Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein

ISME Journal

Volumn 8, Issue 10, 2014, Pages 2093-2103

  Hopkins, Max ^a   Kailasan, Shweta ^b   Cohen, Allison ^a   Roux, Simon ^c,d   Tucker, Kimberly Pause ^e   Shevenell, Amelia ^a   Agbandje Mckenna, Mavis ^b   Breitbart, Mya ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

^d UNIVERSITÉ BLAISE PASCAL   (France)

^e STEVENSON UNIVERSITY   (United States)

Author keywords

gokushovirus; Microviridae; phage; single stranded; virus

Indexed keywords

DNA; ENVIRONMENTAL FACTOR; PHYLOGENETICS; POLYMERASE CHAIN REACTION; PROTEIN; VIRUS;

FLORIDA [UNITED STATES]; UNITED STATES;

CHLAMYDIA; MICROVIRIDAE; MIRIDAE;

CAPSID PROTEIN; SINGLE STRANDED DNA; VIRUS DNA;

BIODIVERSITY; CHEMISTRY; CLASSIFICATION; GENETICS; MICROBIOLOGY; MICROVIRIDAE; PHYLOGENY; POLYMERASE CHAIN REACTION;

BIODIVERSITY; CAPSID PROTEINS; DNA, SINGLE-STRANDED; DNA, VIRAL; ENVIRONMENTAL MICROBIOLOGY; MICROVIRIDAE; PHYLOGENY; POLYMERASE CHAIN REACTION;

EID: 84904894989     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.43     Document Type: Article

References (60)

1. Ackermann HW. (2007 ). 5500 phages examined in the electron microscope. Arch Virol 152: 227-243.
2. Agbandje-McKenna M, Kleinschmidt J. (2011). AAV capsid structure and cell interactions. In: Snyder R, Moullier P (eds) Met hods in Molecular Biology: Adeno-Associated Virus; Methods and Protocols. Springer: New York, USA, pp 47-92.
3. Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C et al. (2006). The marine viromes of four oceanic regions. PLoS Biol 4: e368.
4. Anisimova M, Gascuel O. (2006). Approximate likelihoodratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55: 539-552.
5. Bahadur RP, Janin J. (2008). Residue conservation in viral capsid assembly. Proteins 71: 407-414.
6. Breitbart M. (2012). Marine viruses: truth or dare. Ann Rev Mar Sci 4: 425-448.
7. Breitbart M, Miyake JH, Rohwer F. (2004). Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol Lett 236: 249-256.
8. Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D et al. (2002). Genomic analysis of uncultured marine viral communities. PNAS 99: 14250-14255.
9. Brentlinger KL, Hafenstein S, Novak CR, Fane BA, Borgon R, McKenna R et al. (2002). Microviridae, a family divided: isolation, characterization, and genome sequence of jMH2K, a bacteriophage of the obligate intracellular parasitic bacterium Bdellovibrio bacteriovorus. J Bacterio l 184: 1089-1094.
10. Brum JR, Schenck RO, Sullivan MB. (2013). Global morphological analysis of marine viruses shows minimal regional variation and dominance of nontailed viruses. ISME J 7: 1738-1751.
11. Bull J, Badgett M, Wichman H. (2000). Big-benefit mutations in a bacteriophage inhibited with heat. Mol Biol Evol 17: 942-950.
12. Carrillo-Tripp M, Shepherd CM, Borelli IA, Venkatara man S, Lander G, Natarajan P et al. (2009). VIPERdb2: an enhanced and web API enabled relational database for structural virology. Nucleic Acids Res 37: D436-D442.
13. Cherwa JE, Fane BA. (2011). Microviridae: Microviruses and Gokushoviruses. eLS; e-pub ahead of print 16 May 2011; doi:10.1002/9780470015902.a0000781.pub2.
14. Chipman PR, Agbandje-McKenna M, Renaudin J, Baker TS, McKenna R. (1998). Structural analysis of the spiroplasma virus, SpV4: implications for evolutionary variation to obtain host diversity among the Microviridae. Structure 6: 135-145.
15. Clarke IN, Cutcliffe LT , Everson JS, Garner SA, Lambden PR, Pead PJ et al. (2004). Chlamydiaphage Chp2, a skeleton in the jX174 closet: scaffolding protein and procapsid identification. J Bacteriol 186: 7571-7574.
16. Cul ley AI, Steward GF. (2007). New genera of RNA viruses in subtropical seawater, inferred from polymerase gene sequences. Appl Environ Microbiol 73: 5937-5944.
17. Desnues C, Rodriguez-Brito B, Rayhawk S, Kelley S, Tran T, Haynes M et al. (2008). Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature 452: 340-343.
18. Dokland T,McKenna R, Ilag LL, Bowman BR, Incardona NL, Fane BA et al. (1997). Structure of a viral procapsid with molecular scaffolding. Nature 389: 308-313.
19. Dwivedi B, Schmieder R, Goldsmith DB, Edwards RA, Breitbart M. (2012). PhiSiGns: an online tool to identify signature genes in phages and design PCR primers for examining phage diversity. BMC Bioinformatics 13: 37.
20. Eddy SR. 2008 A probabilistic model of local sequence alignment that simplifies statistical significance estimation. PLoS Comp Biol 4 e1000069.
21. Emsley P, Lohkamp B, Scott WG, Cowtan K. (2010). Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
22. Everson J, Garner S, Lambden P, Fane B, Clarke I. (2003). Host range of chlamydiaphages FCPAR39 and Chp3. J Bacteriol 185: 6490-6492.
23. Fane B. (2005). Family microviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds). Virus Taxonomy, Classification and Nomenclature of Viruses, 8th ICTV Report of the International Committee on Taxonomy of V iruses. Elsevier/Academic Press: San Diego, USA.
24. FileéJ, Tétart F, Suttle CA, Krisch H. (2005). Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. PNAS 102: 12471-12476.
25. Garcia-Boronat M, Diez-Rivero CM, Reinherz EL, Reche PA. (2008). PVS: a web server for protein sequence variability analysis tuned to facilitate conserved epitope discovery. Nucleic Acids Res 3 6: W35-W41.
26. Goldsmith DB, Crosti G, Dwivedi B,McDaniel LD, Varsani A, Suttle CA et al. (2011). Development of phoH as a novel signature gene for assessing marine phage diversity. Appl Environ Microbiol 77: 7730-7739.
27. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321.
28. Kim K-H, Bae J-W. (2011). Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl Environ Microbiol 77: 7663-7668.
29. Kim K-H, Chang H-W, Nam Y-D, Roh SW, Kim M-S, Sung Y et al. (2008). Amplifica tion of uncultured single-stranded DNA viruses from rice paddy soil. Appl Environ Microbiol 74: 5975-5985.
30. Krupovic M, Prangishvili D, Hendrix RW, Bamford DH. (2011). Genomics of bacterial and archaeal viru ses: dynamics within the prokaryotic virosphere. Microbiol Mol Biol Rev 75: 610-635.
31. LabontéJM, Suttle CA. (2013). Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J 7: 2169-2177.
32. Larkin M, Blackshields G, Brown N, Chenna R, McGettigan PA, McWilliam H et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
33. Lóp ez-Bueno A, Tamames J, Velázquez D, Moya A, Quesada A, AlcamíA. (2009). High diversity of the viral community from an Antarctic lake. Science 326: 858-861.
34. Magurran AE. (2004). Measu ring Biological Diversity. Blackwell Science Ltd: Malden M.A.
35. McDaniel L, Breitbart M, Mobberley J, Long A, Haynes M, Rohwer F et al. (2008). Metagenomic analysis of lysogeny in Tampa Bay: implicati ons for prophage gene expression. PLoS One 3: e3263.
36. McDaniel LD, Rosario K, Breitbart M, Paul JH. (2013). Comparative metagenomics: Natural populations of induced prophages demonstrate highly unique, lower diversity viral sequences. Environ Microbiol 16: 570-585.
37. McKenna R, Bowman BR, Ilag LL, Rossmann MG, Fane BA. (1996). Atomic structure of the degraded procapsid particle of the bacteriophage G4: i nduced structural changes in the presence of calcium ions and functional implications. J Mol Biol 256: 736-750.
38. McKenna R, Xia D, Willingmann P, Hag LL, Krishnaswamy S, Rossmann MG et al. (1992). Atomic structure of single-stranded DNA bacteriophage ^j174 and its functional implications. Nature 355: 137.
39. Patel A, Noble RT, Steele JA, Schwalbach MS, Hewson I, Fuhrman JA. (2007). Vir us and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I. Nat Protoc 2: 269-276.
40. Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, Thomson NR et al. (2010). Antagonistic coevolution accelerates molecular evolution. Nature 464: 275-278.
41. Pettersen EF Goddard TD Huang CC Couch GS Greenblatt DM Meng EC et al.2004 UCSF Chimera-A visualization system for exploratory research and analysis. J Comput Chem 25 1605-1612.
42. Price MN, Dehal PS, Arkin AP. (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26: 1641-1650.
43. Rosario K, Breitbart M. (2011). Exploring the viral world through metagenomics. Curr Opin Virol 1: 289-297.
44. Rosario K, Nilsson C, Lim YW, Ruan Y, Breitbart M. (2009). Metagenomic analysis of viruses in reclaimed water. Environ Microbiol 11: 2806-2820.
45. Roux S, Enault F, Robin A, Ravet V, Personnic S, Theil S et al. (2012a). Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS One 7: e33641.
46. Roux S, Krupovic M, Poulet A, Debroas D, Enault F. (2012b). Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLoS One 7: e40418.
47. Sanger F, Air G, Barrell B, Brown N, Coulson A, Fiddes J et al. (1977). Nucleotide sequence of bacteriophage PhiX174 DNA. Nature 265: 687-695.
48. Schuster-Böckler B, Schultz J, Rahmann S. (2004). HMM logos for visualization of protein families. BMC Bioinformatics 5: 7.
49. Shannon CE, Weaver W. (1949). The Mathematical Theory of Communication. University of Illinois Press: Urbana, IL.
50. Smith RJ, Jeffries TC, Roudnew B, Seymour JR, Fitch AJ, Simons KL et al. (2013). Confined aquifers as viral reservoirs. Environ Microbiol Rep 5: 725-730.
51. Soetaert K, Heip C. (1990). Sample-size dependence of diversity indices and the determination of sufficient sample size in a high-diversity deep-sea environment. Mar Ecol Prog Ser 59: 305-307.
52. Steward GF, Culley AI, Mueller JA, Wood-Charlson EM, Belcaid M, Poisson G. (2012). Are we missing half of the viruses in the ocean? ISME J 7: 672-679.
53. Steward GF, Montiel JL, Aza m F. (2000). Genome size distributions indicate variability and similarities among marine viral assemblages from diverse environments. Limnol Oceanogr 45: 1697-1706.
54. Tamura K, Peterson D, Peterson N, St echer G, Nei M, Kumar S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
55. Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F. (2009). Laboratory procedures to generate viral metagenomes. Nat Protoc 4: 470-483.
56. Tomaru Y, Nagasaki K. (2007). Flow cytometric detection and enumeration of DNA and RNA viruses infecting marine eukaryotic microalgae. J Oceanogr 63: 215-221.
57. Tucker KP, Parsons R, Symonds EM, Breitbart M. (2011). Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean. ISME J 5: 822-830.
58. Yang Z, Lasker K, Schneidman-Duhovny D, Webb B, Huang CC, Pettersen EF et al. (2012). UCSF Chimera, MODELLER, and IMP: an integrated modeling system. J Struct Biol 179: 269-278.
59. Yoshida M, Takaki Y, Eitoku M, Nunoura T, Takai K. (2013). Metagenomic analysis of viral communities in (hado) pelagic sediments. PLoS One 8: e57271.
60. Yu Y, Breitbart M, McNairnie P, Rohwer F. (2006). FastGroupII: a web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinformatics 7: 57.