Advertisement

Parasitology Research

, Volume 114, Issue 11, pp 3959–3967 | Cite as

Viruses in close associations with free-living amoebae

  • Patrick ScheidEmail author
Review

Abstract

As both groups of organisms, free-living amoebae (FLA) and viruses, can be found in aquatic environments side by side, it appears obvious that there are multiple interactions with respect to host—endocytobiont relationships. Several relationships between viruses and protozoan hosts are described and it was the discovery of the so called “giant viruses,” associated with amoebae, which gave another dimension to these interactions. Mimiviruses, Pandoraviruses and Pithoviruses are examples for interesting viral endocytobionts within FLA. In the Mimivirus viral factories, viral DNA undergoes replication and transcription, and the DNA is prepared to be packed in procapsids. Theses Mimivirus factories can be considered as efficient “production lines” where, at any given moment, all stages of viral generation including membrane biogenesis, capsid assembly and genome encapsidation, are occurring concomitantly. There are some hints that similar replication factories are involved as well during the Pandoravirus development. Some scientists favour the assumption that the giant viruses have received many of their genes from their hosts or from sympatric occurring endocytobionts via lateral gene transfer. This hypothesis would mean that this type of transfer has been an important process in the evolution of genomes in the context of the intracellular parasitic or endocytobiotic lifestyle. In turn, that would migitate against hypothesizing development of a new branch in the tree of life. Based on the described scenarios to explain the presence of genes related to translation, it is also possible that earlier ancestors of today’s DNA viruses were involved in the origin of eukaryotes. That possibly could in turn support the idea that cellular organisms could have evolved from viruses with growing autarkic properties. In future we expect the discovery of further (giant) viruses within free-living amoebae and other protozoa through genomic, transcriptomic and proteomic analyses.

Keywords

Viruses Free living amoebae Acanthamoeba Pandoravirus Mimivirus Pithovirus Endocytobiont 

Notes

Acknowledgements

I want to thank B. Hauroeder and team (ZInstSanBw Koblenz) and Lars Möller (RKI) for the outstanding EM-photos. I thank Albrecht Kiderlen and Rolf Michel for their fruitful discussions, David Lam (Shaman Medical Consulting) for review and English-language editing of the article.

References

  1. Abrahao J, Dornas F, Silva L, Almeida G, Boratto P, Colson P, La Scola B, Kroon E (2014) Acanthamoeba polyphaga Mimivirus and other giant viruses: an open field to outstanding discoveries. Virology Journal 11:120PubMedCentralCrossRefPubMedGoogle Scholar
  2. Antwerpen M, Georgi E, Zoeller L, Woelfel R, Stoecker K, Scheid P (2015) Whole-genome sequencing of a Pandoravirus isolated from keratitis-inducing Acanthamoeba. Genome Announc 3(2):e00136–15. doi: 10.1128/genomeA.00136-15 PubMedCentralCrossRefPubMedGoogle Scholar
  3. Bandea C (1983) A new theory on the origin and the nature of viruses. J Theor Biol 105:591–602CrossRefPubMedGoogle Scholar
  4. Bandea C (2009) The origin and evolution of viruses as molecular organisms. Nature proceedings: hdl:10101/npre.2009.3886.1Google Scholar
  5. Barker J, Lambert P, Brown M (1992) Influence of intra-amoebic and other growth conditions on the surface properties of Legionella pneumophila. Infect Immun 61:3503–3510Google Scholar
  6. Baron D, Danglot C, Vilagines R (1980) Role of a free-living amoeba from water, Acanthamoeba castellanii, in the transport of naked or enveloped animal viruses. CR Seances Acad Sci D 291; 629–632Google Scholar
  7. Battistini R, Marcucci E, Verania M, Di Guiseppe G, Dini F, Carduccia A (2013) Ciliate-Adenovirus interactions in experimental co-cultures of Eupletes octocarinatus and in wastewater environment. Eur J Protistol 49:381–388CrossRefPubMedGoogle Scholar
  8. Boyer M, Yutin N, Pagnier I (2009) Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. Proc Natl Acad Sci 106:21848–22853PubMedCentralCrossRefPubMedGoogle Scholar
  9. Chelikani V, Ranjan T, Kondabagil K (2014a) Revisiting the genome packaging in viruses with lessons from the “Giants”. Virology 466-467:15-26Google Scholar
  10. Chelikani V, Ranjan T, Zade A, Shukla A, Kondabagil K (2014b) Genome segregation and packaging machinery in Acanthamoeba polyphaga Mimivirus is reminiscent of bacterial apparatus. J Virol 88: 6069-6075Google Scholar
  11. Claverie J (2006) Viruses take center stage in cellular evolution. Genome Biol 7:110PubMedCentralCrossRefPubMedGoogle Scholar
  12. Claverie J, Abergel C (2011) Family Mimiviridae. Virus Taxonomy, ninth report of the International Committee on Taxonomy of Viruses (ICTV), Elsevier, Academic Press, ISBN : 978-0-12-384684-6; 223–228Google Scholar
  13. Colson P, Raoult D (2010) Gene repertoire of amoeba-associated giant viruses. Intervirology 53(5):330–343CrossRefPubMedGoogle Scholar
  14. Colson P, De Lamballerie X, Fournous G, Raoult D (2012) Reclassification of giant viruses composing a fourth domain in the new order Megavirales. Intervirology 55:321–332CrossRefPubMedGoogle Scholar
  15. Colson P, La Scola B, Raoult D (2013) Giant viruses of amoebae as potential human pathogens. Intervirology 56:376–385CrossRefPubMedGoogle Scholar
  16. Danes L, Cerva L (1981) Survival of Polioviruse and Echoviruses in Acanthamoeba castellanii cultivated in vitro. J Hyg Epidemiol Microbiol Immunol 25(2):169–174PubMedGoogle Scholar
  17. Dare R, Chittaganpitch M, Erdman D (2008) Screening pneumonia patients for Mimivirus. Emerg Infect Dis 14:465–467PubMedCentralCrossRefPubMedGoogle Scholar
  18. De Silva F, Moss B (2005) Origin-independent plasmid replication occurs in vaccinia virus cytoplasmic factories and requires all five known poxvirus replication factors. Virol J doi: 10.186/1743-422X-2-23Google Scholar
  19. Desnues C, La Scola B, Yutin N, Fournous G, Robert C, Azza S, Jardot P, Monteil S, Campocasso A, Koonin E, Raoult D (2012) Provirophages and transportvirons as the diverse mobilome of giant viruses. Proc Natl Acad Sci USA 109:18078–18083PubMedCentralCrossRefPubMedGoogle Scholar
  20. Diamond L, Mattern C (1976) Protozoal viruses. Adv Virus Res 20:87–112CrossRefPubMedGoogle Scholar
  21. Dunnebacke T, Schuster F (1971) Infectious agent from a free-living soil amoeba, Naegleria gruberi. Science 174:516–518CrossRefPubMedGoogle Scholar
  22. Dunnebacke T, Schuster F (1974) An infectious agent associated with amebas oft he genus Naegleria. J Protozool 21:327–329CrossRefPubMedGoogle Scholar
  23. Fischer M, Allen M, Wilson W, Suttle C (2010) Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci USA 107:19508–19513PubMedCentralCrossRefPubMedGoogle Scholar
  24. Gajdatsy A, Kosmin A, Barrett G (2008) Coexistent adenoviral keratoconjunctivitis and Acanthamoeba keratitis; Clin & Exp Ophtal; doi:  10.1046/j.1442-9071.2000.00352.x
  25. Ghigo E, Kartenbeck J, Lien P, Pelkmans L, Capo C, Mege J-L, Raoult D (2008) Amebal pathogen Mimivirus infects macrophages through phagocytosis. PLoS Pathogens 4, e1000087PubMedCentralCrossRefPubMedGoogle Scholar
  26. Greub G, Raoult D (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17:413–433PubMedCentralCrossRefPubMedGoogle Scholar
  27. Hoffmann R, Michel R, Müller K-D, Schmid E (1998) Archaea-like endocytobiotic organisms isolated from Acanthamoeba sp. (Gr II). Endo Cell Res 12:185–188Google Scholar
  28. Hsueh T, Gibson K (2015) Interactions between Human Norovirus Surrogates and Acanthamoeba spp.. Appl Environ Microbiol. 81(12):4005-13. doi: 10.1128/AEM.00649-15. Epub 2015 Apr 3. Google Scholar
  29. Khan N (2009) Acanthamoeba, biology and pathogenesis. Caister Academic Press, NorfolkGoogle Scholar
  30. Klose T, Kuznetsov Y, Xiao C, Sun S, McPherson A, Rossmann M (2010) The three-dimensional structure of Mimivirus. 53; 268–273; DOI:  10.1159/000312911
  31. Koonin E (2005) Virology; Gulliver among the Lilliputians. Curr Biol 15:167–169CrossRefGoogle Scholar
  32. La Scola B, Audic S, Robert C, Jungjang L, De Lamballerie X, Drancourt M, Birtles R, Claverie J, Raoult D (2003) A giant virus in amoebae. Science 299:5615CrossRefGoogle Scholar
  33. La Scola B, Marrie T, Auffray J, Raoult D (2005) Mimivirus in pneumonia patients. Emerg Infect Dis 11:449–452PubMedCentralCrossRefPubMedGoogle Scholar
  34. La Scola B, Desnues C, Pagnier I, Robert C, Barassi L, Fournous G, Merchat M, Suzan-Monti M, Forterre P, Koonin E, Raoult D (2008) The virophage as a unique parasite of the giant Mimivirus. Nature 445:100–105CrossRefGoogle Scholar
  35. La Scola B, Campocasso A, N’dong R, Fournous G, Barrassi L, Flaudrops C, Raoult D (2010) Tentative characterization of new environmental giant viruses by MALDI-TOF mass spectrometry. Intervirology 53:344–353CrossRefPubMedGoogle Scholar
  36. Lamrabet O, Merhej V, Pontarotti P, Raoult D, Drancourt M (2012) The genealogic tree of Mycobacteria reveals a long standing sympatric life into free-living protozoa. PLoS ONE 7, e34754PubMedCentralCrossRefPubMedGoogle Scholar
  37. Legendre M, Bartoli J, Shmakova L, Jeudy S, Labadie K, Adrait A, Lescot M, Poirot O, Bertaux L, Bruley C, Coute Y, Rivkina E, Abergel C, Claverie J (2014) Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a Pandoravirus morphology. PNAS 111:4274–4279PubMedCentralCrossRefPubMedGoogle Scholar
  38. Lorenzo-Morales J, Coronado-Alvarez N, Martinez-Carretero E, Maciver S, Valladares B (2007) Detection of four Adenovirus serotypes within water-isolated strains of Acanthamoeba in the Canary Islands, Spain. Am J Trop Med Hyg 77(4):753–756PubMedGoogle Scholar
  39. Margulis L, Schwartz K (1989) Die fünf Reiche der Organismen. Ein Leitfaden. Spektrum-der-Wissenschaft-Verlagsgesellschaft mbH & Co, HeidelbergGoogle Scholar
  40. Mattana A, Serra C, Mariotti E, Delogu G, Fiori P, Cappucinelli P (2006) Acanthamoeba castellanii promotion of in vitro survival and transmission of Coxsackie B3 viruses. Eukaryotic Cel 5(4):665–671CrossRefGoogle Scholar
  41. Michel R, Müller K-D, Schmid E, Zöller L, Hoffmann R (2003) Endocytobiont KC 5/2 induces transformation into sol-like cytoplasm of its host Acanthamoeba sp. as substrate for his own development. Parasitol Res 90:52–56PubMedGoogle Scholar
  42. Miller J, Swartzwelder J (1960) Virus-like particles in an Entamoeba histolytica trophozoite. Parasite 46:523–524CrossRefGoogle Scholar
  43. Moliner C, Raoult D, Fournier P (2009) Evidence that intra-amoebal Legionella drancourtii acquired a sterol reductase gene from eukaryotes. BMC Res Notes 2:51PubMedCentralCrossRefPubMedGoogle Scholar
  44. Molmeret M, Horn M, Wagner M, Santic M, Kwaik Y (2005) Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 71:20–28PubMedCentralCrossRefPubMedGoogle Scholar
  45. Moreira D, Brochier-Armanet C (2008) Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol Biol 8:12. doi: 10.1186/1471-2148-8-12 PubMedCentralCrossRefPubMedGoogle Scholar
  46. Mutsafi Y, Zauberman N, Sabanay I, Minsky A (2010) Vaccinia-like cytoplasmic replication oft he giant Mimivirus. Proc Natl Acad Sci USA 107:5978–5982PubMedCentralCrossRefPubMedGoogle Scholar
  47. Mutsafi Y, Shimoni E, Shimion A, Minsky A (2013) Membrane assembly during the infection cycle of the giant Mimivirus. PLOS Pathogens 9:e1003367PubMedCentralCrossRefPubMedGoogle Scholar
  48. Ngounga T, Pagnier I, Reteno D, Raoult D, La Scola B, Colson P (2013) Real-time PCR targeting giant viruses of amoebae and their virophages. Intervirology 56:413–423CrossRefPubMedGoogle Scholar
  49. Oliveira S, Costa J (1995) Replication of transfected plasmid DNA by cells infected with African swine fever virus. Virology 207:392–399CrossRefPubMedGoogle Scholar
  50. Philippe N, Legendre M, Doutre G, Coute Y, Poirot O, Lescot M, Arslan D, Seltzer V, Bertraux L, Bruley C, Garin J, Claverie J, Abergel C (2013) Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341:281–286CrossRefPubMedGoogle Scholar
  51. Popgeorgiev N, Boyer M, Fancello L, Monteil S, Robert C, Rivet R, Nappez C, Azza S, Chiaroni J, Raoult D, Desnues C (2013) Marseillevirus-like virus recovered from blood donated by asymptomatic humans. J Infect Dis 208:1042–1050. doi: 10.1093/infdis/jit292 CrossRefPubMedGoogle Scholar
  52. Raoult D, Boyer M (2010) Amoebae as genitors and reservoirs of giant viruses. Intervirology 53:321–329CrossRefPubMedGoogle Scholar
  53. Raoult D, Forterre P (2008) Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 6:315–319CrossRefPubMedGoogle Scholar
  54. Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, La Scola B, Suzan M, Claverie J (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306:1344–1350CrossRefPubMedGoogle Scholar
  55. Raoult D, Renesto P, Brouqui P (2006) Laboratory infection of a technician by Mimivirus. Ann Intern Med 144(9):702–703CrossRefPubMedGoogle Scholar
  56. Raoult D, La Scola B, Birtles R (2007) The discovery and characterization of Mimivirus, the largest known virus and putative pneumonia agent. Emerg Inf 45:95–101Google Scholar
  57. Saadi H, Pagnier I, Colson P, Cherif J, Beji M, Boughalmi M, Azza S, Armstrong N, Robert C, Fournous G, La Scola B, Raoult D (2013) First isolation of Mimivirus in a patient with pneumonia. Clin Infect Dis; 57; doi:  10.1093/cid/cit354
  58. Scheid P (2008) Freilebende Amöben als Krankheitserreger und Vektoren. Wehr Med Mo 52:171–175Google Scholar
  59. Scheid P (2014) Relevance of free-living amoebae as hosts for phylogenetically diverse microorganisms. Parasitol Res 113:2407–2414. doi: 10.1007/s00436-014-3932-7 CrossRefPubMedGoogle Scholar
  60. Scheid P, Schwarzenberger R (2012) Acanthamoeba spp. as vehicle and reservoir of adenoviruses; Parasitol Res; doi  10.1007/s00436-012-2828-7
  61. Scheid P, Pressmar S, Richard G, Zöller R, Michel R (2008) An extraordinary endocytobiont in Acanthamoeba sp. isolated from a patient with keratitis. Parasitol Res 102:945–950CrossRefPubMedGoogle Scholar
  62. Scheid P, Hauroeder B, Michel R (2010) Investigations of an extraordinary endocytobiont in Acanthamoeba sp.: development and replication. Parasitol Res 106:1371–1377CrossRefPubMedGoogle Scholar
  63. Scheid P, Balczun C, Schaub G (2014) Some secrets are revealed: parasitic keratitis amoebae as vectors of the scarcely described Pandoraviruses to humans. Parasitol Res 113(10):3759–3764. doi: 10.1007/s00436-014-4041-3 CrossRefPubMedGoogle Scholar
  64. Schuster F (1969) Intranuclear virus-like bodies in the amoeboflagellate Naegleria gruberi. J Protozool 16:724–727CrossRefPubMedGoogle Scholar
  65. Selinka H, Botzenhart K, Feuerpfeil I, Puchert W, Schmoll O, Szewzyk R, Willmitzer H (2011) Nachweis von Viren im Rohwasser als Grundlage einer Risikoabschätzung. Bundesgesundheitsbl 54:496–504CrossRefGoogle Scholar
  66. Sharma V, Colson P, Giorgi R, Pontarotti P, Raoult D (2014) DNA-dependent RNA polymerase detects hidden giant viruses in published databanks. Genome Biol Evol 6:1–22. doi: 10.1093/gbe/evu128 CrossRefGoogle Scholar
  67. Sharma V, Colson P, Chabrol O, Scheid P, Pontarotti P, Raoult D (2015a) Welcome to pandoraviruses at the “Fourth TRUC” club. Front Microbiol 6:423. doi: 10.3389/fmicb.2015.00423
  68. Sharma V, Colson P, Chabrol O, Pontarotti P, Raoult D (2015b) Pithovirus sibericum, a new bona fide member of the “Fourth TRUC” club. Front Microbiol 6:722. doi: 10.3389/fmicb.2015.00722
  69. Suzan-Monti M, La Scola B, Barrassi L, Espinosa L, Raoult D (2007) Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS ONE 2:e328. doi: 10.1371/journal.pone.0000328 PubMedCentralCrossRefPubMedGoogle Scholar
  70. Thomas V, Greub G (2010) Amoeba/Amoebal symbiont genetic transfers: lessons from giant virus neighbours. Intervirology 53:254–267CrossRefPubMedGoogle Scholar
  71. Van Regenmortel M (2000) 7th report of the international committee on the taxonomy of viruses. Academic, San Diego, pp 3–16Google Scholar
  72. Woese C, Kandler O, Wheelis M (1990) Towards a natural sytem of organisms: proposal for the domains Archaea, Bacteria and Eucarya. Proc Natl Acad Sci USA 87:4576–4579PubMedCentralCrossRefPubMedGoogle Scholar
  73. Yoosuf N, Yutin N, Colson P, Shabalina S, Pagnier I, Robert C, Azza S, Klose T, Wong J, Rossmann M, La Scola B, Raoult D, Koonin E (2012) Related giant viruses in distinct locations and different habitats: Acanthamoeba polyphaga Moumouvirus represents a third lineage of the Mimiviridae that is close to the megavirus lineage. Genome Biol Evol 4:1324–1330PubMedCentralCrossRefPubMedGoogle Scholar
  74. Yutin N, Koonin E (2013) Pandoraviruses are highly derived phycodnaviruses. Biol Direct 8:25. doi: 10.1186/1745-6150-8-25 PubMedCentralCrossRefPubMedGoogle Scholar
  75. Zauberman N, Mutsafi Y, Havely D, Shimoni E, Klein E, Xiao C, Sund S, Minsky A (2008) Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga Mimivirus. PLoS Biol 6:e114, 1104–1114Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Central Institute of the Bundeswehr Medical Service KoblenzKoblenzGermany

Personalised recommendations