An antisense RNA in a lytic cyanophage links psbA to a gene encoding a homing endonuclease

ISME Journal

Volumn 4, Issue 9, 2010, Pages 1121-1135

  Millard, Andrew D ^a   Gierga, Gregor ^b   Clokie, Martha R J ^c   Evans, David J ^a   Hess, Wolfgang R ^b   Scanlan, David J ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

asRNA; cyanophage; endonuclease; intron; psbA

Indexed keywords

COMPLEMENTARY RNA; ENDONUCLEASE; MESSENGER RNA; PHOTOSYSTEM II, PSBA SUBUNIT; VIRUS PROTEIN; VIRUS RNA;

BIOINFORMATICS; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; MARINE ENVIRONMENT; PHOTOSYNTHESIS; PROTEIN; VIRUS;

AMINO ACID SEQUENCE; ARTICLE; BACTERIOPHAGE; BIOLOGY; CYANOBACTERIUM; GENE EXPRESSION PROFILING; GENETICS; INTRON; METABOLISM; METAGENOME; MOLECULAR GENETICS; NORTHERN BLOTTING; PHOTOSYSTEM II; PHYLOGENY; RNA SPLICING; SEQUENCE HOMOLOGY; VIROLOGY;

AMINO ACID SEQUENCE; BACTERIOPHAGES; BLOTTING, NORTHERN; COMPUTATIONAL BIOLOGY; CYANOBACTERIA; ENDONUCLEASES; GENE EXPRESSION PROFILING; INTRONS; METAGENOME; MOLECULAR SEQUENCE DATA; PHOTOSYSTEM II PROTEIN COMPLEX; PHYLOGENY; RNA SPLICING; RNA, ANTISENSE; RNA, MESSENGER; RNA, VIRAL; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

ANIMALIA; EUKARYOTA; PROKARYOTA;

EID: 77956095145     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2010.43     Document Type: Article

References (64)

1. Backofen R, Hess WR. (2010). Computational prediction of sRNAs and their targets in bacteria. RNA Biol 7: 1-10.
2. Bonocora RP, Shub DA. (2009). A likely pathway for formation of mobile group I introns. Curr Biol 19: 223-228.
3. Bragg JG, Chisholm SW. (2008). Modeling the fitness consequences of a cyanophage-encoded photosynthesis gene. PLoS One 3: e3550.
4. Brantl S. (2007). Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 10: 102-109.
5. Brouard JS, Otis C, Lemieux C, Turmel M. (2008). Chloroplast DNA sequence of the green alga Oedogonium cardiacum (Chlorophyceae): unique genome architecture, derived characters shared with the Chaetophorales and novel genes acquired through horizontal transfer. BMC Genomics 9: 290.
6. Chenard C, Suttle CA. (2008). Phylogenetic diversity of sequences of cyanophage photosynthetic gene psbA in marine and freshwaters. Appl Environ Microbiol 74: 5317-5324.
7. Clokie MR, Shan J, Bailey S, Jia Y, Krisch HM,West S et al. (2006). Transcription of a 'photosynthetic' T4-type phage during infection of a marine cyanobacterium. Environ Microbiol 8: 827-835.
8. Deshpande NN, Bao Y, Herrin DL. (1997). Evidence for light/redox- regulated splicing of psbA pre-RNAs in Chlamydomonas chloroplasts. RNA 3: 37-48.
9. Dufresne A, Ostrowski M, Scanlan DJ, Garczarek L, Mazard S, Palenik BP et al. (2008). Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria. Genome Biol 9: R90.
10. Duhring U, Axmann IM, Hess WR, Wilde A. (2006). An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci USA 103: 7054-7058.
11. Georg J, Voss B, Scholz I, Mitschke J, Wilde A, Hess WR. (2009). Evidence for a major role of antisense RNAs in cyanobacterial gene regulation. Mol Syst Biol 5: 305.
12. Hellweger FL. (2009). Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. Environ Microbiol 11: 1386-1394.
13. Hernandez JA, Muro-Pastor AM, Flores E, Bes MT, Peleato ML, Fillat MF. (2006). Identification of a furA cis antisense RNA in the cyanobacterium Anabaena sp. PCC 7120. J Mol Biol 355: 325-334.
14. Huelsenbeck JP, Ronquist F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
15. Itoh T, Tomizawa J. (1980). Formation of an RNA primer for initiation of replication of ColE1 DNA by ribonuclease H. Proc Natl Acad Sci USA 77: 2450-2454.
16. Jurica MS, Stoddard BL. (1999). Homing endonucleases: structure, function and evolution. Cell Mol Life Sci 55: 1304-1326.
17. Kettler GC, Martiny AC, Huang K, Zucker J, Coleman ML, Rodrigue S et al. (2007). Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 3: e231.
18. Krinke L, Wulff DL. (1987). OOP RNA, produced from multicopy plasmids, inhibits lambda cII gene expression through an RNase III-dependent mechanism. Genes Dev 1: 1005-1013.
19. Lacatena RM, Cesareni G. (1981). Base pairing of RNA I with its complementary sequence in the primer precursor inhibits ColE1 replication. Nature 294: 623-626.
20. Lee J, Herrin DL. (2003). Mutagenesis of a light-regulated psbA intron reveals the importance of efficient splicing for photosynthetic growth. Nucleic Acids Res 31: 4361-4372.
21. Lindell D, Jaffe JD, Coleman ML, Futschik ME, Axmann IM, Rector T et al. (2007). Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449: 83-86.
22. Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW. (2005). Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 86-89.
23. Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, Chisholm SW. (2004). Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101: 11013-11018.
24. Liu Q, Belle A, Shub DA, Belfort M, Edgell DR. (2003). SegG endonuclease promotes marker exclusion and mediates co-conversion from a distant cleavage site. J Mol Biol 334: 13-23.
25. Livak KJ, Schmittgen TD. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
26. Logemann J, Schell J, Willmitzer L. (1987). Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16-20.
27. Lu J, Chen F, Hodson RE. (2001). Distribution, isolation, host specificity, and diversity of cyanophages infecting marine Synechococcus spp. in river estuaries. Appl Environ Microbiol 67: 3285-3290.
28. Mann NH, Clokie MR, Millard A, Cook A, Wilson WH, Wheatley PJ et al. (2005). The genome of S-PM2, a 'photosynthetic' T4-type bacteriophage that infects marine Synechococcus strains. J Bacteriol 187: 3188-3200.
29. Mann NH, Cook A, Millard A, Bailey S, Clokie M. (2003). Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424: 741.
30. Markham NR, Zuker M. (2008). UNAFold: software for nucleic acid folding and hybridization. In: Keith JM (ed). Bioinformatics Volume II. Structure, Functions and Applications. Humana Press: Totowa, NJ, USA, pp 3-31.
31. Marston MF, Amrich CG. (2009). Recombination and microdiversity in coastal marine cyanophages. Environ Microbiol 11: 2893-2903.
32. Marston MF, Sallee JL. (2003). Genetic diversity and temporal variation in the cyanophage community infecting marine Synechococcus species in Rhode Island's coastal waters. Appl Environ Microbiol 69: 4639-4647.
33. Maul JE, Lilly JW, Cui L, dePamphilis CW, Miller W, Harris EH et al. (2002). The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14: 2659-2679.
34. Millard A, Clokie MR, Shub DA, Mann NH. (2004). Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci USA 101: 11007-11012.
35. Millard A, Mann NH. (2006). A temporal and spatial investigation of cyanophage abundance in the Gulf of Aqaba, Red Sea. J Mar Biol Assocn UK 86: 507-515.
36. Millard AD, Zwirglmaier K, Downey MJ, Mann NH, Scanlan DJ. (2009). Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence of Synechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution. Environ Microbiol 11: 2370-2387.
37. Raghavan R, Minnick MF. (2009). Group I introns and inteins: disparate origins but convergent parasitic strategies. J Bacteriol 191: 6193-6202.
38. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S et al. (2007). The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through eastern tropical Pacific. PLoS Biol 5: e77.
39. Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR et al. (2009). Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73: 249-299.
40. Seshadri R, Kravitz SA, Smarr L, Gilna P, Frazier M. (2007). CAMERA: a community resource for metagenomics. PLoS Biol 5: e75.
41. Sharon I, Alperovitch A, Rohwer F, Haynes M, Glaser F, Atamna-Ismaeel N et al. (2009). Photosystem I gene cassettes are present in marine virus genomes. Nature 461: 258-262.
42. Sharon I, Tzahor S, Williamson S, Shmoish M, Man-Aharonovich D, Rusch DB et al. (2007). Viral photosynthetic reaction center genes and transcripts in the marine environment. ISME J 1: 492-501.
43. Simmonds P, Smith DB. (1999). Structural constraints on RNA virus evolution. J Virol 73: 5787-5794.
44. Spiegelman WG, Reichardt LF, Yaniv M, Heinemann SF, Kaiser AD, Eisen H. (1972). Bidirectional transcription and the regulation of Phage lambda repressor synthesis. Proc Natl Acad Sci USA 69: 3156-3160.
45. Steglich C, Futschik ME, Lindell D, Voss B, Chisholm SW, Hess WR. (2008). The challenge of regulation in a minimal photoautotroph: non-coding RNAs in Prochlorococcus. PLoS Genet 4: e1000173.
46. Stork M, Di Lorenzo M, Welch TJ, Crosa JH. (2007). Transcription termination within the iron transportbiosynthesis operon of Vibrio anguillarum requires an antisense RNA. J Bacteriol 189: 3479-3488.
47. Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW. (2005). Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3: e144.
48. Sullivan MB, Krastins B, Hughes JL, Kelly L, Chase M, Sarracino D et al. (2009). The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial 'mobilome'. Environ Microbiol 11: 2935-2951.
49. Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW. (2006). Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4: e234.
50. Sullivan MB, Waterbury JB, Chisholm SW. (2003). Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424: 1047-1051.
51. Suttle CA. (2005). Viruses in the sea. Nature 437: 356-361.
52. Suttle CA. (2007). Marine viruses-major players in the global ecosystem. Nat Rev Microbiol 5: 801-812.
53. Suttle CA, Chan AM. (1994). Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp. Appl Environ Microbiol 60: 3167-3174.
54. Tramonti A, De Canio M, De Biase D. (2008). GadX/GadWdependent regulation of the Escherichia coli acid fitness island: transcriptional control at the gadY-gadW divergent promoters and identification of four novel 42 bp GadX/GadW-specific binding sites. Mol Microbiol 70: 965-982.
55. Wang K, Chen F. (2008). Prevalence of highly host-specific cyanophages in the estuarine environment. Environ Microbiol 10: 300-312.
56. Waterbury JB, Valois FW. (1993). Resistance to cooccurring phages enables marine Synechococcus communities to coexist with cyanophages abundant in seawater. Appl Environ Microbiol 59: 3393-3399.
57. Weigele PR, Pope WH, Pedulla ML, Houtz JM, Smith AL, Conway JF et al. (2007). Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus. Environ Microbiol 9: 1675-1695.
58. Williamson SJ, Rusch DB, Yooseph S, Halpern AL, Heidelberg KB, Glass JI et al. (2008). The Sorcerer II Global ocean sampling expedition: metagenomic characterization of viruses within aquatic microbial samples. PLoS One 3: e1456.
59. Wilson WH, Carr NG, Mann NH. (1996). The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp WH7803. J Phycol 32: 506-516.
60. Wilson WH, Joint IR, Carr NG, Mann NH. (1993). Isolation and molecular characterization of five marine cyanophages propagated on Synechococcus sp. Strain WH7803. Appl Environ Microbiol 59: 3736-3743.
61. Wyman M, Gregory RP, Carr NG. (1985). Novel role for phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2. Science 230: 818-820.
62. Zeidner G, Bielawski JP, Shmoish M, Scanlan DJ, Sabehi G, Beja O. (2005). Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ Microbiol 7: 1505-1513.
63. Zeidner G, Preston CM, Delong EF, Massana R, Post AF, Scanlan DJ et al. (2003). Molecular diversity among marine picophytoplankton as revealed by psbA analyses. Environ Microbiol 5: 212-216.
64. Zeng Q, Bonocora RP, Shub DA. (2009). A free-standing homing endonuclease targets an intron insertion site in the psbA gene of cyanophages. Curr Biol 19: 218-222.