Transcriptome dynamics of a broad host-range cyanophage and its hosts

ISME Journal

Volumn 10, Issue 6, 2016, Pages 1437-1455

  Doron, Shany ^a   Fedida, Ayalla ^b   Hernndez Prieto, Miguel A ^c,e   Sabehi, Gazalah ^b   Karunker, Iris ^a   Stazic, Damir ^d   Feingersch, Roi ^b   Steglich, Claudia ^d   Futschik, Matthias ^c   Lindell, Debbie ^b   Sorek, Rotem ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c UNIVERSITY OF ALGARVE   (Portugal)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOBACTERIUM; GENE EXPRESSION; GENOME; HOST RANGE; INFECTIVITY; MARINE ENVIRONMENT; PARADIGM SHIFT; RNA; VIRUS;

CYANOBACTERIA; PROCHLOROCOCCUS; SYNECHOCOCCUS;

TRANSCRIPTOME;

BACTERIOPHAGE; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; HOST RANGE; METAGENOMICS; PHYLOGENY; PHYSIOLOGY; PROCHLOROCOCCUS; SEA; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SYNECHOCOCCUS; VIROLOGY;

BACTERIOPHAGES; GENE EXPRESSION PROFILING; HOST SPECIFICITY; METAGENOMICS; OCEANS AND SEAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; PROCHLOROCOCCUS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, RNA; SYNECHOCOCCUS; TRANSCRIPTOME;

EID: 84949604565     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.210     Document Type: Article

References (94)

1. Anantharaman V, Aravind L. (2003). New connections in the prokaryotic toxin-Antitoxin network: relationship with the eukaryotic nonsense-mediated RNA decay system. Genome Biol 4: R81
2. 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
3. Avrani S, Lindell D. (2015). Convergent evolution toward an improved growth rate and a reduced resistance range in Prochlorococcus strains resistant to phage. Proc Natl Acad Sci USA 112: E2191-E2200
4. Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D. (2011). Genomic island variability facilitates Prochlorococcusvirus coexistence. Nature 474: 604-608
5. Bench SR, Hanson TE, Williamson KE, Ghosh D, Radosovich M, Wang K, et al. (2007). Metagenomic characterization of Chesapeake Bay virioplankton. Appl Environ Microbiol 73: 7629-7641
6. Breitbart M. (2012). Marine viruses: truth or dare. Ann Rev Mar Sci 4: 425-448
7. Bullard JH, Purdom E, Hansen KD, Dudoit S. (2010). Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 11: 94
8. Clokie MR, Mann NH. (2006). Marine cyanophages and light. Environ Microbiol 8: 2074-2082
9. 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
10. Coleman ML, Sullivan MB, Martiny AC, Steglich C, Barry K, Delong EF, et al. (2006). Genomic islands and the ecology and evolution of Prochlorococcus. Science 311: 1768-1770
11. Comeau AM, Chan AM, Suttle CA. (2006). Genetic richness of vibriophages isolated in a coastal environment. Environ Microbiol 8: 1164-1176
12. Dekel-Bird NP, Sabehi G, Mosevitzky B, Lindell D. (2015). Host-dependent differences in abundance, composition and host range of cyanophages from the Red Sea. Environ Microbiol 17: 1286-1299
13. Desplats C, Dez C, Tétart F, Eleaume H, Krisch HM. (2002). Snapshot of the genome of the pseudo-T-even bacteriophage RB49. J Bacteriol 184: 2789-2804
14. 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
15. Edelheit S, Schwartz S, Mumbach MR, Wurtzel O, Sorek R. (2013). Transcriptome-wide mapping of 5-methylcytidine RNA modifications in bacteria, archaea, and yeast reveals m5C within archaeal mRNAs. PLoS Genet 9: e1003602
16. Elena SF, Agudelo-Romero P, Lali? J. (2009). The evolution of viruses in multi-host fitness landscapes. Open Virol J 3: 1-6
17. Enav H, Béjà O, Mandel-Gutfreund Y. (2012). Cyanophage tRNAs may have a role in cross-infectivity of oceanic Prochlorococcus and Synechococcus hosts. ISME J 6: 619-628
18. Fuhrman JA. (1999). Marine viruses and their biogeochemical and ecological effects. Nature 399: 541-548
19. Fuller NJ, Marie D, Partensky F, Vaulot D, Post AF, Scanlan DJ. (2003). Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl Environ Microbiol 69: 2430-2443
20. 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
21. Guttman B, Raya R, Kutter E. (2005) Basic phage biology. In: Kutter E, Sulakvelidze A (eds). Bacteriophages Biology and Application. CRC Press: Boca Raton, FL, USA, pp 29-66
22. Herrero A, Muro-Pastor AM, Flores E. (2001). Nitrogen control in cyanobacteria. J Bacteriol 183: 411-425
23. Holtzendorff J, Partensky F, Jacquet S, Bruyant F, Marie D, Garczarek L, et al. (2001). Diel expression of cell cycle-related genes in synchronized cultures of Prochlorococcus sp. strain PCC 9511. J Bacteriol 183: 915-920
24. Horvitz HR. (1974). Bacteriophage T4 mutants deficient in alteration and modification of the Escherichia coli RNA polymerase. J Mol Biol 90: 739-750
25. Horvitz HR. (1974). Control by bacteriophage T4 of two sequential phosphorylations of the alpha subunit of Escherichia coli RNA polymerase. J Mol Biol 90: 727-738
26. Jabbar MA, Snyder L. (1984). Genetic and physiological studies of an Escherichia coli locus that restricts polynucleotide kinase-And RNA ligase-deficient mutants of bacteriophage T4. J Virol 51: 522-529
27. Koch T, Raudonikiene A, Wilkens K, Rüger W. (1995). Overexpression, purification, and characterization of the ADP-ribosyltransferase (gpAlt) of bacteriophage T4: ADP-ribosylation of E. coli RNA polymerase modulates T4 early transcription. Gene Expr 4: 253-264
28. Koerner JF, Snustad DP. (1979). Shutoff of host macromolecular synthesis after T-even bacteriophage infection. Microbiol Rev 43: 199-223
29. Labrie SJ, Samson JE, Moineau S. (2010). Bacteriophage resistance mechanisms. Nat Rev Microbiol 8: 317-327
30. Lavigne R, Lecoutere E, Wagemans J, Cenens W, Aertsen A, Schoofs L, et al. (2013). A multifaceted study of Pseudomonas aeruginosa shutdown by virulent podovirus LUZ19. MBio 4: e00061-13
31. Limor-Waisberg K, Carmi A, Scherz A, Pilpel Y, Furman I. (2011). Specialization versus adaptation: two strategies employed by cyanophages to enhance their translation efficiencies. Nucleic Acids Res 39: 6016-6028
32. 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
33. 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
34. Lindell D, Padan E, Post AF. (1998). Regulation of ntcA expression and nitrite uptake in the marine Synechococcus sp. strain WH 7803. J Bacteriol 180: 1878-1886
35. Mann NH, Clokie MR, Millard AD, 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
36. Mann NH, Cook A, Millard A, Bailey S, Clokie M. (2003). Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424: 741
37. Marchand I, Nicholson AW, Dreyfus M. (2001). Bacteriophage T7 protein kinase phosphorylates RNase E and stabilizes mRNAs synthesized by T7 RNA polymerase. Mol Microbiol 42: 767-776
38. Marston MF, Pierciey FJ, Shepard A, Gearin G, Qi J, Yandava C, et al. (2012). Rapid diversification of coevolving marine Synechococcus and a virus. Proc Natl Acad Sci USA 109: 4544-4549
39. Marston MF, Sallee JL. (2003). Genetic diversity and temporal variation in the cyanophage community infecting marine Synechococcus species in Rhode Islands coastal waters. Appl Environ Microbiol 69: 4639-4647
40. Martiny AC, Coleman ML, Chisholm SW. (2006). Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci USA 103: 12552-12557
41. Millard AD, Gierga G, Clokie MR, Evans DJ, Hess WR, Scanlan DJ. (2010). An antisense RNA in a lytic cyanophage links psbA to a gene encoding a homing endonuclease. ISME J 4: 1121-1135
42. Millard AD, Mann NH. (2006). A temporal and spatial investigation of cyanophage abundance in the Gulf of Aqaba, Red Sea. J Mar Biol Assoc UK 86: 507-515
43. 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
44. Miller ES, Heidelberg JF, Eisen JA, Nelson WC, Durkin AS, Ciecko A, et al. (2003). Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J Bacteriol 185: 5220-5233
45. Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Ruger W. (2003). Bacteriophage T4 genome. Microbiol Mol Biol Rev 67: 86-156
46. Mitschke J, Georg J, Scholz I, Sharma C, Dienst D, Bantscheff J, et al. (2011). An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc Natl Acad Sci USA 108: 1-6
47. Moore LR, Coe A, Zinser ER, Saito MA, Sullivan MB, Lindell D, et al. (2007). Culturing the marine cyanobacterium. Prochlorococcus Limnol Ocean Methods 5: 353-362
48. Mosig G, Eiserling F. (2006) T4 and related phages: structure and development. In: Calendar R (ed). The Bacteriophages. Oxford University Press: New York, NY, USA, pp 225-267
49. Mosig G, Yu S, Myung H, Haggård-Ljungquist E, Davenport L, Carlson K, et al. (1997). A novel mechanism of virus-virus interactions: bacteriophage P2 Tin protein inhibits phage T4 DNA synthesis by poisoning the T4 single-stranded DNA binding protein, gp32. Virology 230: 72-81
50. Muro-Pastor MI, Reyes JC, Florencio FJ. (2001). Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J Biol Chem 276: 38320-38328
51. Nolan JM, Petrov V, Bertrand C, Krisch HM, Karam JD. (2006). Genetic diversity among five T4-like bacteriophages. Virol J 3: 30
52. Palenik BP, Brahamsha B, Larimer FW, Land M, Hauser L, Chain P, et al. (2003). The genome of a motile marine. Synechococcus Nature 424: 1037-1042
53. Palenik BP, Ren Q, Dupont CL, Myers GS, Heidelberg JF, Badger JH, et al. (2006). Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment. Proc Natl Acad Sci USA 103: 13555-13559
54. Pinto FL, Thapper A, Sontheim W, Lindblad P. (2009). Analysis of current and alternative phenol based RNA extraction methodologies for cyanobacteria. BMC Mol Biol 10: 79-87
55. Poranen MM, Ravantti JJ, Grahn AM, Gupta R, Auvinen P, Bamford DH. (2006). Global changes in cellular gene expression during bacteriophage PRD1 infection. J Virol 80: 8081-8088
56. Puerta-Fernández E, Vioque A. (2011). Hfq is required for optimal nitrate assimilation in the Cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 193: 3546-3555
57. Pène C, Uzan M. (2000). The bacteriophage T4 anti-sigma factor AsiA is not necessary for the inhibition of early promoters in vivo. Mol Microbiol 35: 1180-1191
58. Ravantti JJ, Ruokoranta TM, Alapuranen AM, Bamford DH. (2008). Global transcriptional responses of Pseudomonas aeruginosa to phage PRR1 infection. J Virol 82: 2324-2329
59. Riede I, Eschbach ML. (1986). Evidence that TraT interacts with OmpA of Escherichia coli. FEBS Lett 205: 241-245
60. Rifat D, Wright NT, Varney KM, Weber DJ, Black LW. (2008). Restriction endonuclease inhibitor I.P.I of bacteriophage T4: a novel structure for a dedicated target. J Mol Biol 375: 720-734
61. Rocap G, Distel DL, Waterbury JB, Chisholm SW. (2002). Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68: 1180-1191
62. Roucourt B, Lavigne R. (2009). The role of interactions between phage and bacterial proteins within the infected cell: a diverse and puzzling interactome. Environ Microbiol 11: 2789-2805
63. 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
64. Sabehi G, Shaulov L, Silver DH, Yanai I, Harel A, Lindell D. (2012). A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans. Proc Natl Acad Sci USA 109: 2037-2042
65. Salzberg SL, Delcher AL, Kasif S, White O. (1998). Microbial gene identification using interpolated Markov models. Nucleic Acids Res 26: 544-548
66. 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
67. Scanlan DJ. (2003). Physiological diversity and niche adaptation in marine Synechococcus. Adv Microb Physiol 47: 1-64
68. Smyth GK. (2005). Limma: linear models for microarray data. In: Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S (eds). Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Statistics for Biology and Health, Springer-Verlag: New York, NY, USA, pp 397-420
69. Staley JT, Gunsalus RP, Lory S, Perry JJ. (2007) Viruses. In: Microbial Life. Sinauer Associates, Inc.: Sunderland, MA, USA, pp 389-408
70. Stazic D, Lindell D, Steglich C. (2011). Antisense RNA protects mRNA from RNase E degradation by RNARNA duplex formation during phage infection. Nucleic Acids Res 39: 4890-4899
71. Stern A, Sorek R. (2011). The phage-host arms race: shaping the evolution of microbes. Bioessays 33: 43-51
72. Stork T, Michel K-P, Pistorius EK, Dietz K-J. (2005). Bioinformatic analysis of the genomes of the cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942 for the presence of peroxiredoxins and their transcript regulation under stress. J Exp Bot 56: 3193-3206
73. Stuart RK, Brahamsha B, Busby K, Palenik B. (2013). Genomic island genes in a coastal marine Synechococcus strain confer enhanced tolerance to copper and oxidative stress. ISME J 7: 1139-1149
74. Su Z, Mao F, Dam P, Wu H, Olman V, Paulsen IT, et al. (2006). Computational inference and experimental validation of the nitrogen assimilation regulatory network in cyanobacterium Synechococcus sp. WH 8102. Nucleic Acids Res 34: 1050-1065
75. Sullivan MB, Coleman ML, Weigele PR, Rohwer F, Chisholm SW. (2005). Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3: e144
76. Sullivan MB, Huang KH, Ignacio-Espinoza JC, Berlin AM, Kelly L, Weigele PR, et al. (2010). Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol 12: 3035-3056
77. Sullivan MB, Waterbury JB, Chisholm SW. (2003). Cyanophages infecting the oceanic cyanobacterium. Prochlorococcus Nature 424: 1047-1051
78. Suttle CA, Chan AM. (1993). Marine cyanophages infecting oceanic and coastal strains of Synechococcus: abundance, morphology, cross-infectivity and growth characteristics. Mar Ecol Prog Ser 92: 99-109
79. Suttle CA. (2005). Viruses in the sea. Nature 437: 356-361
80. Tetu SG, Johnson DA, Varkey D, Phillippy K, Stuart RK, Dupont CL, et al. (2013). Impact of DNA damaging agents on genome-wide transcriptional profiles in two marine Synechococcus species. Front Microbiol 4: 232
81. Thompson AW, Huang K, Saito MA, Chisholm SW. (2011). Transcriptome response of high-And lowlight-Adapted Prochlorococcus strains to changing iron availability. ISME J 5: 1580-1594
82. Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, Stubbe J, et al. (2011). Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci USA 108: E757-E764
83. Tolonen AC, Aach J, Lindell D, Johnson ZI, Rector T, Steen R, et al. (2006). Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol Syst Biol 2: 53
84. Ueno H, Yonesaki T. (2004). Phage-induced change in the stability of mRNAs. Virology 329: 134-141
85. Uzan M. (2009). RNA processing and decay in bacteriophage T4. Prog Mol Biol Transl Sci 85: 43-89
86. Wang K, Chen F. (2008). Prevalence of highly host-specific cyanophages in the estuarine environment. Environ Microbiol 10: 300-312
87. Waterbury JB, Valois FW. (1993). Resistance to co-occurring phages enables marine Synechococcus communities to coexist with cyanophages abundant in seawater. Appl Environ Microbiol 59: 3393-3399
88. 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
89. Woolhouse ME, Taylor LH, Haydon DT. (2001). Population biology of multihost pathogens. Science 292: 1109-1112
90. Wurtzel O, Sesto N, Mellin JR, Karunker I, Edelheit S, Becavin C, et al. (2012). Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol Syst Biol 8: 583
91. Wurtzel O, Yoder-Himes DR, Han K, Dandekar AA, Edelheit S, Greenberg EP, et al. (2012). The singlenucleotide resolution transcriptome of Pseudomonas aeruginosa grown in body temperature. PLoS Pathog 8: e1002945
92. Wyman M, Gregory RP, Carr NG. (1985). Novel role for phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2. Science 230: 818-820
93. Zinser ER, Coe A, Johnson ZI, Martiny AC, Fuller NJ, Scanlan DJ, et al. (2006). Prochlorococcus ecotype abundances in the North Atlantic Ocean as revealed by an improved quantitative PCR method. Appl Environ Microbiol 72: 723-732
94. Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L, Vaulot D, et al. (2008). Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10: 147-161