Skip to main content
Top
Published in: Virology Journal 1/2018

Open Access 01-12-2018 | Research

Ubiquitous giants: a plethora of giant viruses found in Brazil and Antarctica

Authors: Ana Cláudia dos S. P. Andrade, Thalita S. Arantes, Rodrigo A. L. Rodrigues, Talita B. Machado, Fábio P. Dornas, Melissa F. Landell, Cinthia Furst, Luiz G. A. Borges, Lara A. L. Dutra, Gabriel Almeida, Giliane de S. Trindade, Ivan Bergier, Walter Abrahão, Iara A. Borges, Juliana R. Cortines, Danilo B. de Oliveira, Erna G. Kroon, Jônatas S. Abrahão

Published in: Virology Journal | Issue 1/2018

Login to get access

Abstract

Background

Since the discovery of giant viruses infecting amoebae in 2003, many dogmas of virology have been revised and the search for these viruses has been intensified. Over the last few years, several new groups of these viruses have been discovered in various types of samples and environments.In this work, we describe the isolation of 68 giant viruses of amoeba obtained from environmental samples from Brazil and Antarctica.

Methods

Isolated viruses were identified by hemacolor staining, PCR assays and electron microscopy (scanning and/or transmission).

Results

A total of 64 viruses belonging to the Mimiviridae family were isolated (26 from lineage A, 13 from lineage B, 2 from lineage C and 23 from unidentified lineages) from different types of samples, including marine water from Antarctica, thus being the first mimiviruses isolated in this extreme environment to date. Furthermore, a marseillevirus was isolated from sewage samples along with two pandoraviruses and a cedratvirus (the third to be isolated in the world so far).

Conclusions

Considering the different type of samples, we found a higher number of viral groups in sewage samples. Our results reinforce the importance of prospective studies in different environmental samples, therefore improving our comprehension about the circulation anddiversity of these viruses in nature.
Appendix
Available only for authorised users
Literature
1.
go back to reference La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, et al. A giant virus in amoebae. Science. 2003;299:2033.CrossRefPubMed La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, et al. A giant virus in amoebae. Science. 2003;299:2033.CrossRefPubMed
2.
go back to reference Aherfi S, Colson P, La Scola B, Raoult D. Giant viruses of amoebas: an update. Front Microbiol. 2016;7:1–14.CrossRef Aherfi S, Colson P, La Scola B, Raoult D. Giant viruses of amoebas: an update. Front Microbiol. 2016;7:1–14.CrossRef
3.
go back to reference 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. 2009;106:21848–53.CrossRefPubMedPubMedCentral 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. 2009;106:21848–53.CrossRefPubMedPubMedCentral
4.
go back to reference Legendre M, Bartoli J, Shmakova L, Jeudy S, Labadie K, Adrait A, et al. Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc Natl Acad Sci. 2014;111:4274–9.CrossRefPubMedPubMedCentral Legendre M, Bartoli J, Shmakova L, Jeudy S, Labadie K, Adrait A, et al. Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc Natl Acad Sci. 2014;111:4274–9.CrossRefPubMedPubMedCentral
5.
go back to reference Abrahão JS, Araújo R, Colson P, La Scola B. The analysis of translation-related gene set boosts debates around origin and evolution of mimiviruses. PLoS Genet. 2017;16:1–12. Abrahão JS, Araújo R, Colson P, La Scola B. The analysis of translation-related gene set boosts debates around origin and evolution of mimiviruses. PLoS Genet. 2017;16:1–12.
6.
go back to reference Colson P, La Scola B, Levasseur A, Caetano-Anollés G, Raoult D. Mimivirus: leading the way in the discovery of giant viruses of amoebae. Nat Rev Microbiol. 2017;4:243–54.CrossRef Colson P, La Scola B, Levasseur A, Caetano-Anollés G, Raoult D. Mimivirus: leading the way in the discovery of giant viruses of amoebae. Nat Rev Microbiol. 2017;4:243–54.CrossRef
7.
go back to reference Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, et al. The 1.2-megabase genome sequence of mimivirus. Science. 2004;306:1344–50.CrossRefPubMed Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, et al. The 1.2-megabase genome sequence of mimivirus. Science. 2004;306:1344–50.CrossRefPubMed
9.
go back to reference Sharma V, Colson P, Pontarotti P, Raoult D. Mimivirus inaugurated in the 21st century the beginning of a reclassification of viruses. Curr Opin Microbiol. 2016;31:16–24.CrossRefPubMed Sharma V, Colson P, Pontarotti P, Raoult D. Mimivirus inaugurated in the 21st century the beginning of a reclassification of viruses. Curr Opin Microbiol. 2016;31:16–24.CrossRefPubMed
10.
go back to reference Sharma V, Colson P, Chabrol O, Scheid P, Pontarotti P, Raoult D. Welcome to pandoraviruses at the “Fourth TRUC” club. Front Microbiol. 2015;6:1–11. Sharma V, Colson P, Chabrol O, Scheid P, Pontarotti P, Raoult D. Welcome to pandoraviruses at the “Fourth TRUC” club. Front Microbiol. 2015;6:1–11.
11.
go back to reference Sharma V, Colson P, Chabrol O, Pontarotti P, Raoult D. Pithovirus sibericum, a new bona fide member of the “Fourth TRUC” club. Front Microbiol. 2015;6:1–9. Sharma V, Colson P, Chabrol O, Pontarotti P, Raoult D. Pithovirus sibericum, a new bona fide member of the “Fourth TRUC” club. Front Microbiol. 2015;6:1–9.
12.
go back to reference Benamar S, DGI R, Bandaly V, Labas N, Raoult D, La Scola B. Faustoviruses: comparative genomics of new megavirales family members. Front Microbiol. 2016;7:1–9.CrossRef Benamar S, DGI R, Bandaly V, Labas N, Raoult D, La Scola B. Faustoviruses: comparative genomics of new megavirales family members. Front Microbiol. 2016;7:1–9.CrossRef
13.
go back to reference Andreani J, Bou Khalil JY, Sevvana M, Benamar S, Di Pinto F, Bitam I, et al. Pacmanvirus, a new giant icosahedral virus at the crossroads between Asfarviridae and Faustoviruses. J Virol. 2017;91:212–7. Andreani J, Bou Khalil JY, Sevvana M, Benamar S, Di Pinto F, Bitam I, et al. Pacmanvirus, a new giant icosahedral virus at the crossroads between Asfarviridae and Faustoviruses. J Virol. 2017;91:212–7.
14.
go back to reference 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. 2015;112:5327–35.CrossRef 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. 2015;112:5327–35.CrossRef
15.
go back to reference Bajrai LH, Benamar S, Azhar EI, Robert C, Levasseur A, Raoult D, et al. Kaumoebavirus, a new virus that clusters with Faustoviruses and Asfarviridae. Viruses. 2016;8:1–10.CrossRef Bajrai LH, Benamar S, Azhar EI, Robert C, Levasseur A, Raoult D, et al. Kaumoebavirus, a new virus that clusters with Faustoviruses and Asfarviridae. Viruses. 2016;8:1–10.CrossRef
16.
go back to reference Andreani J, Aherfi S, JYB K, Di Pinto F, Bitam I, Raoult D, et al. Cedratvirus, a double-cork structured giant virus, is a distant relative of pithoviruses. Viruses. 2016;8:1–11.CrossRef Andreani J, Aherfi S, JYB K, Di Pinto F, Bitam I, Raoult D, et al. Cedratvirus, a double-cork structured giant virus, is a distant relative of pithoviruses. Viruses. 2016;8:1–11.CrossRef
17.
go back to reference Bertelli C, Mueller L, Thomas V, Pillonel T, Jacquier N, Greub G. Cedratvirus lausannensis - digging into Pithoviridae diversity. Environ Microbiol. 2017;10:4022–34.CrossRef Bertelli C, Mueller L, Thomas V, Pillonel T, Jacquier N, Greub G. Cedratvirus lausannensis - digging into Pithoviridae diversity. Environ Microbiol. 2017;10:4022–34.CrossRef
18.
go back to reference Dornas FP, JYB K, Pagnier I, Raoult D, Abrahão J, La Scola B. Isolation of new Brazilian giant viruses from environmental samples using a panel of protozoa. Front Microbiol. 2015;6:1–9.CrossRef Dornas FP, JYB K, Pagnier I, Raoult D, Abrahão J, La Scola B. Isolation of new Brazilian giant viruses from environmental samples using a panel of protozoa. Front Microbiol. 2015;6:1–9.CrossRef
19.
go back to reference La Scola B, Campocasso A, N’Dong R, Fournous G, Barrassi L, Flaudrops C, et al. Tentative characterization of new environmental giant viruses by MALDI-TOF mass spectrometry. Intervirology. 2010;53:344–53.CrossRefPubMed La Scola B, Campocasso A, N’Dong R, Fournous G, Barrassi L, Flaudrops C, et al. Tentative characterization of new environmental giant viruses by MALDI-TOF mass spectrometry. Intervirology. 2010;53:344–53.CrossRefPubMed
20.
go back to reference Ghedin E, Claverie J-MM. Mimivirus relatives in the Sargasso sea. Virol J. 2005;2:1–62.CrossRef Ghedin E, Claverie J-MM. Mimivirus relatives in the Sargasso sea. Virol J. 2005;2:1–62.CrossRef
21.
go back to reference Zhang W, Zhou J, Liu T, Yu Y, Pan Y, Yan S, et al. Four novel algal virus genomes discovered from Yellowstone Lake metagenomes. Sci Rep. 2015;5:1–13. Zhang W, Zhou J, Liu T, Yu Y, Pan Y, Yan S, et al. Four novel algal virus genomes discovered from Yellowstone Lake metagenomes. Sci Rep. 2015;5:1–13.
22.
go back to reference Kerepesi C, Grolmusz V. The “Giant Virus Finder” discovers an abundance of giant viruses in the Antarctic dry valleys. Arch Virol. 2017;162:1–6.CrossRef Kerepesi C, Grolmusz V. The “Giant Virus Finder” discovers an abundance of giant viruses in the Antarctic dry valleys. Arch Virol. 2017;162:1–6.CrossRef
23.
go back to reference Boughalmi M, Pagnier I, Aherfi S, Colson P, Raoult D, La Scola B. First isolation of a marseillevirus in the diptera syrphidae eristalis tenax. Intervirology. 2013;56:386–94.CrossRefPubMed Boughalmi M, Pagnier I, Aherfi S, Colson P, Raoult D, La Scola B. First isolation of a marseillevirus in the diptera syrphidae eristalis tenax. Intervirology. 2013;56:386–94.CrossRefPubMed
24.
go back to reference Popgeorgiev N, Colson P, Thuret I, Chiarioni J, Gallian P, Raoult D, et al. Marseillevirus prevalence in multitransfused patients suggests blood transmission. J Clin Virol. 2013;58:722–5.CrossRefPubMed Popgeorgiev N, Colson P, Thuret I, Chiarioni J, Gallian P, Raoult D, et al. Marseillevirus prevalence in multitransfused patients suggests blood transmission. J Clin Virol. 2013;58:722–5.CrossRefPubMed
25.
go back to reference Saadi H, DGI R, Colson P, Aherfi S, Minodier P, Pagnier I, et al. Shan virus: a new mimivirus isolated from the stool of a tunisian patient with pneumonia. Intervirology. 2013;56:424–9.CrossRefPubMed Saadi H, DGI R, Colson P, Aherfi S, Minodier P, Pagnier I, et al. Shan virus: a new mimivirus isolated from the stool of a tunisian patient with pneumonia. Intervirology. 2013;56:424–9.CrossRefPubMed
26.
go back to reference Dornas FP, Rodrigues FP, PVM B, LCF S, PCP F, Bonjardim CA, et al. Mimivirus circulation among wild and domestic mammals, Amazon Region, Brazil. Emerg Infect Dis. 2014;20:469–72.CrossRefPubMedPubMedCentral Dornas FP, Rodrigues FP, PVM B, LCF S, PCP F, Bonjardim CA, et al. Mimivirus circulation among wild and domestic mammals, Amazon Region, Brazil. Emerg Infect Dis. 2014;20:469–72.CrossRefPubMedPubMedCentral
27.
go back to reference Reteno DG, Benamar S, Khalil JB, Andreani J, Armstrong N, Klose T, et al. Faustovirus, an Asfarvirus-related new lineage of giant viruses infecting amoebae. J Virol. 2015;89:6585–94.CrossRefPubMedPubMedCentral Reteno DG, Benamar S, Khalil JB, Andreani J, Armstrong N, Klose T, et al. Faustovirus, an Asfarvirus-related new lineage of giant viruses infecting amoebae. J Virol. 2015;89:6585–94.CrossRefPubMedPubMedCentral
28.
go back to reference Colson P, Aherfi S, La Scola B, Raoult D. The role of giant viruses of amoebas in humans. Curr Opin Microbiol. 2016;31:199–208.CrossRefPubMed Colson P, Aherfi S, La Scola B, Raoult D. The role of giant viruses of amoebas in humans. Curr Opin Microbiol. 2016;31:199–208.CrossRefPubMed
30.
go back to reference Aherfi S, Colson P, Audoly G, Nappez C, Xerri L, Valensi A, et al. Marseillevirus in lymphoma: a giant in the lymph node. Lancet Infect Dis. 2016;1:225–34.CrossRef Aherfi S, Colson P, Audoly G, Nappez C, Xerri L, Valensi A, et al. Marseillevirus in lymphoma: a giant in the lymph node. Lancet Infect Dis. 2016;1:225–34.CrossRef
31.
32.
go back to reference Sambrook J, Russell DW. Molecular Cloning-Sambrook & Russel. 3rd ed. New York: Cold Spring Harbor Laboratory Press; 2001. Sambrook J, Russell DW. Molecular Cloning-Sambrook & Russel. 3rd ed. New York: Cold Spring Harbor Laboratory Press; 2001.
33.
go back to reference Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Hyg. 1938;27:493–7. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Hyg. 1938;27:493–7.
34.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
35.
go back to reference Andrade KR, Boratto PPVM, Rodrigues FP, LCF S, Dornas FP, Pilotto MR, et al. Oysters as hot spots for mimivirus isolation. Arch Virol. 2014;160:477–82.CrossRefPubMed Andrade KR, Boratto PPVM, Rodrigues FP, LCF S, Dornas FP, Pilotto MR, et al. Oysters as hot spots for mimivirus isolation. Arch Virol. 2014;160:477–82.CrossRefPubMed
36.
go back to reference 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;7:3483–99.CrossRefPubMedPubMedCentral 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;7:3483–99.CrossRefPubMedPubMedCentral
37.
go back to reference dos Santos RN, Campos FS, Medeiros de Albuquerque NR, Finoketti F, Côrrea RA, Cano-Ortiz L, et al. A new marseillevirus isolated in Southern Brazil from Limnoperna fortunei. Sci Rep. 2016;6:35237.CrossRefPubMedPubMedCentral dos Santos RN, Campos FS, Medeiros de Albuquerque NR, Finoketti F, Côrrea RA, Cano-Ortiz L, et al. A new marseillevirus isolated in Southern Brazil from Limnoperna fortunei. Sci Rep. 2016;6:35237.CrossRefPubMedPubMedCentral
38.
go back to reference Dornas FP, Assis FL, Aherfi S, Arantes T, Abrahão JS, Colson P, et al. A Brazilian marseillevirus is the founding member of a lineage in family marseilleviridae. Viruses. 2016;8:76.CrossRefPubMedPubMedCentral Dornas FP, Assis FL, Aherfi S, Arantes T, Abrahão JS, Colson P, et al. A Brazilian marseillevirus is the founding member of a lineage in family marseilleviridae. Viruses. 2016;8:76.CrossRefPubMedPubMedCentral
39.
go back to reference PVM B, Arantes TS, LCF S, 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;6:1–11. PVM B, Arantes TS, LCF S, 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;6:1–11.
40.
go back to reference Antwerpen MH, Georgi E, Zoeller L, Woelfel R, Stoecker K, Scheid P. Whole-genome sequencing of a pandoravirus isolated from keratitis-inducing acanthamoeba. Genome Announc. 2015;3:1–2.CrossRef Antwerpen MH, Georgi E, Zoeller L, Woelfel R, Stoecker K, Scheid P. Whole-genome sequencing of a pandoravirus isolated from keratitis-inducing acanthamoeba. Genome Announc. 2015;3:1–2.CrossRef
41.
go back to reference Philippe N, Legendre M, Doutre G, Coute Y, Poirot O, Lescot M, et al. Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science. 2013;341:281–6.CrossRefPubMed Philippe N, Legendre M, Doutre G, Coute Y, Poirot O, Lescot M, et al. Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science. 2013;341:281–6.CrossRefPubMed
42.
43.
go back to reference Dutra LAL, de Freitas Almeida GM, Oliveira GP, Abrahão JS, Kroon EG, de Trindade GS. Molecular evidence of Orthopoxvirus DNA in capybara (Hydrochoerus hydrochaeris) stool samples. Arch Virol. 2017;162:439–48.CrossRefPubMed Dutra LAL, de Freitas Almeida GM, Oliveira GP, Abrahão JS, Kroon EG, de Trindade GS. Molecular evidence of Orthopoxvirus DNA in capybara (Hydrochoerus hydrochaeris) stool samples. Arch Virol. 2017;162:439–48.CrossRefPubMed
44.
go back to reference JYB K, Robert S, Reteno DG, Andreani J, Raoult D, La Scola B. High-throughput isolation of giant viruses in liquid medium using automated flow cytometry and fluorescence staining. Front Microbiol. 2016;7:1–9. JYB K, Robert S, Reteno DG, Andreani J, Raoult D, La Scola B. High-throughput isolation of giant viruses in liquid medium using automated flow cytometry and fluorescence staining. Front Microbiol. 2016;7:1–9.
46.
go back to reference Saadi H, Pagnier I, Colson P, Cherif JK, Beji M, Boughalmi M, et al. First isolation of Mimivirus in a patient with pneumonia. Clin Infect Dis. 2013;57:127–34.CrossRef Saadi H, Pagnier I, Colson P, Cherif JK, Beji M, Boughalmi M, et al. First isolation of Mimivirus in a patient with pneumonia. Clin Infect Dis. 2013;57:127–34.CrossRef
47.
48.
go back to reference 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. 2013;110:10800–5.CrossRefPubMedPubMedCentral 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. 2013;110:10800–5.CrossRefPubMedPubMedCentral
49.
go back to reference Yau S, Lauro FM, MZ DM, Brown MV, Thomas T, Raftery MJ, et al. Virophage control of antarctic algal host-virus dynamics. Proc Natl Acad Sci. 2011;108:6163–8.CrossRefPubMedPubMedCentral Yau S, Lauro FM, MZ DM, Brown MV, Thomas T, Raftery MJ, et al. Virophage control of antarctic algal host-virus dynamics. Proc Natl Acad Sci. 2011;108:6163–8.CrossRefPubMedPubMedCentral
Metadata
Title
Ubiquitous giants: a plethora of giant viruses found in Brazil and Antarctica
Authors
Ana Cláudia dos S. P. Andrade
Thalita S. Arantes
Rodrigo A. L. Rodrigues
Talita B. Machado
Fábio P. Dornas
Melissa F. Landell
Cinthia Furst
Luiz G. A. Borges
Lara A. L. Dutra
Gabriel Almeida
Giliane de S. Trindade
Ivan Bergier
Walter Abrahão
Iara A. Borges
Juliana R. Cortines
Danilo B. de Oliveira
Erna G. Kroon
Jônatas S. Abrahão
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2018
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-018-0930-x

Other articles of this Issue 1/2018

Virology Journal 1/2018 Go to the issue