Microbial Ecology

, Volume 52, Issue 2, pp 217–225 | Cite as

Environmental Factors that influence the Transition from Lysogenic to Lytic Existence in the ϕHSIC/Listonella pelagia Marine Phage–Host System

  • S. J. Williamson
  • J. H. PaulEmail author


The marine phage ϕHSIC has been previously reported to enter into a pseudolysogenic-like interaction with its host Listonella pelagia. This phage–host system displays behaviors that are characteristic of both pseudolysogeny and lysogeny including a high rate of spontaneous induction and chromosomal integration of the prophage. To determine what parameters may influence the transition from lysogenic to lytic existence in the ϕHSIC/L. pelagia phage–host system, cultures of this organism were incubated under different environmental conditions, while host cell growth and bacteriophage production were monitored. The environmental parameters tested included salinity, temperature, a rapid temperature shift, and degree of culture aeration. The highest titers of phage were produced by HSIC-1a cells grown in high-salinity nutrient artificial seawater media (67 ppt with a natural salinity equivalent of 57 ppt) or those cultured in highly aerated nutrient artificial seawater media (cultures shaken at 300 rpm). Conversely, the lowest titers of phage were produced under low salinity or rate of aeration. In general, conditions that stimulated growth resulted in greater lytic phage production, whereas slow growth favored lysogeny. These results indicate that elevated salinity and aeration influenced the switch from lysogenic to lytic existence for the phage ϕHSIC. These results may have implications for environmental controls of the lysogenic switch in natural populations of marine bacteria.


Optical Density Ratio Host System Repressor Protein Lytic Infection Initial Growth Rate 
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This research was supported by a grant from the National Science Foundation no. 0221763.


  1. 1.
    Ackermann, HW, DuBow, MS (1987) Viruses of Prokaryotes: General Properties of Bacteriophages. CRC Press, Inc, Boca Raton, FLGoogle Scholar
  2. 2.
    Aggarwal, AK, Rodgers, DW, Drottar, M, Ptashne, M, Harrison, SC (1988) Recognition of a DNA operator by the repressor of phage 434: a view at high resolution. Science 242: 899–907PubMedCrossRefGoogle Scholar
  3. 3.
    Bell, AC, Koudelka, GB (1993) Operator sequence context influences amino acid–base-pair interactions in 434 repressor–operator complexes. J Mol Biol 234: 542–553PubMedCrossRefGoogle Scholar
  4. 4.
    Bratbak, G, Egge, JK, Heldal, M (1993) Viral mortality of the marine alga Emiliania huxleyi (haptophyceae) and termination of algal blooms. Mar Ecol Prog Ser 93: 39–48CrossRefGoogle Scholar
  5. 5.
    Cochran, PK, Paul, JH (1998) Seasonal abundance of lysogenic bacteria in a subtropical estuary. Appl Environ Microbiol 64: 2308PubMedGoogle Scholar
  6. 6.
    Gupta, A, Rao, G (2003) A study of oxygen transfer in shake flasks using a non-invasive oxygen sensor. Biotechnol Bioeng 84: 351–358PubMedCrossRefGoogle Scholar
  7. 7.
    Jana, NK, Roy, S, Bhattacharyya, B, Mandal, NC (1999) Amino acid changes in the repressor of bacteriophage lambda due to temperature-sensitive mutations in its cI gene and the structure of a highly temperature-sensitive mutant repressor. Protein Eng 12: 225–233PubMedCrossRefGoogle Scholar
  8. 8.
    Jiang, SC, Kellogg, CA, Paul, JH (1998) Characterization of marine temperate phage–host systems isolated from Mamala Bay, Hawaii. Appl Environ Microbiol 64: 535–542PubMedGoogle Scholar
  9. 9.
    Koudelka, GB, Carlson, P (1992) DNA twisting and the effects of non-contacted bases on affinity of 434 operator and 434 repressor. Nature 355: 89–91PubMedCrossRefGoogle Scholar
  10. 10.
    Koudelka, GB, Harbury, P, Harrison, SC, Ptahsne, M (1988) DNA twisting and the affinity of bacteriophage 434 operator for bacteriophage 434 repressor. Proc Natl Acad Sci USA 85: 4633–4637PubMedCrossRefGoogle Scholar
  11. 11.
    McDaniel, L, Houchin, LA, Williamson, SJ, Paul, JH (2002) Lysogeny in marine Synechococcus. Nature 415: 496PubMedCrossRefGoogle Scholar
  12. 12.
    McDaniel, LE, Bailey, EG (1969) Effect of shaking speed and type of closure on shake flask cultures. Appl Microbiol 17: 286–290PubMedGoogle Scholar
  13. 13.
    Moebus, K (1997) Investigations of the marine lysogenic bacterium H24.1. General description of the phage–host system. Mar Ecol Prog Ser 148: 217–228CrossRefGoogle Scholar
  14. 14.
    Mukhopadhyay, B, Marshall-Batty, KR, Kim, BD, O'Handley, D, Nakai, H (2003) Modulation of phage Mu repressor DNA binding and degradation by distinct determinants in its C-terminal domain. Mol Microbiol 47: 171–182PubMedCrossRefGoogle Scholar
  15. 15.
    Paul, JH (1982) Use of hoechst dyes 33258 and 33342 for enumeration of attached and planktonic bacteria. Appl Environ Microbiol 43: 939–944PubMedGoogle Scholar
  16. 16.
    Paul, JH, Williamson, SJ, Long, A, Authement, RN, John, D, Segall, AM, Rohwer, FL, Androlewicz, M, Patterson, S (2005) Complete genome sequence of phiHSIC, a pseudotemperate marine phage of Listonella pelagia. Appl Environ Microbiol 71: 3311–3320PubMedCrossRefGoogle Scholar
  17. 17.
    Ptashne, M (1992) A Genetic Switch, 2nd edn. Cell Press and Blackwell Scientific Publications, Cambridge, MA, pp 20–24Google Scholar
  18. 18.
    Ptashne, M, Jeffery, A, Johnson, AD, Maurer, R, Meyer, BJ, Pabo, CO, Roberts, TM, Sauer, RT (1980) How the lambda repressor and cro work. Cell 19: 1–19PubMedCrossRefGoogle Scholar
  19. 19.
    Rai, SS, O'Handley, D, Nakai, H (2001) Conformational dynamics of a transposition repressor in modulating DNA binding. J Mol Biol 312: 311–322PubMedCrossRefGoogle Scholar
  20. 20.
    Shimon, LJ, Harrison, SC (1993) The phage 434 OR2/R1-69 complex at 2.5 A resolution. J Mol Biol 232: 826–838PubMedCrossRefGoogle Scholar
  21. 21.
    Snyder, L, Champness, W (1997) Molecular Genetics of Bacteria. ASM Press, Washington, DCGoogle Scholar
  22. 22.
    Tuomi, P, Fagerbakke, KM, Bratbak, G, Heldal, M (1995) Nutritional enrichment of a microbial community: the effects on activity, elemental composition, community structure and virus production. FEMS Microbiol Ecol 16: 123–134CrossRefGoogle Scholar
  23. 23.
    Vasala, A, Panula, J, Bollok, M, Illmann, L, Halsig, C, Neubauer, P (2006) A new wireless system for decentralised measurement of physiological parameters from shake flasks. Microb Cell Fact 5: 8PubMedCrossRefGoogle Scholar
  24. 24.
    Weaver, RF (1999) Molecular Biology. WCB/McGraw-Hill, Boston, MAGoogle Scholar
  25. 25.
    Weinbauer, MG, Brettar, I, Hofle, MG (2003) Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol Oceanogr 48: 1457–1465CrossRefGoogle Scholar
  26. 26.
    Williamson, SJ, Houchin, LA, McDaniel, L, Paul, JH (2002) Seasonal variation in lysogeny as depicted by prophage induction in Tampa Bay, Florida. Appl Environ Microbiol 68: 4307–4314PubMedCrossRefGoogle Scholar
  27. 27.
    Williamson, SJ, McLaughlin, MR, Paul, JH (2001) Interaction of the phi HSIC virus with its host: lysogeny or pseudolysogeny. Appl Environ Microbiol 67: 1682–1688PubMedCrossRefGoogle Scholar
  28. 28.
    Williamson, SJ, Paul, JH (2004) Nutrient stimulation of lytic phage production in bacterial populations of the Gulf of Mexico. Aquat Microb Ecol 36: 9–17CrossRefGoogle Scholar
  29. 29.
    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: 506–516CrossRefGoogle Scholar
  30. 30.
    Wilson, WH, Mann, NH (1997) Lysogenic and lytic viral production in marine microbial communities. Aquat Microb Ecol 13: 95–100CrossRefGoogle Scholar
  31. 31.
    Wood, HE, Devine, KM, McConnell, DJ (1990) Characterization of a repressor gene (xre) and a temperature-sensitive allele from the Bacillus subtilis prophage, PBSX. Gene 96: 83–88PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.J. Craig Venter InstituteRockvilleUSA
  2. 2.College of Marine ScienceUniversity of South FloridaSt. PetersburgUSA

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