Zamilon, a Novel Virophage with Mimiviridae Host Specificity

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2014 Apr 22

PMID 24747414

Citations 61

Authors

Morgan Gaia

Samia Benamar

Mondher Boughalmi

Isabelle Pagnier

Olivier Croce

Philippe Colson

Didier Raoult

Bernard La Scola

Affiliations

Soon will be listed here.

Abstract

Virophages, which are potentially important ecological regulators, have been discovered in association with members of the order Megavirales. Sputnik virophages target the Mimiviridae, Mavirus was identified with the Cafeteria roenbergensis virus, and virophage genomes reconstructed by metagenomic analyses may be associated with the Phycodnaviridae. Despite the fact that the Sputnik virophages were isolated with viruses belonging to group A of the Mimiviridae, they can grow in amoebae infected by Mimiviridae from groups A, B or C. In this study we describe Zamilon, the first virophage isolated with a member of group C of the Mimiviridae family. By co-culturing amoebae with purified Zamilon, we found that the virophage is able to multiply with members of groups B and C of the Mimiviridae family but not with viruses from group A. Zamilon has a 17,276 bp DNA genome that potentially encodes 20 genes. Most of these genes are closely related to genes from the Sputnik virophage, yet two are more related to Megavirus chiliensis genes, a group B Mimiviridae, and one to Moumouvirus monve transpoviron.

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References

Wodarz D . Evolutionary dynamics of giant viruses and their virophages. Ecol Evol. 2013; 3(7):2103-15. PMC: 3728950. DOI: 10.1002/ece3.600. View

Pagnier I, Reteno D, Saadi H, Boughalmi M, Gaia M, Slimani M . A decade of improvements in Mimiviridae and Marseilleviridae isolation from amoeba. Intervirology. 2013; 56(6):354-63. DOI: 10.1159/000354556. View

Hyman P, Abedon S . Bacteriophage host range and bacterial resistance. Adv Appl Microbiol. 2010; 70:217-48. DOI: 10.1016/S0065-2164(10)70007-1. View

Koskella B, Meaden S . Understanding bacteriophage specificity in natural microbial communities. Viruses. 2013; 5(3):806-23. PMC: 3705297. DOI: 10.3390/v5030806. View

Zhang X, Sun S, Xiang Y, Wong J, Klose T, Raoult D . Structure of Sputnik, a virophage, at 3.5-Å resolution. Proc Natl Acad Sci U S A. 2012; 109(45):18431-6. PMC: 3494952. DOI: 10.1073/pnas.1211702109. View

Hyatt D, Chen G, LoCascio P, Land M, Larimer F, Hauser L . Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010; 11:119. PMC: 2848648. DOI: 10.1186/1471-2105-11-119. View

Iyer L, Aravind L, Koonin E . Common origin of four diverse families of large eukaryotic DNA viruses. J Virol. 2001; 75(23):11720-34. PMC: 114758. DOI: 10.1128/JVI.75.23.11720-11734.2001. View

Jassim S, Limoges R . Impact of external forces on cyanophage-host interactions in aquatic ecosystems. World J Microbiol Biotechnol. 2013; 29(10):1751-62. DOI: 10.1007/s11274-013-1358-5. View

Riede I, Degen M, Henning U . The receptor specificity of bacteriophages can be determined by a tail fiber modifying protein. EMBO J. 1985; 4(9):2343-6. PMC: 554507. DOI: 10.1002/j.1460-2075.1985.tb03936.x. View

10.

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(42):17486-91. PMC: 3198346. DOI: 10.1073/pnas.1110889108. View

11.

Guindon S, Delsuc F, Dufayard J, Gascuel O . Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol. 2009; 537:113-37. DOI: 10.1007/978-1-59745-251-9_6. View

12.

Yoosuf N, Yutin N, Colson P, Shabalina S, Pagnier I, Robert C . 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. 2012; 4(12):1324-30. PMC: 3542560. DOI: 10.1093/gbe/evs109. View

13.

Talavera G, Castresana J . Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007; 56(4):564-77. DOI: 10.1080/10635150701472164. View

14.

Gaia M, Pagnier I, Campocasso A, Fournous G, Raoult D, La Scola B . Broad spectrum of mimiviridae virophage allows its isolation using a mimivirus reporter. PLoS One. 2013; 8(4):e61912. PMC: 3626643. DOI: 10.1371/journal.pone.0061912. View

15.

Sun S, La Scola B, Bowman V, Ryan C, Whitelegge J, Raoult D . Structural studies of the Sputnik virophage. J Virol. 2009; 84(2):894-7. PMC: 2798384. DOI: 10.1128/JVI.01957-09. View

16.

Besemer J, Lomsadze A, Borodovsky M . GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res. 2001; 29(12):2607-18. PMC: 55746. DOI: 10.1093/nar/29.12.2607. View

17.

Duffy S, Burch C, Turner P . Evolution of host specificity drives reproductive isolation among RNA viruses. Evolution. 2007; 61(11):2614-22. PMC: 7202233. DOI: 10.1111/j.1558-5646.2007.00226.x. View

18.

Kurtz S, Phillippy A, Delcher A, Smoot M, Shumway M, Antonescu C . Versatile and open software for comparing large genomes. Genome Biol. 2004; 5(2):R12. PMC: 395750. DOI: 10.1186/gb-2004-5-2-r12. View

19.

Scanlan P, Hall A, Lopez-Pascua L, Buckling A . Genetic basis of infectivity evolution in a bacteriophage. Mol Ecol. 2010; 20(5):981-9. DOI: 10.1111/j.1365-294X.2010.04903.x. View

20.

Colson P, de Lamballerie X, Fournous G, Raoult D . Reclassification of giant viruses composing a fourth domain of life in the new order Megavirales. Intervirology. 2012; 55(5):321-32. DOI: 10.1159/000336562. View