Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease

English version

Autoři: Justine Charon ^aff001; Matthew J. Grigg ^aff002; John-Sebastian Eden ^aff001; Kim A. Piera ^aff002; Hafsa Rana ^aff004; Timothy William ^aff003; Karrie Rose ^aff007; Miles P. Davenport ^aff008; Nicholas M. Anstey ^aff002; Edward C. Holmes ^aff001
Působiště autorů: Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, New South Wales, Australia ^aff001; Global and Tropical Health Division, Menzies School of Health Research and Charles Darwin University, Darwin, Northern Territory, Australia ^aff002; Infectious Disease Society Kota Kinabalu Sabah – Menzies School of Health Research Clinical Research Unit, Kota Kinabalu, Sabah, Malaysia ^aff003; Centre for Virus Research, Westmead Institute for Medical Research, Westmead, New South Wales, Australia ^aff004; Clinical Research Centre – Queen Elizabeth Hospital, Kota Kinabalu, Sabah, Malaysia ^aff005; Gleneagles Hospital, Kota Kinabalu, Sabah, Malaysia ^aff006; Australian Registry of Wildlife Health, Taronga Conservation Society Australia, Mosman, New South Wales, Australia ^aff007; Kirby Institute for Infection and Immunity, University of New South Wales, Sydney, New South Wales, Australia ^aff008
Vyšlo v časopise: Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008216
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008216

Souhrn

Eukaryotes of the genus Plasmodium cause malaria, a parasitic disease responsible for substantial morbidity and mortality in humans. Yet, the nature and abundance of any viruses carried by these divergent eukaryotic parasites is unknown. We investigated the Plasmodium virome by performing a meta-transcriptomic analysis of blood samples taken from patients suffering from malaria and infected with P. vivax, P. falciparum or P. knowlesi. This resulted in the identification of a narnavirus-like sequence, encoding an RNA polymerase and restricted to P. vivax samples, as well as an associated viral segment of unknown function. These data, confirmed by PCR, are indicative of a novel RNA virus that we term Matryoshka RNA virus 1 (MaRNAV-1) to reflect its analogy to a "Russian doll": a virus, infecting a parasite, infecting an animal. Additional screening revealed that MaRNAV-1 was abundant in geographically diverse P. vivax derived from humans and mosquitoes, strongly supporting its association with this parasite, and not in any of the other Plasmodium samples analyzed here nor Anopheles mosquitoes in the absence of Plasmodium. Notably, related bi-segmented narnavirus-like sequences (MaRNAV-2) were retrieved from Australian birds infected with a Leucocytozoon—a genus of eukaryotic parasites that group with Plasmodium in the Apicomplexa subclass hematozoa. Together, these data support the establishment of two new phylogenetically divergent and genomically distinct viral species associated with protists, including the first virus likely infecting Plasmodium parasites. As well as broadening our understanding of the diversity and evolutionary history of the eukaryotic virosphere, the restriction to P. vivax may be of importance in understanding P. vivax-specific biology in humans and mosquitoes, and how viral co-infection might alter host responses at each stage of the P. vivax life-cycle.

Klíčová slova:

Birds – Mosquitoes – Parasitic diseases – Plasmodium – Protozoan infections – RNA viruses – Sequence alignment – Sequence motif analysis

Zdroje

1. Forterre P. Defining life: the virus viewpoint. Orig Life Evol Biosph. 2010; 40: 151–160. doi: 10.1007/s11084-010-9194-1 20198436

2. Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C, et al. The marine viromes of four oceanic regions. PLoS Biol. 2006; 4: e368. doi: 10.1371/journal.pbio.0040368 17090214

3. Culley AI, Lang AS, Suttle CA. Metagenomic analysis of coastal RNA virus communities. Science. 2006; 312: 1795–1798. doi: 10.1126/science.1127404 16794078

4. Desnues C, Rodriguez-Brito B, Rayhawk S, Kelley S, Tran T, Haynes M, et al. Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature. 2008; 452: 340–343. doi: 10.1038/nature06735 18311127

5. Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, et al. Uncovering Earth’s virome. Nature. 2016; 536: 425–430. doi: 10.1038/nature19094 27533034

6. Suttle CA. Viruses in the sea. Nature. 2005; 437: 356–361. doi: 10.1038/nature04160 16163346

7. Zhang Y-Z, Shi M, Holmes EC. Using metagenomics to characterize an expanding virosphere. Cell. 2018; 172: 1168–1172. doi: 10.1016/j.cell.2018.02.043 29522738

8. Miles MA. Viruses of parasitic protozoa. Parasitol Today. 1988; 4: 289–290. doi: 10.1016/0169-4758(88)90023-3 15463003

9. Khramtsov NV, Woods KM, Nesterenko MV, Dykstra CC, Upton SJ. Virus-like, double-stranded RNAs in the parasitic protozoan Cryptosporidium parvum. Mol Microbiol. 1997; 26: 289–300. doi: 10.1046/j.1365-2958.1997.5721933.x 9383154

10. Miller RL, Wang AL, Wang CC. Purification and characterization of the Giardia lamblia double-stranded RNA virus. Mol Biochem Parasitol. 1988; 28: 189–195. doi: 10.1016/0166-6851(88)90003-5 3386680

11. Tarr PI, Aline RF Jr, Smiley BL, Scholler J, Keithly J, Stuart K. LR1: a candidate RNA virus of Leishmania. Proc Natl Acad Sci USA. 1988; 85: 9572–9575. doi: 10.1073/pnas.85.24.9572 3200841

12. Wang AL, Wang CC. A linear double-stranded RNA in Trichomonas vaginalis. J Biol Chem. 1985; 260: 3697–3702. 2982874

13. Wang AL, Wang CC. Discovery of a specific double-stranded RNA virus in Giardia lamblia. Mol Biochem Parasitol. 1986; 21: 269–276. doi: 10.1016/0166-6851(86)90132-5 3807947

14. Widmer G, Comeau AM, Furlong DB, Wirth DF, Patterson JL. Characterization of a RNA virus from the parasite Leishmania. Proc Natl Acad Sci USA. 1989; 86: 5979–5982. doi: 10.1073/pnas.86.15.5979 2762308

15. Akopyants NS, Lye L-F, Dobson DE, Lukeš J, Beverley SM. A novel bunyavirus-like virus of trypanosomatid protist parasites. Genome Announce. 2016; 4: e00715–16. doi: 10.1128/genomeA.00715-16 27491985

16. Grybchuk D, Akopyants NS, Kostygov AY, Konovalovas A, Lye L-F, Dobson DE, et al. Viral discovery and diversity in trypanosomatid protozoa with a focus on relatives of the human parasite. Proc Natl Acad Sci USA. 2018; 115: E506–E515. doi: 10.1073/pnas.1717806115 29284754

17. Lye L-F, Akopyants NS, Dobson DE, Beverley SM. A narnavirus-like element from the trypanosomatid protozoan parasite Leptomonas seymouri. Genome Announce. 2016; 4: e00713–16. doi: 10.1128/genomeA.00713-16 27491984

18. Sukla S, Roy S, Sundar S, Biswas S. Leptomonas seymouri narna-like virus 1 and not leishmaniaviruses detected in kala-azar samples from India. Arch Virol. 2017; 162: 3827–3835. doi: 10.1007/s00705-017-3559-y 28939968

19. Padma TV. Russian doll disease is a virus inside a parasite inside a fly. New Scientist. August 10th, 2015. https://www.newscientist.com/article/dn28020-russian-doll-disease-is-a-virus-inside-a-parasite-inside-a-fly/.

20. Gómez-Arreaza A, Haenni A-L, Dunia I, Avilán L. Viruses of parasites as actors in the parasite-host relationship: A “ménage à trois”. Acta Tropica. 2017; 166:126–132. doi: 10.1016/j.actatropica.2016.11.028 27876650

21. Fichorova RN, Lee Y, Yamamoto HS, Takagi Y, Hayes GR, Goodman RP, et al. Endobiont viruses sensed by the human host—beyond conventional antiparasitic therapy. PLoS One. 2012; 7: e48418. doi: 10.1371/journal.pone.0048418 23144878

22. Ito MM, Catanhêde LM, Katsuragawa TH, da Silva CF Junior, Camargo LMA, de Godoi Mattos R, et al. Correlation between presence of Leishmania RNA virus 1 and clinical characteristics of nasal mucosal leishmaniosis. Braz J Otorhinol. 2015; 81: 533–540. doi: 10.1016/j.bjorl.2015.07.014 26277588

23. Ives A, Ronet C, Prevel F, Ruzzante G, Fuertes-Marraco S, Schutz F, et al. Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science. 2011; 331: 775–778. doi: 10.1126/science.1199326 21311023

24. Brettmann EA, Shaik JS, Zangger H, Lye L-F, Kuhlmann FM, Akopyants NS, et al. Tilting the balance between RNA interference and replication eradicates Leishmania RNA virus 1 and mitigates the inflammatory response. Proc Natl Acad Sci USA. 2016; 113: 11998–12005. doi: 10.1073/pnas.1615085113 27790981

25. Zangger H, Hailu A, Desponds C, Lye L-F, Akopyants NS, Dobson DE, et al. Leishmania aethiopica field isolates bearing an endosymbiontic dsRNA virus induce pro-inflammatory cytokine response. PLoS Negl Trop Dis. 2014; 8: e2836. doi: 10.1371/journal.pntd.0002836 24762979

26. Adaui V, Lye L-F, Akopyants NS, Zimic M, Llanos-Cuentas A, Garcia L, et al. Association of the endobiont double-stranded RNA virus LRV1 with treatment failure for human Leishmaniasis caused by Leishmania braziliensis in Peru and Bolivia. J Infect Dis. 2016; 213: 112–121. doi: 10.1093/infdis/jiv354 26123565

27. Bourreau E, Ginouves M, Prévot G, Hartley M-A, Gangneux J-P, Robert-Gangneux F, et al. Presence of Leishmania RNA Virus 1 in Leishmania guyanensis increases the risk of first-line treatment failure and symptomatic relapse. J Infect Dis. 2016; 213: 105–111. doi: 10.1093/infdis/jiv355 26123564

28. Nibert ML, Woods KM, Upton SJ, Ghabrial SA. Cryspovirus: a new genus of protozoan viruses in the family Partitiviridae. Arch Virol. 2009; 154: 1959–1965. doi: 10.1007/s00705-009-0513-7 19856142

29. Jenkins MC, Higgins J, Abrahante JE, Kniel KE, O’Brien C, Trout J, et al. Fecundity of Cryptosporidium parvum is correlated with intracellular levels of the viral symbiont CPV. Int J Parasitol. 2008; 38: 1051–1055. doi: 10.1016/j.ijpara.2007.11.005 18096164

30. Garnham PC, Bird RG, Baker JR. Electron microscope studies of motile stages of malaria parasites. III. The ookinetes of Haemamoeba and Plasmodium. Trans R Soc Trop Med Hyg. 1962; 56: 116–120. doi: 10.1016/0035-9203(62)90137-2 13897014

31. WHO. 2018. World Health Organization. World Malaria Report 2018.

32. Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Micro Rev. 2011; 24: 377–410. doi: 10.1128/CMR.00051-10 21482730

33. Grigg MJ, William T, Barber BE, Rajahram GS, Menon J, Schimann E, et al. Age-related clinical spectrum of Plasmodium knowlesi malaria and predictors of severity. Clin Infect Dis. 2018; 67: 350–359. doi: 10.1093/cid/ciy065 29873683

34. Shi M, Neville P, Nicholson J, Eden J-S, Imrie A, Holmes EC. High-resolution metatranscriptomics reveals the ecological dynamics of mosquito-associated RNA viruses in Western Australia. J Virol. 2017; 91: e00680–17. doi: 10.1128/JVI.00680-17 28637756

35. Illergård K, Ardell DH, Elofsson A. Structure is three to ten times more conserved than sequence—a study of structural response in protein cores. Proteins. 2009; 77: 499–508. doi: 10.1002/prot.22458 19507241

36. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protocol. 2015; 10: 845–858. doi: 10.1038/nprot.2015.053 25950237

37. Cai G, Myers K, Fry WE, Hillman BI. A member of the virus family Narnaviridae from the plant pathogenic oomycete Phytophthora infestans. Arch Virol. 2012; 157: 165–169. doi: 10.1007/s00705-011-1126-5 21971871

38. Di Giallonardo F, Schlub TE, Shi M, Holmes EC. Dinucleotide composition in animal RNA Viruses is shaped more by virus family than by host species. J Virol. 2017; 91: e02381–16. doi: 10.1128/JVI.02381-16 28148785

39. Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap T, Patil AP, Temperley WH, et al. The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2011; 4: 89. doi: 10.1186/1756-3305-4-89 21612587

40. Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X, Li C-X, et al. Redefining the invertebrate RNA virosphere. Nature. 2016; 540: 539–543. doi: 10.1038/nature20167 27880757

41. Hedges SB, Blair JE, Venturi ML, Shoe JL. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol Biol. 2004; 4: 2. doi: 10.1186/1471-2148-4-2 15005799

42. Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet. 2008; 9: 267–276. doi: 10.1038/nrg2323 18319742

43. Li C-X, Shi M, Tian J-H, Lin X-D, Kang Y-J, Chen L-J, et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife. 2015; 4: e05378. doi: 10.7554/eLife.05378 25633976

44. Akopyants NS, Lye L-F, Dobson DE, Lukeš J, Beverley SM. A narnavirus in the trypanosomatid protist plant pathogen Phytomonas serpens. Genome Announce. 2016; 4: e00711–16. doi: 10.1128/genomeA.00711-16 27469953

45. Rastgou M, Habibi MK, Izadpanah K, Masenga V, Milne RG, Wolf YI, et al. Molecular characterization of the plant virus genus Ourmiavirus and evidence of inter-kingdom reassortment of viral genome segments as its possible route of origin. J Gen Virol. 2009; 90: 2525–2535. doi: 10.1099/vir.0.013086-0 19535502

46. Dolja VV, Koonin EV. Capsid-less RNA viruses. eLS. 2012; doi: 10.1002/9780470015902.a0023269

47. Hillman BI, Cai G. The family Narnaviridae: simplest of RNA viruses. Adv Virus Res. 2013; 86:149–176. doi: 10.1016/B978-0-12-394315-6.00006-4 23498906

48. White NJ. Why do some primate malarias relapse? Trends Parasitol. 2016; 32: 918–920. doi: 10.1016/j.pt.2016.08.014 27743866

49. Pava Z, Burdam FH, Handayuni I, Trianty L, Utami RAS, Tirta YK, et al. Submicroscopic and asymptomatic Plasmodium parasitaemia associated with significant risk of anaemia in Papua, Indonesia. PLoS One. 2016; 11: e0165340. doi: 10.1371/journal.pone.0165340 27788243

50. Barber BE, William T, Grigg MJ, Parameswaran U, Piera KA, Price RN, et al. Parasite biomass-related inflammation, endothelial activation, microvascular dysfunction and disease severity in vivax malaria. PLoS Pathog. 2015; 11: e1004558. doi: 10.1371/journal.ppat.1004558 25569250

51. Padley D, Moody AH, Chiodini PL, Saldanha J. Use of a rapid, single-round, multiplex PCR to detect malarial parasites and identify the species present. Ann Trop Med Parasitol. 2003; 97: 131–137. doi: 10.1179/000349803125002977 12803868

52. Imwong M, Tanomsing N, Pukrittayakamee S, Day NPJ, White NJ, Snounou G. Spurious amplification of a Plasmodium vivax small-subunit RNA gene by use of primers currently used to detect P. knowlesi. J Clin Micro. 2009; 47: 4173–4175. doi: 10.1128/jcm.00811-09 19812279

53. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30: 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404

54. Kopylova E, Noé L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012; 28: 3211–3217. doi: 10.1093/bioinformatics/bts611 23071270

55. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Meth. 2012; 9: 357–359. doi: 10.1038/nmeth.1923 22388286

56. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotech 2011; 29: 644–652. doi: 10.1038/nbt.1883 21572440

57. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12: 323. doi: 10.1186/1471-2105-12-323 21816040

58. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Meth. 2015; 12: 59–60. doi: 10.1038/nmeth.3176 25402007

59. Wickham H. 2009. ggplot2: Elegant Graphics for Data Analysis. Springer.

60. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012; 28: 1647–1649. doi: 10.1093/bioinformatics/bts199 22543367

61. Remmert M, Biegert A, Hauser A, Söding J. HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat Meth. 2012; 9: 173–175. doi: 10.1038/nmeth.1818 22198341

62. Söding J. Protein homology detection by HMM-HMM comparison. Bioinformatics. 2005; 21: 951–960. doi: 10.1093/bioinformatics/bti125 15531603

63. Su M-W, Lin H-M, Yuan HS, Chu W-C. Categorizing host-dependent RNA viruses by principal component analysis of their codon usage preferences. J Comp Biol. 2009; 16: 1539–1547. doi: 10.1089/cmb.2009.0046 19958082

64. Puigbò P, Bravo IG, Garcia-Vallve S. CAIcal: a combined set of tools to assess codon usage adaptation. Biol Direct. 2008; 3: 38. doi: 10.1186/1745-6150-3-38 18796141

65. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001; 305: 567–580. doi: 10.1006/jmbi.2000.4315 11152613

66. Mulder N, Apweiler R. InterPro and InterProScan: Tools for protein sequence classification and comparison. Meth Mol Biol. 2007; 396: 59–70. doi: 10.1007/978-1-59745-515-2_5 18025686

67. Boratyn GM, Thierry-Mieg J, Thierry-Mieg D, Busby B, Madden TL. Magic-BLAST, an accurate DNA and RNA-seq aligner for long and short reads. bioRxiv 2018; doi: 10.1101/390013

68. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30: 772–780. doi: 10.1093/molbev/mst010 23329690

69. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000; 17: 540–552. doi: 10.1093/oxfordjournals.molbev.a026334 10742046

70. Lefort V, Longueville J-E, Gascuel O. SMS: Smart Model Selection in PhyML. Mol Biol Evol. 2017; 34: 2422–2424. doi: 10.1093/molbev/msx149 28472384

71. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Meth. 2017; 14: 587–589. doi: 10.1038/nmeth.4285 28481363

72. Guindon S, Delsuc F, Dufayard J-F, Gascuel O. Estimating Maximum Likelihood Phylogenies with PhyML. Meth Mol Biol. 2009; 537: 113–137. doi: 10.1007/978-1-59745-251-9_6 19378142

73. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015; 32: 268–274. doi: 10.1093/molbev/msu300 25371430

74. Pacheco MA, Cepeda AS, Bernotienė R, Lotta IA, Matta NE, Valkiūnas G, et al. Primers targeting mitochondrial genes of avian haemosporidians: PCR detection and differential DNA amplification of parasites belonging to different genera. Int J Parasitol. 2018; 48: 657–670. doi: 10.1016/j.ijpara.2018.02.003 29625126