Contrasting diversity of phycodnavirus signature genes in two large and deep western European lakes

Environmental Microbiology

Volumn 16, Issue 3, 2014, Pages 759-773

  Zhong, Xu ^a   Jacquet, Stéphan ^a  

^a UMR CARRTEL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; DNA DIRECTED DNA POLYMERASE;

ARTICLE; BIODIVERSITY; CLASSIFICATION; ECOSYSTEM; FRANCE; GENETIC VARIABILITY; GENETICS; LAKE; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYCODNAVIRIDAE; PHYLOGENY; VIROLOGY;

BIODIVERSITY; CAPSID PROTEINS; DNA-DIRECTED DNA POLYMERASE; ECOSYSTEM; FRANCE; GENETIC VARIATION; LAKES; MOLECULAR SEQUENCE DATA; PHYCODNAVIRIDAE; PHYLOGENY;

EID: 84894747774     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12201     Document Type: Article

References (63)

1. Angly, F.E., Felts, B., Breitbart, M., Salamon, P., Edwards, R.A., Carlson, C., etal. (2006) The marine viromes of four oceanic regions. PLoS Biol 4: 2121e2131.
2. Bratbak, G., Egge, J.K., and Heldal, M. (1993) Viral mortality of the marine alga Emiliana huxleyi (Haptophyceae) and termination of algal blooms. Mar Ecol Prog Ser 93: 39-48.
3. Bellec, L., Grimsley, N., Moreau, H., and Desdevises, Y. (2009) Phylogenetic analysis of new prasinoviruses (phycodnaviridae) that infect the green unicellular algae Ostreococcus, Bathycoccus and Micromonas. Environ Microbiol Rep 1: 114-119.
4. Bench, S.R., Hanson, T.E., Williamson, K.E., Ghosh, D., Radosovich, M., Wang, K., etal. (2007) Metagenomic characterization of Chesapeake Bay virioplankton. Appl Environ Microbiol 73: 7629-7641.
5. Berdjeb, L., Ghiglione, J.-F., and Jacquet, S. (2011) Bottom-up vs. top-down factors regulating the bacterial community structure in two peri-alpine lakes. Appl Environ Microbiol 77: 3591-3599.
6. Brussaard, C.P.D. (2004) Viral control of phytoplankton populations - a review. J Eukaryot Microbiol 51: 125-138.
7. Brussaard, C.P.D., Wilhelm, S.W., Thingstad, F., Weinbauer, M.G., Bratbak, G., Heldal, M., etal. (2008) Global-scale processes with a nanoscale drive: the role of marine viruses. ISME J 2: 575-578.
8. Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
9. Chen, F., and Suttle, C.A. (1995) Amplification of DNA polymerase gene fragments from viruses infecting microalgae. Appl Environ Microbiol 61: 1274-1278.
10. Chen, F., Suttle, C.A., and Short, S.M. (1996) Genetic diversity in marine algal virus communities as revealed by sequence analysis of DNA polymerase genes. Appl Environ Microbiol 62: 2869-2874.
11. Clasen, J.L., and Suttle, C.A. (2009) Identification of freshwater Phycodnaviridae and their potential phytoplankton hosts, using DNA pol sequence fragments and a genetic-distance analysis. Appl Environ Microbiol 75: 991-997.
12. Danovaro, R., Dell'Anno, A., Corinaldesi, C., Magagnini, M., Noble, R., Tamburini, C., etal. (2008) Major viral impact on the functioning of benthic deep-sea ecosystems. Nature 454: 1084-1087.
13. Derelle, E., Ferraz, C., Escande, M.L., Eychenié, S., Cooke, R., Piganeau, G., etal. (2008) Life-cycle and genome of OtV5, a large DNA virus of the pelagic marine unicellular green alga Ostreococcus tauri. PLoS ONE 3: e2250.
14. Dimmic, M.W., Rest, J.S., Mindell, D.P., and Goldstein, R.A. (2002) rtREV: an amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. J Mol Evol 55: 65-73.
15. Domaizon, I., Lainé, L., Lazzarotto, J., Perga, M.E., and Rimet, F. (2012) Suivi de la qualité des eaux du lac d'Annecy 2011. Rapport SILA-INRA, 92 pp.
16. Dunigan, D.D., Fitzgerald, L.A., and Van Etten, J.L. (2006) Phycodnaviruses: a peek at genetic diversity. Vir Res 117: 119-132.
17. Gimenes, M.V., Zanotto, P.M., Suttle, C.A., Da Cunha, H.B., and Mehnert, D.U. (2012) Phylodynamics and movement of phycodnaviruses among aquatic environments. ISME J 6: 237-247.
18. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
19. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
20. Iyer, L.M., Balaji, S., Koonin, E.V., and Aravind, L. (2006) Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Vir Res 117: 156-184.
21. Jacquet, S., Heldal, M., Iglesias-Rodriguez, D., Larsen, A., Wilson, W.H., and Bratbak, G. (2002) Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aquat Microb Ecol 27: 111-124.
22. Jacquet, S., Barbet, D., Cachera, S., Caudron, A., Colon, M., Girel, C., etal. (2012) Suivi environnemental des eaux du lac du Bourget pour l'année 2011. Rapport INRA-CISALB, 220 pp.
23. Jacquet, S., Domaizon, I., and Anneville, O. (in press) Long-term trend of physico-chemical and biological indicators of water-quality and functioning of large peri-alpine lakes (Lakes Geneva, Annecy and Bourget): a comparative study of ecosystem trajectories during re-oligotrophication. Arch Sci 65: 225-242.
24. Katoh, K., Misawa, K., Kuma, K., and Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.
25. Larsen, A., Fonnes Flaten, G.A., Sandaa, R.A., Castberg, T., Thyrhaug, R., Erga, S.R., etal. (2004) Spring phytoplankton bloom dynamics in Norwegian coastal waters: microbial community succession and diversity. Limnol Oceanogr 49: 180-190.
26. Larsen, J.B., Larsen, A., Bratbak, G., and Sandaa, R.A. (2008) Phylogenetic analysis of members of the Phycodnaviridae virus family, using amplified fragments of the major capsid protein gene. Appl Environ Microbiol 74: 3048-3057.
27. Lauro, F.M., DeMaere, M.Z., Yau, S., Brown, M.V., Ng, C., Wilkins, D., etal. (2011) An integrative study of a meromictic lake ecosystem in Antarctica. ISME J 5: 879-895.
28. Lepère, C., Masquelier, S., Mangot, J.F., Debroas, D., and Domaizon, I. (2010) Vertical structure of small eukaryotes in three lakes that differ by their trophic status: a quantitative approach. ISME J 4: 1509-1519.
29. Logares, R., Bråte, J., Bertilsson, S., Clasen, J.L., Shalchian-Tabrizi, K., and Rengefors, K. (2009) Infrequent marine - freshwater transitions in the microbial world. Trends Microbiol 17: 414-422.
30. Lozupone, C., and Knight, R. (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235.
31. Lozupone, C.A., Hamady, M., Kelley, S.T., and Knight, R. (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73: 1576-1585.
32. Mangot, J.F., Lepère, C., Bouvier, C., Debroas, D., and Domaizon, I. (2009) Community structure and dynamics of small eukaryotes targeted by new oligonucleotide probes: new insight into the lacustrine microbial food web. Appl Environ Microbiol 75: 6373-6381.
33. Mangot, J.F., Domaizon, I., Taib, N., Marouni, N., Duffaud, E., Bronner, G., etal. (2013) Short-term dynamics of diversity patterns: evidence of continual reassembly within lacustrine small eukaryotes. Environ Microbiol 15: 1745-1758.
34. Monier, A., Larsen, J.B., Sandaa, R.A., Bratbak, G., Claverie, J.M., and Ogata, H. (2008) Marine mimivirus relatives are probably large algal viruses. Virol J 5: 12.
35. Moreau, H., Piganeau, G., Desdevises, Y., Cooke, R., Derelle, E., and Grimsley, N. (2010) Marine prasinovirus genomes show low evolutionary divergence and acquisition of protein metabolism genes by horizontal gene transfer. J Virol 84: 12555-12563.
36. Nagasaki, K. (2008) Dinoflagellates, diatoms, and their viruses. J Microbiol 46: 235-243.
37. Park, Y., Lee, K., Lee, Y.S., Kim, S.W., and Choi, T.J. (2011) Detection of diverse marine algal viruses in the South Sea regions of Korea by PCR amplification of the DNA polymerase and major capsid protein genes. Virus Res 159: 43-50.
38. Personnic, S., Domaizon, I., Dorigo, U., Berdjeb, L., and Jacquet, S. (2009) Seasonal and spatial variability of virio, bacterio- and picophytoplanktonic abundances in three peri-alpine lakes. Hydrobiologia 627: 99-111.
39. Ronquist, F., Teslenko, M., Van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., etal. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61: 539-542.
40. Roux, S., Enault, F., Robin, A., Ravet, V., Personnic, S., Theil, S., etal. (2012) Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS ONE 7: e33641.
41. Rusch, D.B., Halpern, A.L., Sutton, G., Heidelberg, K.B., Williamson, S., Yooseph, S., etal. (2007) The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5: e77.
42. Sandaa, R.A., Heldal, M., Castberg, T., Thyrhaug, R., and Bratbak, G. (2001) Isolation and characterization of two viruses with large genome size infecting Chrysochromulina ericina (Prymnesiophyceae) and Pyramimonas orientalis (Prasinophyceae). Virology 290: 272-280.
43. Schroeder, D.C., Oke, J., Hall, M., Malin, G., and Wilson, W.H. (2003) Virus succession observed during an Emiliana huxleyi bloom. Appl Environ Microbiol 69: 2484-2490.
44. Seshadri, R., Kravitz, S.A., Smarr, L., Gilna, P., and Frazier, M. (2007) CAMERA: a community resource for metagenomics. PLoS Biol 5: e75.
45. Short, C.M., Rusanova, O., and Short, S.M. (2011) Quantification of virus genes provides evidence for seed-bank populations of phycodnaviruses in Lake Ontario Canada. ISME J 5: 810-821.
46. Short, S.M. (2012) The ecology of viruses that infect eukaryotic algae. Environ Microbiol 14: 2253-2271.
47. Short, S.M., and Short, C.M. (2008) Diversity of algal viruses in various North American freshwater environments. Aquat Microb Ecol 51: 13-21.
48. Short, S.M., and Suttle, C.A. (2002) Sequence analysis of marine virus communities reveals that groups of related algal viruses are widely distributed in nature. Appl Environ Microbiol 68: 1290-1296.
49. Short, S.M., and Suttle, C.A. (2003) Temporal dynamics of natural communities of marine algal viruses and eukaryotes. Aquat Microb Ecol 32: 107-119.
50. Snyder, J.C., Wiedenheft, B., Lavin, M., Roberto, F.F., Spuhler, J., Ortmann, A.C., etal. (2007) Virus movement maintains local virus population diversity. Proc Natl Acad Sci USA 104: 19102-19107.
51. Suttle, C.A. (2005) Viruses in the sea. Nature 437: 356-361.
52. Taib, N., Mangot, J.-F., Domaizon, I., Bronner, G., and Debroas, D. (2013) Phylogenetic affiliation of SSU rRNA genes generated by massively parallel sequencing: new insights in the freshwater protist diversity. PLoS ONE 8: e58950.
53. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
54. Thomas, R., Jacquet, S., Grimsley, N., and Moreau, H. (2012) Strategies and mechanisms of resistance to virues in photosynthetic aquatic microorganisms. Adv Limnol Oceanogr 3: 1-15.
55. Tomaru, Y., Shirai, Y., and Nagasaki, K. (2008) Ecology, physiology and genetics of a phycoDNAvirus infecting the noxious bloom-forming raphidophyte Heterosigma akashiwo. Fish Sci 74: 701-711.
56. Van Etten, J.L., and Meints, R.H. (1999) Giant viruses infecting algae. Annu Rev Microbiol 53: 447-494.
57. Van Etten, J.L., Graves, M.V., Muller, D.G., Boland, W., and Delaroque, N. (2002) Phycodnaviridae - large DNA algal viruses. Arch Virol 147: 1479-1516.
58. Van Etten, J.L., Lane, L.C., and Dunigan, D.D. (2010) DNA viruses: the really big ones (giruses). Annu Rev Microbiol 64: 83-99.
59. Vaulot, D., Eikrem, W., Viprey, M., and Moreau, H. (2008) The diversity of small eukaryotic phytoplankton (≤3 μm) in marine ecosystems. FEMS Microbiol Rev 32: 795-820.
60. Weinbauer, M.G. (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28: 127-181.
61. Williamson, S.J., Rusch, D.B., Yooseph, S., Halpern, A.L., Heidelberg, K.B., Glass, J.I., etal. (2008) The Sorcerer II Global Ocean Sampling Expedition: metagenomic characterization of viruses within aquatic microbial samples. PLoS ONE 3: e1456.
62. Wilson, W.H., Schroeder, D.C., Ho, J., and Canty, M. (2006) Phylogenetic analysis of PgV-102P, a new virus from the English Channel that infects Phaeocystis globosa. J Mar Biolog Assoc UK 86: 485-490.
63. Wilson, W.H., Van Etten, J.L., and Allen, M.J. (2009) The Phycodnaviridae: the story of how tiny giants rule the world. Curr Top Microbiol Immunol 328: 1-42.