Skip to main content
Top
Published in: Virology Journal 1/2014

Open Access 01-12-2014 | Research

Samba virus: a novel mimivirus from a giant rain forest, the Brazilian Amazon

Authors: Rafael K Campos, Paulo V Boratto, Felipe L Assis, Eric RGR Aguiar, Lorena CF Silva, Jonas D Albarnaz, Fabio P Dornas, Giliane S Trindade, Paulo P Ferreira, João T Marques, Catherine Robert, Didier Raoult, Erna G Kroon, Bernard La Scola, Jônatas S Abrahão

Published in: Virology Journal | Issue 1/2014

Login to get access

Abstract

Background

The identification of novel giant viruses from the nucleocytoplasmic large DNA viruses group and their virophages has increased in the last decade and has helped to shed light on viral evolution. This study describe the discovery, isolation and characterization of Samba virus (SMBV), a novel giant virus belonging to the Mimivirus genus, which was isolated from the Negro River in the Brazilian Amazon. We also report the isolation of an SMBV-associated virophage named Rio Negro (RNV), which is the first Mimivirus virophage to be isolated in the Americas.

Methods/results

Based on a phylogenetic analysis, SMBV belongs to group A of the putative Megavirales order, possibly a new virus related to Acanthamoeba polyphaga mimivirus (APMV). SMBV is the largest virus isolated in Brazil, with an average particle diameter about 574 nm. The SMBV genome contains 938 ORFs, of which nine are ORFans. The 1,213.6 kb SMBV genome is one of the largest genome of any group A Mimivirus described to date. Electron microscopy showed RNV particle accumulation near SMBV and APMV factories resulting in the production of defective SMBV and APMV particles and decreasing the infectivity of these two viruses by several logs.

Conclusion

This discovery expands our knowledge of Mimiviridae evolution and ecology.
Appendix
Available only for authorised users
Literature
1.
go back to reference Yamada T: Giant viruses in the environment: their origins and evolution. Curr Opin Virol. 2011, 1: 58-62. 10.1016/j.coviro.2011.05.008.PubMedCrossRef Yamada T: Giant viruses in the environment: their origins and evolution. Curr Opin Virol. 2011, 1: 58-62. 10.1016/j.coviro.2011.05.008.PubMedCrossRef
2.
go back to reference Culley AI: Virophages to viromes: a report from the frontier of viral oceanography. Curr Opin Virol. 2011, 1: 52-57. 10.1016/j.coviro.2011.05.003.PubMedCrossRef Culley AI: Virophages to viromes: a report from the frontier of viral oceanography. Curr Opin Virol. 2011, 1: 52-57. 10.1016/j.coviro.2011.05.003.PubMedCrossRef
3.
go back to reference La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D: A giant virus in amoebae. Science. 2003, 299: 2033-10.1126/science.1081867.PubMedCrossRef La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D: A giant virus in amoebae. Science. 2003, 299: 2033-10.1126/science.1081867.PubMedCrossRef
4.
go back to reference Arslan D, Legendre M, Seltzer V, Abergel C, Claverie J: Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci U S A. 2011, 108: 17486-17491. 10.1073/pnas.1110889108.PubMedPubMedCentralCrossRef Arslan D, Legendre M, Seltzer V, Abergel C, Claverie J: Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci U S A. 2011, 108: 17486-17491. 10.1073/pnas.1110889108.PubMedPubMedCentralCrossRef
5.
go back to reference Legendre M, Arslan D, Abergel C, Claverie JM: Genomics of Megavirus and the elusive fourth domain of Life. Commun Integr Biol. 2012, 5: 102-106. 10.4161/cib.18624.PubMedPubMedCentralCrossRef Legendre M, Arslan D, Abergel C, Claverie JM: Genomics of Megavirus and the elusive fourth domain of Life. Commun Integr Biol. 2012, 5: 102-106. 10.4161/cib.18624.PubMedPubMedCentralCrossRef
7.
go back to reference Xiao C, Chipman PR, Battisti AJ, Bowman VD, Renesto P, Raoult D, Rossmann MG: Cryo-electron microscopy of the giant Mimivirus. J Mol Biol. 2005, 28 (3): 493-496. 353CrossRef Xiao C, Chipman PR, Battisti AJ, Bowman VD, Renesto P, Raoult D, Rossmann MG: Cryo-electron microscopy of the giant Mimivirus. J Mol Biol. 2005, 28 (3): 493-496. 353CrossRef
8.
go back to reference Zauberman N, Mutsafi Y, Halevy DB, Shimoni E, Klein E, Xiao C, Sun S, Minsky A: Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol. 2008, 13;6 (5): e114-CrossRef Zauberman N, Mutsafi Y, Halevy DB, Shimoni E, Klein E, Xiao C, Sun S, Minsky A: Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol. 2008, 13;6 (5): e114-CrossRef
9.
go back to reference Boughalmi M, Saadi H, Pagnier I, Colson P, Fournous G, Raoult D, La Scola B: High-throughput isolation of giant viruses of the Mimiviridae and Marseilleviridae families in the Tunisian environment. Environ Microbiol. 2012, 53: 344-353. Boughalmi M, Saadi H, Pagnier I, Colson P, Fournous G, Raoult D, La Scola B: High-throughput isolation of giant viruses of the Mimiviridae and Marseilleviridae families in the Tunisian environment. Environ Microbiol. 2012, 53: 344-353.
11.
go back to reference Monier A, Larsen JB, Sandaa RA, Bratbak G, Claverie JM, Ogata H: Marine mimivirus relatives are probably large algal viruses. Virol J. 2008, 5: 12-10.1186/1743-422X-5-12.PubMedPubMedCentralCrossRef Monier A, Larsen JB, Sandaa RA, Bratbak G, Claverie JM, Ogata H: Marine mimivirus relatives are probably large algal viruses. Virol J. 2008, 5: 12-10.1186/1743-422X-5-12.PubMedPubMedCentralCrossRef
12.
go back to reference Williamson SJ, Allen LZ, Lorenzi HA, Fadrosh DW, Brami D, Thiagarajan M, McCrow JP, Tovchigrechko A, Yooseph S, Venter JC: Metagenomic exploration of viruses throughout the Indian Ocean. PLoS One. 2012, 7: e42047-10.1371/journal.pone.0042047.PubMedPubMedCentralCrossRef Williamson SJ, Allen LZ, Lorenzi HA, Fadrosh DW, Brami D, Thiagarajan M, McCrow JP, Tovchigrechko A, Yooseph S, Venter JC: Metagenomic exploration of viruses throughout the Indian Ocean. PLoS One. 2012, 7: e42047-10.1371/journal.pone.0042047.PubMedPubMedCentralCrossRef
13.
go back to reference La Scola B, Desnues C, Pagnier I, Robert C, Barrassi L, Fournous G, Merchat M, Suzan-Monti M, Forterre P, Koonin E, Raoult D: The virophage as a unique parasite of the giant mimivirus. Nature. 2008, 455: 100-104. 10.1038/nature07218.PubMedCrossRef La Scola B, Desnues C, Pagnier I, Robert C, Barrassi L, Fournous G, Merchat M, Suzan-Monti M, Forterre P, Koonin E, Raoult D: The virophage as a unique parasite of the giant mimivirus. Nature. 2008, 455: 100-104. 10.1038/nature07218.PubMedCrossRef
14.
go back to reference Yau S, Lauro FM, DeMaere MZ, Brown MV, Thomas T, Raftery MJ, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Gibson JA, Cavicchioli R: Virophage control of antarctic algal host-virus dynamics. Proc Natl Acad Sci U S A. 2011, 108: 6163-6168. 10.1073/pnas.1018221108.PubMedPubMedCentralCrossRef Yau S, Lauro FM, DeMaere MZ, Brown MV, Thomas T, Raftery MJ, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Gibson JA, Cavicchioli R: Virophage control of antarctic algal host-virus dynamics. Proc Natl Acad Sci U S A. 2011, 108: 6163-6168. 10.1073/pnas.1018221108.PubMedPubMedCentralCrossRef
15.
go back to reference Fischer MG, Suttle CA: A virophage at the origin of large DNA transposons. Science. 2011, 332: 231-234. 10.1126/science.1199412.PubMedCrossRef Fischer MG, Suttle CA: A virophage at the origin of large DNA transposons. Science. 2011, 332: 231-234. 10.1126/science.1199412.PubMedCrossRef
16.
17.
go back to reference Philippe N, Legendre M, Doutre G, Couté Y, Poirot O, Lescot M, Arslan D, Seltzer V, Bertaux L, Bruley C, Garin J, Claverie JM, Abergel C: Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science. 2013, 341: 281-286. 10.1126/science.1239181.PubMedCrossRef Philippe N, Legendre M, Doutre G, Couté Y, Poirot O, Lescot M, Arslan D, Seltzer V, Bertaux L, Bruley C, Garin J, Claverie JM, Abergel C: Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science. 2013, 341: 281-286. 10.1126/science.1239181.PubMedCrossRef
18.
go back to reference Xiao C, Kuznetsov YG, Sun S, Hafenstein SL, Kostyuchenko VA, Chipman PR, Suzan-Monti M, Raoult D, McPherson A, Rossmann MG: Structural studies of the giant mimivirus. PLoS Biol. 2009, 7: e92-10.1371/journal.pbio.1000092.PubMedCrossRef Xiao C, Kuznetsov YG, Sun S, Hafenstein SL, Kostyuchenko VA, Chipman PR, Suzan-Monti M, Raoult D, McPherson A, Rossmann MG: Structural studies of the giant mimivirus. PLoS Biol. 2009, 7: e92-10.1371/journal.pbio.1000092.PubMedCrossRef
19.
go back to reference Claverie JM, Abergel C: Mimivirus: the emerging paradox of quasi-autonomous viruses. Trends Genet. 2010, 26: 431-437. 10.1016/j.tig.2010.07.003.PubMedCrossRef Claverie JM, Abergel C: Mimivirus: the emerging paradox of quasi-autonomous viruses. Trends Genet. 2010, 26: 431-437. 10.1016/j.tig.2010.07.003.PubMedCrossRef
20.
go back to reference Boyer M, Azza S, Barrassi L, Klose T, Campocasso A, Pagnier I, Fournous G, Borg A, Robert C, Zhang X, Desnues C, Henrissat B, Rossmann MG, La Scola B, Raoult D: Mimivirus shows dramatic genome reduction after intraamoebal culture. Proc Natl Acad Sci U S A. 2011, 108: 10296-10301. 10.1073/pnas.1101118108.PubMedPubMedCentralCrossRef Boyer M, Azza S, Barrassi L, Klose T, Campocasso A, Pagnier I, Fournous G, Borg A, Robert C, Zhang X, Desnues C, Henrissat B, Rossmann MG, La Scola B, Raoult D: Mimivirus shows dramatic genome reduction after intraamoebal culture. Proc Natl Acad Sci U S A. 2011, 108: 10296-10301. 10.1073/pnas.1101118108.PubMedPubMedCentralCrossRef
21.
go back to reference Suzan-Monti M, La Scola B, Barrassi L, Espinosa L, Raoult D: Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS One. 2007, 2: e328-10.1371/journal.pone.0000328.PubMedPubMedCentralCrossRef Suzan-Monti M, La Scola B, Barrassi L, Espinosa L, Raoult D: Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS One. 2007, 2: e328-10.1371/journal.pone.0000328.PubMedPubMedCentralCrossRef
22.
go back to reference Krupovic M, Cvirkaite-Krupovic V: Virophages or satellite viruses?. Nat Rev Microbiol. 2011, 9: 762-763. 10.1038/nrmicro2676.PubMedCrossRef Krupovic M, Cvirkaite-Krupovic V: Virophages or satellite viruses?. Nat Rev Microbiol. 2011, 9: 762-763. 10.1038/nrmicro2676.PubMedCrossRef
23.
go back to reference Desnues C, Raoult D: Inside the lifestyle of the virophage. Intervirology. 2010, 53: 293-303. 10.1159/000312914.PubMedCrossRef Desnues C, Raoult D: Inside the lifestyle of the virophage. Intervirology. 2010, 53: 293-303. 10.1159/000312914.PubMedCrossRef
24.
go back to reference Claverie JM, Grzela R, Lartigue A, Bernadac A, Nitsche S, Vacelet J, Ogata H, Abergel C: Mimivirus and Mimiviridae: giant viruses with an increasing number of potential hosts, including corals and sponges. J Invertebr Pathol. 2009, 101: 172-180. 10.1016/j.jip.2009.03.011.PubMedCrossRef Claverie JM, Grzela R, Lartigue A, Bernadac A, Nitsche S, Vacelet J, Ogata H, Abergel C: Mimivirus and Mimiviridae: giant viruses with an increasing number of potential hosts, including corals and sponges. J Invertebr Pathol. 2009, 101: 172-180. 10.1016/j.jip.2009.03.011.PubMedCrossRef
25.
go back to reference Fischer MG, Allen MJ, Wilson WH, Suttle CA: Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci U S A. 2010, 107: 19508-19513. 10.1073/pnas.1007615107.PubMedPubMedCentralCrossRef Fischer MG, Allen MJ, Wilson WH, Suttle CA: Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci U S A. 2010, 107: 19508-19513. 10.1073/pnas.1007615107.PubMedPubMedCentralCrossRef
26.
go back to reference Desnues C, La Scola B, Yutin N, Fournous G, Robert C, Azza S, Jardot P, Monteil S, Campocasso A, Koonin EV, Raoult D: Provirophages and transpovirons as the diverse mobilome of giant viruses. Proc Natl Acad Sci U S A. 2012, 30: 18078-18083.CrossRef Desnues C, La Scola B, Yutin N, Fournous G, Robert C, Azza S, Jardot P, Monteil S, Campocasso A, Koonin EV, Raoult D: Provirophages and transpovirons as the diverse mobilome of giant viruses. Proc Natl Acad Sci U S A. 2012, 30: 18078-18083.CrossRef
27.
go back to reference Slimani M, Pagnier I, Raoult D, La Scola B: Amoebae as battlefields for bacteria, giant viruses, and virophages. J Virol. 2013, 87 (8): 4783-4785. 10.1128/JVI.02948-12.PubMedPubMedCentralCrossRef Slimani M, Pagnier I, Raoult D, La Scola B: Amoebae as battlefields for bacteria, giant viruses, and virophages. J Virol. 2013, 87 (8): 4783-4785. 10.1128/JVI.02948-12.PubMedPubMedCentralCrossRef
28.
go back to reference Reed LJ, Muench H: A simple method of estimating fifty percent endpoints. Am J Hyg. 1938, 27: 493-497. Reed LJ, Muench H: A simple method of estimating fifty percent endpoints. Am J Hyg. 1938, 27: 493-497.
Metadata
Title
Samba virus: a novel mimivirus from a giant rain forest, the Brazilian Amazon
Authors
Rafael K Campos
Paulo V Boratto
Felipe L Assis
Eric RGR Aguiar
Lorena CF Silva
Jonas D Albarnaz
Fabio P Dornas
Giliane S Trindade
Paulo P Ferreira
João T Marques
Catherine Robert
Didier Raoult
Erna G Kroon
Bernard La Scola
Jônatas S Abrahão
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2014
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-11-95

Other articles of this Issue 1/2014

Virology Journal 1/2014 Go to the issue