017) Genomic exploration of individual giant ocean viruses. ISME J 11(8):1736–1745

    Article  PubMed  PubMed Central  Google Scholar 

  55. Andreani J, Khalil JYB, Sevvana M, Benamar S, Di Pinto F, Bitam I, Colson P, Klose T, Rossmann MG, Raoult D et al (2017) Pacmanvirus, a new giant icosahedral virus at the crossroads between Asfarviridae and Faustoviruses. J Viol 91(14):e00212-17

    Google Scholar 

  56. Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, La Scola B, Suzan M, Claverie JM (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306(5700):1344–1350

    Article  CAS  PubMed  Google Scholar 

  57. Assis FL, Franco-Luiz APM, Dos Santos RN, Campos FS, Dornas FP, Borato PVM, Franco AC, Abrahao JS, Colson P, Scola B (2017) Genome characterization of the first Mimiviruses of lineage C isolated in Brazil. Front Microbiol 8:2562

    Article  PubMed  PubMed Central  Google Scholar 

  58. Legendre M, Santini S, Rico A, Abergel C, Claverie JM (2011) Breaking the 1000-gene barrier for Mimivirus using ultra-deep genome and transcriptome sequencing. Virol J 8:99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Boyer M, Azza S, Barrassi L, Klose T, Campocasso A, Pagnier I, Fournous G, Borg A, Robert C, Zhang X et al (2011) Mimivirus shows dramatic genome reduction after intraamoebal culture. Proc Natl Acad Sci USA 108(25):10296–10301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Takemura M, Mikami T, Murono S (2016) Nearly complete genome sequences of two Mimivirus strains isolated from a Japanese freshwater pond and river mouth. Genome Announc 4(6):e01378-16

    Article  PubMed  PubMed Central  Google Scholar 

  61. Colson P, Yutin N, Shabalina SA, Robert C, Fournous G, La Scola B, Raoult D, Koonin EV (2011) Viruses with more than 1,000 genes: Mamavirus, a new Acanthamoeba polyphaga mimivirus strain, and reannotation of Mimivirus genes. Genome Biol Evol 3:737–742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Desnues C, La Scola B, Yutin N, Fournous G, Robert C, Azza S, Jardot P, Monteil S, Campocasso A, Koonin EV et al (2012) Provirophages and transpovirons as the diverse mobilome of giant viruses. Proc Natl Acad Sci USA 109(44):18078–18083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Yoosuf N, Yutin N, Colson P, Shabalina SA, Pagnier I, Robert C, Azza S, Klose T, Wong J, Rossmann MG et al (2012) 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 4(12):1324–1330

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Jeudy S, Bertaux L, Alempic JM, Lartigue A, Legendre M, Belmudes L, Santini S, Philippe N, Beucher L, Biondi EG et al (2020) Exploration of the propagation of transpovirons within Mimiviridae reveals a unique example of commensalism in the viral world. ISME J 14(3):727–739

    Article  CAS  PubMed  Google Scholar 

  65. Bajrai LH, de Assis FL, Azhar EI, Jardot P, Robert C, Abrahao J, Raoult D, La Scola B (2016) Saudi Moumouvirus, the first group B mimivirus isolated from Asia. Front Microbiol 7:2029

    Article  PubMed  PubMed Central  Google Scholar 

  66. Boughalmi M, Pagnier I, Aherfi S, Colson P, Raoult D, La Scola B (2013) First isolation of a giant virus from wild Hirudo medicinalis leech: Mimiviridae isolation in Hirudo medicinalis. Viruses 5(12):2920–2930

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Chatterjee A, Ali F, Bange D, Kondabagil K (2013) Complete genome sequence of a new megavirus family member isolated from an Inland Water Lake for the first time in India. Genome Announc 4(3):e00402-16

    Article  Google Scholar 

  68. Boratto PV, Arantes TS, Silva LC, Assis FL, Kroon EG, La Scola B, Abrahao JS, Niemeyer Virus, (2015) A new Mimivirus group A isolate harboring a set of duplicated aminoacyl-tRNA synthetase genes. Front Microbiol 6:1256

    Article  PubMed  PubMed Central  Google Scholar 

  69. Campos RK, Boratto PV, Assis FL, Aguiar ER, Silva LC, Albarnaz JD, Dornas FP, Trindade GS, Ferreira PP, Marques JT et al (2014) Samba virus: a novel mimivirus from a giant rain forest, the Brazilian Amazon. Virol J 11:95

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Chatterjee A, Sicheritz-Ponten T, Yadav R, Kondabagil K (2019) Genomic and metagenomic signatures of giant viruses are ubiquitous in water samples from sewage, inland lake, waste water treatment plant, and municipal water supply in Mumbai, India. Sci Rep 9(1):3690

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Yoosuf N, Pagnier I, Fournous G, Robert C, La Scola B, Raoult D, Colson P (2014) Complete genome sequence of Courdo11 virus, a member of the family Mimiviridae. Virus Genes 48(2):218–223

    Article  CAS  PubMed  Google Scholar 

  72. Arslan D, Legendre M, Seltzer V, Abergel C, Claverie JM (2011) Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci USA 108(42):17486–17491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Saadi H, Pagnier I, Colson P, Cherif JK, Beji M, Boughalmi M, Azza S, Armstrong N, Robert C, Fournous G et al (2013) First isolation of Mimivirus in a patient with pneumonia. Clin Infect Dis 57(4):e127–e134

    Article  PubMed  Google Scholar 

  74. Kuchay S, Wang H, Marzio A, Jain K, Homer H, Fehrenbacher N, Philips MR, Zheng N, Pagano M (2019) GGTase3 is a newly identified geranylgeranyltransferase targeting a ubiquitin ligase. Nat Struct Mol Biol 26(7):628–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Andreani J, Khalil JYB, Baptiste E, Hasni I, Michelle C, Raoult D, Levasseur A, La Scola B (2017) Orpheovirus IHUMI-LCC2: a new virus among the giant viruses. Front Microbiol 8:2643

    Article  PubMed  Google Scholar 

  76. Skinner MA, Buller RM, Damon IK, Lefkowitz EJ, McFadden G, McInnes CJ, Mercer AA, Moyer RW, Upton C (2011) Poxviridae. Elsevier, Amsterdam

    Google Scholar 

  77. Rodriguez JM, Moreno LT, Alejo A, Lacasta A, Rodriguez F, Salas ML (2015) Genome sequence of African swine fever virus BA71, the virulent parental strain of the nonpathogenic and tissue-culture adapted BA71V. PloS One 10(11):e0142889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Portugal R, Coelho J, Hoper D, Little NS, Smithson C, Upton C, Martins C, Leitao A, Keil GM (2015) Related strains of African swine fever virus with different virulence: genome comparison and analysis. J Gen Virol 96(2):408–419

    Article  CAS  PubMed  Google Scholar 

  79. Bacciu D, Deligios M, Sanna G, Madrau MP, Sanna ML, Dei Giudici S, Oggiano A (2016) Genomic analysis of Sardinian 26544/OG10 isolate of African swine fever virus. Virol Rep 6:81–89

    Google Scholar 

  80. Granberg F, Torresi C, Oggiano A, Malmberg M, Iscaro C, De Mia GM, Belak S (2016) Complete genome sequence of an African swine fever virus isolate from Sardinia, Italy. Genome Announc 4(6):e01220-16

    Article  PubMed  PubMed Central  Google Scholar 

  81. Bishop RP, Fleischauer C, de Villiers EP, Okoth EA, Arias M, Gallardo C, Upton C (2015) Comparative analysis of the complete genome sequences of Kenyan African swine fever virus isolates within p72 genotypes IX and X. Virus Genes 50(2):303–309

    Article  CAS  PubMed  Google Scholar 

  82. Masembe C, Sreenu VB, Da Silva Filipe A, Wilkie GS, Ogweng P, Mayega FJ, Muwanika VB, Biek R, Palmarini M, Davison AJ: Genome Sequences of Five African swine fever virus genotype IX isolates from domestic pigs in Uganda. Microbiol Resour Announc 7(13):e01018-18

  83. Yanez RJ, Rodriguez JM, Nogal ML, Yuste L, Enriquez C, Rodriguez JF, Vinuela E (1995) Analysis of the complete nucleotide sequence of African swine fever virus. Virology 208(1):249–278

    Article  CAS  PubMed  Google Scholar 

  84. Chapman DA, Tcherepanov V, Upton C, Dixon LK (2008) Comparison of the genome sequences of non-pathogenic and pathogenic African swine fever virus isolates. J Gen Virol 89(2):397–408

    Article  CAS  PubMed  Google Scholar 

  85. de Villiers EP, Gallardo C, Arias M, da Silva M, Upton C, Martin R, Bishop RP (2010) Phylogenomic analysis of 11 complete African swine fever virus genome sequences. Virology 400(1):128–136

    Article  PubMed  CAS  Google Scholar 

  86. Chapman DA, Darby AC, Da Silva M, Upton C, Radford AD, Dixon LK (2011) Genomic analysis of highly virulent Georgia 2007/1 isolate of African swine fever virus. Emerg Infect Dis 17(4):599–605

    Article  PubMed  PubMed Central  Google Scholar 

  87. Farlow J, Donduashvili M, Kokhreidze M, Kotorashvili A, Vepkhvadze NG, Kotaria N, Gulbani A (2018) Intra-epidemic genome variation in highly pathogenic African swine fever virus (ASFV) from the country of Georgia. Virol J 15(1):190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Wen X, He X, Zhang X, Zhang X, Liu L, Guan Y, Zhang Y, Bu Z (2019) Genome sequences derived from pig and dried blood pig feed samples provide important insights into the transmission of African swine fever virus in China in 2018. Emerg Microb Infect 8(1):303–306

    Article  CAS  Google Scholar 

  89. Bao J, Wang Q, Lin P, Liu C, Li L, Wu X, Chi T, Xu T, Ge S, Liu Y et al (2019) Genome comparison of African swine fever virus China/2018/AnhuiXCGQ strain and related European p72 Genotype II strains. Transbound Emerg Dis 66(3):1167–1176

    Article  CAS  PubMed  Google Scholar 

  90. Vydelingum S, Baylis SA, Bristow C, Smith GL, Dixon LK (1993) Duplicated genes within the variable right end of the genome of a pathogenic isolate of African swine fever virus. J Gen Virol 74(10):2125–2130

    Article  CAS  PubMed  Google Scholar 

  91. Dixon LK, Twigg SR, Baylis SA, Vydelingum S, Bristow C, Hammond JM, Smith GL (1994) Nucleotide sequence of a 55 kbp region from the right end of the genome of a pathogenic African swine fever virus isolate (Malawi LIL20/1). J Gen Virol 75(7):1655–1684

    Article  CAS  PubMed  Google Scholar 

  92. Rodriguez JM, Salas ML, Vinuela E (1992) Genes homologous to ubiquitin-conjugating proteins and eukaryotic transcription factor SII in African swine fever virus. Virology 186(1):40–52

    Article  CAS  PubMed  Google Scholar 

  93. de Oliveira VL, Almeida SC, Soares HR, Crespo A, Marshall-Clarke S, Parkhouse RM (2011) A novel TLR3 inhibitor encoded by African swine fever virus (ASFV). Arch Virol 156(4):597–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Lepetit D, Gillet B, Hughes S, Kraaijeveld K, Varaldi J (2016) Genome Sequencing of the behavior manipulating virus LbFV reveals a possible new virus family. Genome Biol Evol 8(12):3718–3739

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Kariithi HM, Vlak JM, Jehle JA, Bergoin M, Boucias DG, Abd-Alla AMM, Ictv Report C (2019) ICTV virus taxonomy profile: Hytrosaviridae. J Gen Virol 100(9):1271–1272

    Article  CAS  PubMed  Google Scholar 

  96. Abd-Alla A, Bossin H, Cousserans F, Parker A, Bergoin M, Robinson A (2007) Development of a non-destructive PCR method for detection of the salivary gland hypertrophy virus (SGHV) in tsetse flies. J Virol Methods 139(2):143–149

    Article  CAS  PubMed  Google Scholar 

  97. Abd-Alla AMM, Kariithi HM, Cousserans F, Parker NJ, Ince IA, Scully ED, Boeren S, Geib SM, Mekonnen S, Vlak JM et al (2016) Comprehensive annotation of Glossina pallidipes salivary gland hypertrophy virus from Ethiopian tsetse flies: a proteogenomics approach. J Gen Virol 97(4):1010–1031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Taha A, Nour-El-Din A, Croizier L, Ferber ML, Croizier G (2000) Comparative analysis of the granulin regions of the Phthorimaea operculella and Spodoptera littoralis granuloviruses. Virus Genes 21(3):147–155

    Article  CAS  PubMed  Google Scholar 

  99. Jukes MD, Motsoeneng BM, Knox CM, Hill MP, Moore SD (2016) The comparative analysis of complete genome sequences from two South African betabaculoviruses: Phthorimaea operculella granulovirus and Plutella xylostella granulovirus. Arch Virol 161(10):2917–2920

    Article  CAS  PubMed  Google Scholar 

  100. Rodrigues RAL, Andreani J, Andrade A, Machado TB, Abdi S, Levasseur A, Abrahao JS, La Scola B (2018) Morphologic and genomic analyses of new isolates reveal a second lineage of Cedratviruses. J Virol 92(13):e00372-18

    Article  PubMed  PubMed Central  Google Scholar 

  101. Schvarcz CR, Steward GF (2018) A giant virus infecting green algae encodes key fermentation genes. Virology 518:423–433

    Article  CAS  PubMed  Google Scholar 

  102. Bezier A, Louis F, Jancek S, Periquet G, Theze J, Gyapay G, Musset K, Lesobre J, Lenoble P, Dupuy C et al (2013) Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata: insights into the evolutionary dynamics of bracoviruses. Philos Trans R Soc Lond B Biol Sci. 368(1626):20130047

    Article  PubMed  PubMed Central  Google Scholar 

  103. Coombes BK, Wickham ME, Brown NF, Lemire S, Bossi L, Hsiao WW, Brinkman FS, Finlay BB (2005) Genetic and molecular analysis of GogB, a phage-encoded type III-secreted substrate in Salmonella enterica serovar typhimurium with autonomous expression from its associated phage. J Mol Biol 348(4):817–830

    Article  CAS  PubMed  Google Scholar 

  104. Rubino JT, Franz KJ (2012) Coordination chemistry of copper proteins: how nature handles a toxic cargo for essential function. J Inorg Biochem 107(1):129–143

    Article  CAS  PubMed  Google Scholar 

  105. Daeffler KN, Lester HA, Dougherty DA (2012) Functionally important aromatic-aromatic and sulfur-pi interactions in the D2 dopamine receptor. J Am Chem Soc 134(36):14890–14896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Baxter RHG, Steinert S, Chelliah Y, Volohonsky G, Levashina EA, Deisenhofer J (2010) A heterodimeric complex of the LRR proteins LRIM1 and APL1C regulates complement-like immunity in Anopheles gambiae. Proc Natl Acad Sci USA 107(39):16817–16822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Chebrek R, Leonard S, de Brevern AG, Gelly JC (2014) PolyprOnline: polyproline helix II and secondary structure assignment database. Database (Oxford) 2014

  108. Craig KL, Tyers M (1999) The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol 72(3):299–328

    Article  CAS  PubMed  Google Scholar 

  109. Kipreos ET, Pagano M (2000) The F-box protein family. Genome Biol 1(5):REVIEWS3002

  110. Zhang X, Gonzalez-Carranza ZH, Zhang S, Miao Y, Liu VC-J, Roberts JA (2019) F-Box proteins in plants. Annu Plant Rev 2:1–21

    Google Scholar 

  111. Cenciarelli C, Chiaur DS, Guardavaccaro D, Parks W, Vidal M, Pagano M (1999) Identification of a family of human F-box proteins. Curr Biol 9(20):1177–1179

    Article  CAS  PubMed  Google Scholar 

  112. Legendre M, Bartoli J, Shmakova L, Jeudy S, Labadie K, Adrait A, Lescot M, Poirot O, Bertaux L, Bruley C et al (2014) Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc Natl Acad Sci USA 111(11):4274–4279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ER, Finnin MS, Elledge SJ, Harper JW, Pagano M, Pavletich NP (2000) Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408(6810):381–386

    Article  CAS  PubMed  Google Scholar 

  114. Xing W, Busino L, Hinds TR, Marionni ST, Saifee NH, Bush MF, Pagano M, Zheng N (2013) SCFFbxl3 ubiquitin ligase targets cryptochromes at their cofactor pocket. Nature 496(7443):64–68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Yao R, Ming Z, Yan L, Li S, Wang F, Ma S, Yu C, Yang M, Chen L, Chen L et al (2016) DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536(7617):469–473

    Article  CAS  PubMed  Google Scholar 

  116. Tully BJ, Graham ED, Heidelberg JF (2018) The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Sci Data 5:170203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Matheus Carnevali PB, Schulz F, Castelle CJ, Kantor RS, Shih PM, Sharon I, Santini JM, Olm MR, Amano Y, Thomas BC et al (2019) Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria. Nat Commun 10(1):463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Newton IL, Clark ME, Kent BN, Bordenstein SR, Qu J, Richards S, Kelkar YD, Werren JH (2016) Comparative genomics of two closely related Wolbachia with different reproductive effects on hosts. Genome Biol Evol 8(5):1526–1542

    Article  PubMed  PubMed Central  Google Scholar 

  119. Sinha A, Li Z, Sun L, Carlow CKS (2019) Complete genome sequence of the Wolbachia wAlbB endosymbiont of Aedes albopictus. Genome Biol Evol 11(3):706–720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Lefoulon E, Vaisman N, Frydman HM, Sun L, Foster JM, Slatko BE (2019) Large enriched fragment targeted sequencing (LEFT-SEQ) applied to capture of Wolbachia genomes. Sci Rep 9(1):5939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Ellegaard KM, Klasson L, Naslund K, Bourtzis K, Andersson SG (2013) Comparative genomics of Wolbachia and the bacterial species concept. PLoS Genet 9(4):e1003381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Abdelhamed H, Ramachandran R, Ozdemir O, Waldbieser G, Lawrence ML (2019) Characterization of a novel conjugative plasmid in Edwardsiella piscicida strain MS-18-199. Front Cell Infect Microbiol 9:404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F, Mayer C, Miller J, Monier A, Salamov A et al (2013) Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499(7457):209–213

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Bioinformatics, Institute of Tandem Repeats, Noboribetsu, 059-0464, Japan

    Norio Matsushima, Hiroki Miyashita & Shinsuke Tamaki

  2. Center for Medical Education, Sapporo Medical University, Sapporo, 060-8556, Japan

    Norio Matsushima

  3. Hokubu Rinsho Co., Ltd, Sapporo, 060-0061, Japan

    Hiroki Miyashita

  4. Department of Biology, University of Virginia, Charlottesville, VA, 22904, USA

    Robert H. Kretsinger

Authors
  1. Norio Matsushima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroki Miyashita
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shinsuke Tamaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert H. Kretsinger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Norio Matsushima.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: Tim Skern.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matsushima, N., Miyashita, H., Tamaki, S. et al. Shrinking of repeating unit length in leucine-rich repeats from double-stranded DNA viruses. Arch Virol 166, 43–64 (2021). https://doi.org/10.1007/s00705-020-04820-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-020-04820-2

Search

Navigation