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Gene expression of Microcystis aeruginosa during infection of cyanomyovirus Ma-LMM01

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Abstract

Ma-LMM01 is a lytic phage infecting the toxic cyanobacterium Microcystis aeruginosa. We have investigated the transcription dynamics of host genes during phage infection using quantitative reverse transcriptase-PCR. No significant shutdown of host transcription occurred. There was no change in the transcript levels of the psbA genes [photosystem II D1 (PSII D1)], but the transcript levels of the stress response genes and the alternative σ factor gene sigB were upregulated. The transcript levels of the Calvin cycle genes and pentose phosphate pathway genes did not change or only slightly decreased, suggesting that sufficient amounts of NADPH and nucleic acid were available without redirection of the carbon flux. These results suggest that Ma-LMM01 infection induces protection of the host’s photosynthetic apparatus, conserves the host’s PSII through phycobilisome degradation using its own NblA and provides protection to the photosystem using host stress response genes. This protection of the host’s photosystem without extensive genetic manipulation may have some benefits for viruses infecting cyanobacteria that inhabit surface waters and may also be advantageous for Ma-LMM01 to avoid the host defense systems.

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References

  1. Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, Stubbe J, Chisholm SW (2011) Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci USA 108:E757–E764

    Article  CAS  PubMed  Google Scholar 

  2. Lavigne R, Darius P, Summer EJ, Seto D, Mahadevan P, Nilsson AS, Ackermann HW, Kropinski AM (2009) Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 9:224

    Article  PubMed Central  PubMed  Google Scholar 

  3. Carstens EB, Ball LA (2009) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2008). Arch Virol 154:1181–1188

    Article  CAS  PubMed  Google Scholar 

  4. Yoshida T, Nagasaki K, Takashima Y, Shirai Y, Tomaru Y, Takao Y, Sakamoto S, Hiroishi S, Ogata H (2008) Ma-LMM01 infecting toxic Microcystis aeruginosa illuminates diverse cyanophage genome strategies. J Bacteriol 190:1762–1772

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Yoshida T, Takashima Y, Tomaru Y, Shirai Y, Takao Y, Hiroishi S, Nagasaki K (2006) Isolation and characterization of a cyanophage infecting the toxic cyanobacterium Microcystis aeruginosa. Appl Environ Microbiol 72:1239–1247

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Yoshida-Takashima Y, Yoshida M, Ogata H, Nagasaki K, Hiroishi S, Yoshida T (2012) Cyanophage infection in the bloom-forming cyanobacteria Microcystis aeruginosa in surface freshwater. Microbes Environ 27:350–355

    Article  PubMed  Google Scholar 

  7. Mlouka A, Comte K, Castets AM, Bouchier C, Tandeau de Marsac N (2004) The gas vesicle gene cluster from Microcystis aeruginosa and DNA rearrangements that lead to loss of cell buoyancy. J Bacteriol 186:2355–2365

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Gao EB, Gui JF, Zhang QY (2012) A novel cyanophage with a cyanobacterial nonbleaching protein A gene in the genome. J Virol 86:236–245

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Kasai F, Kawachi M, Erata M, Watanabe MM (2004) List of strains, microalgae and protozoa. National Institute for Environmental Studies, Tsukuba

    Google Scholar 

  10. Yoshida T, Maki M, Okamoto H, Hiroishi S (2005) Coordination of DNA replication and cell division in cyanobacteria Microcystis aeruginosa. FEMS Microbiol Lett 251:149–154

    Article  CAS  PubMed  Google Scholar 

  11. Yagi O, Hagiwara T, Takamura Y, Sudo R (1984) Growth characteristics of axenic and unialgal Microcystis isolated from Lake Kasumigaura. Jpn J Water Poll Res 7:496–503

    Article  Google Scholar 

  12. Sato N (1995) A family of cold-regulated RNA-binding protein genes in the cyanobacterium Anabaena variabilis M3. Nucleic Acids Res 23:2161–2167

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134

    Article  CAS  Google Scholar 

  14. Yoshida M, Yoshida T, Yoshida-Takashima Y, Kashima A, Hiroishi S (2010) Real-time PCR detection of host-mediated cyanophage gene transcripts during infection of a natural Microcystis aeruginosa population. Microbes Environ 25:211–215

    Article  PubMed  Google Scholar 

  15. Kimura S, Yoshida T, Hosoda N, Honda T, Kuno S, Kamiji R, Hashimoto R, Sako Y (2012) Diurnal infection patterns and impact of Microcystis cyanophages in a Japanese pond. Appl Environ Microbiol 78:5805–5811

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Lonetto M, Gribskov M, Gross CA (1992) The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol 174:3843–3849

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Mizuuchi K, O’Dea MH, Gellert M (1978) DNA gyrase: subunit structure and ATPase activity of the purified enzyme. Proc Natl Acad Sci USA 75:5960–5963

    Article  CAS  PubMed  Google Scholar 

  18. Radding CM (1981) Recombination activities of E. coli RecA protein. Cell 25:3–4

    Article  CAS  PubMed  Google Scholar 

  19. Kaneko T, Nakajima N, Okamoto S, Suzuki I, Tanabe Y, Tamaoki M, Nakamura Y, Kasai F, Watanabe A, Kawashima K, Kishida Y, Ono A, Shimizu Y, Takahashi C, Minami C, Fujishiro T, Kohara M, Katoh M, Nakazaki N, Nakayama S, Yamada M, Tabata S, Watanabe MM (2007) Complete genomic structure of the bloom-forming toxic cyanobacterium Microcystis aeruginosa NIES-843. DNA Res 14:247–256

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Hohn T, Hohn B, Engel A, Wurtz M, Smith PR (1979) Isolation and characterization of the host protein groE involved in bacteriophage lambda assembly. J Mol Biol 129:359–373

    Article  CAS  PubMed  Google Scholar 

  21. Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  22. Sato T, Minagawa S, Kojima E, Okamoto N, Nakamoto H (2010) HtpG, the prokaryotic homologue of Hsp90, stabilizes a phycobilisome protein in the cyanobacterium Synechococcus elongatus PCC 7942. Mol Microbiol 76:576–589

    Article  CAS  PubMed  Google Scholar 

  23. Tanaka N, Nakamoto H (1999) HtpG is essential for the thermal stress management in cyanobacteria. FEBS Lett 458:117–123

    Article  CAS  PubMed  Google Scholar 

  24. Barker M, de Vries R, Nield J, Komenda J, Nixon PJ (2006) The deg proteases protect Synechocystis sp. PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. J Biol Chem 281:30347–30355

    Article  CAS  PubMed  Google Scholar 

  25. Clausen T, Kaiser M, Huber R, Ehrmann M (2011) HTRA proteases: regulated proteolysis in protein quality control. Nat Rev Mol Cell Biol 12:152–162

    Article  CAS  PubMed  Google Scholar 

  26. Imamura S, Asayama M, Shirai M (2004) In vitro transcription analysis by reconstituted cyanobacterial RNA polymerase: roles of group 1 and 2 sigma factors and a core subunit, RpoC2. Genes Cells 9:1175–1187

    Article  CAS  PubMed  Google Scholar 

  27. Asayama M, Kato H, Shibato J, Shirai M, Ohyama T (2002) The curved DNA structure in the 5′-upstream region of the light-responsive genes: its universality, binding factor and function for cyanobacterial psbA transcription. Nucleic Acids Res 30:4658–4666

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Koerner JF, Snustad DP (1979) Shutoff of host macromolecular synthesis after T-even bacteriophage infection. Microbiol Rev 43:199–223

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Pineda M, Gregory BD, Szczypinski B, Baxter KR, Hochschild A, Miller ES, Hinton DM (2004) A family of anti-sigma70 proteins in T4-type phages and bacteria that are similar to AsiA, a transcription inhibitor and co-activator of bacteriophage T4. J Mol Biol 344:1183–1197

    Article  CAS  PubMed  Google Scholar 

  30. Lindell D, Jaffe JD, Coleman ML, Futschik ME, Axmann IM, Rector T, Kettler G, Sullivan MB, Steen R, Hess WR, Church GM, Chisholm SW (2007) Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449:83–86

    Article  CAS  PubMed  Google Scholar 

  31. Clokie MR, Shan J, Bailey S, Jia Y, Krisch HM, West S, Mann NH (2006) Transcription of a ‘photosynthetic’ T4-type phage during infection of a marine cyanobacterium. Environ Microbiol 8:827–835

    Article  CAS  PubMed  Google Scholar 

  32. Wikner J, Vallino JJ, Steward GF, Smith DC, Azam F (1993) Nucleic acids from the host bacterium as a major source of nucleotides for three marine bacteriophages. FEMS Microbiol Ecol 12:237–248

    Article  CAS  Google Scholar 

  33. Wu J, Sunda W, Boyle EA, Karl DM (2000) Phosphate depletion in the Western North Atlantic Ocean. Science 289:759–762

    Article  CAS  PubMed  Google Scholar 

  34. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Makarova KS, Wolf YI, Snir S, Koonin EV (2011) Defense islands in bacterial and archaeal genomes and prediction of novel defense systems. J Bacteriol 193:6039–6056

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712

    Article  CAS  PubMed  Google Scholar 

  37. Kuno S, Yoshida T, Kaneko T, Sako Y (2012) Intricate interactions between the bloom-forming cyanobacterium Microcystis aeruginosa and foreign genetic elements, revealed by diversified clustered regularly interspaced short palindromic repeat (CRISPR) signatures. Appl Environ Microbiol 78:5353–5360

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Fineran PC, Blower TR, Foulds IJ, Humphreys DP, Lilley KS, Salmond GP (2009) The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc Natl Acad Sci USA 106:894–899

    Article  CAS  PubMed  Google Scholar 

  39. Engelberg-Kulka H, Amitai S, Kolodkin-Gal I, Hazan R (2006) Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2:e135

    Article  PubMed Central  PubMed  Google Scholar 

  40. Imamura S, Asayama M (2009) Sigma factors for cyanobacterial transcription. Gene Regul Syst Bio 3:65–87

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was partially supported by a Grant-in-Aid for Scientific Research (B) (no. 20310045).

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Correspondence to Takashi Yoshida.

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Honda, T., Takahashi, H., Sako, Y. et al. Gene expression of Microcystis aeruginosa during infection of cyanomyovirus Ma-LMM01. Fish Sci 80, 83–91 (2014). https://doi.org/10.1007/s12562-013-0685-7

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  • DOI: https://doi.org/10.1007/s12562-013-0685-7

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