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Characterization of Lysogens in Bacterioplankton Assemblages of the Southern California Borderland

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Abstract

Viruses cause significant mortality of marine microorganisms; however, their role in shaping the composition of microbial assemblages has not been fully elucidated. Because viruses may form lysogenic relationships with their hosts, temperate viruses may influence bacterial assemblage structures through direct lysis of hosts when induced by environmental stimuli or by homoimmunity (i.e., immunity to closely related viruses). We investigated the components of bacterioplankton assemblages that bore prophage using the lysogenic induction agent mitomycin C. Seawater was collected at two locations (the San Pedro Ocean Time Series Station and in the Santa Barbara Channel) in the Southern California Borderland and amended with mitomycin C. After 24-h incubation, the community structure of bacterioplankton was compared with unamended controls using automated rRNA intergenic spacer analysis. The addition of mitomycin C to seawater had effects on the community structure of bacterioplankton, stimulating detectable overall diversity and richness of fingerprints and causing the assemblages within incubations to become different to control assemblages. Most negatively impacted operational taxonomic units (OTU) in mitomycin C-amended incubations individually comprised a large fraction of total amplified DNA in initial seawater (5.3–23.3% of amplified DNA fluorescence) fingerprints, and data suggest that these include organisms putatively classified as members of the γ-Proteobacteria, SAR11 cluster, and Synechococcus groups. The stimulation of assemblage richness by induction of lysogens, and the reduction in the contribution to total DNA of common OTU (and concomitant increase in rare OTU), suggests that temperate phage have the potential to strongly influence the diversity of bacterioplankton assemblages. Because lysogenic OTU may also be resistant to closely related lytic (i.e., free-living) viruses, the impact of lytic virioplankton on assemblages may only be pronounced transiently or when conditions causing lysogenic induction arise.

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References

  1. Ackermann, HW, DuBow, MS (1987) General Properties of Bacteriophages, 1st ed, vol. 1., CRC Press, Boca Raton, FL

    Google Scholar 

  2. Bisen, PS, Audholia, S, Bhatnagar, AK, Bagchi, SN (1986) Evidence for lysogeny and viral resistance in the cyanobacterium Phormidium uncinatum. Curr Microbiol 13: 1–6

    Article  Google Scholar 

  3. Bratbak, G, Heldal, M, Thingstad, TF, Riemann, B, Haslund, OH (1992) Incorporation of viruses into the budget of microbial C-transfer. A first approach. Mar Ecol, Prog Ser 83: 273–280

    Google Scholar 

  4. Brown, MV, Schwalbach, MS, Hewson, I, Fuhrman, JA (2005) Coupling 16S-ITS rDNA clone libraries and ARISA to show marine microbial diversity: development and application to a time series. Environ Microbiol 7: 1466–1479

    Article  PubMed  CAS  Google Scholar 

  5. Cardinale, M, Brusetti, L, Quatrini, P, Borin, S, Puglia, AM, Rizzi, A, Zanardini, E, Sorlini, C, Corselli, C, Daffonchio, D (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70: 6147–6156

    Article  PubMed  CAS  Google Scholar 

  6. Cochran, PK, Kellogg, CA, Paul, JH (1998) Prophage induction of indigenous marine lysogenic bacteria by environmental pollutants. Mar Ecol, Prog Ser 164: 125–133

    CAS  Google Scholar 

  7. Crosby, LD, Criddle, CS (2003) Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. Biotechniques 34: 790–802

    PubMed  CAS  Google Scholar 

  8. Danovaro, R, Corinaldesi, C (2003) Sunscreen products increase virus production through prophage induction in marine bacterioplankton. Microb Ecol 45: 109–118

    Article  PubMed  CAS  Google Scholar 

  9. Fuhrman, JA (1992) Bacterioplankton roles in cycling of organic matter: The Microbial food web. In: Falkowski, PG, Woodhead, AD (Eds.) Primary Productivity and Biogeochemical Cycles in the Sea. Plenum Press, New York

    Google Scholar 

  10. Fuhrman, JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399: 541–548

    Article  PubMed  CAS  Google Scholar 

  11. Fuhrman, JA, Comeau, DE, Hagstrom, A, Chan, AM (1988) Extraction of DNA suitable for molecular biological studies from natural planktonic microorganisms. Appl Environ Microbiol 54: 1426–1429

    PubMed  CAS  Google Scholar 

  12. Fuhrman, JA, McCallum, K, Davis AA (1993) Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific Oceans. Appl Environ Microbiol 59: 1294–1302

    PubMed  CAS  Google Scholar 

  13. Fuhrman, JA, Ouverney, CC (1998) Marine microbial diversity studied via 16S rRNA sequences: cloning results from coastal waters and counting of native Archaea with fluorescent single cell probes. Aquat Ecol 32: 3–15

    Article  CAS  Google Scholar 

  14. Fuhrman, JA, Suttle, CA (1993) Viruses in marine planktonic systems. Oceanography 6: 51–63

    Google Scholar 

  15. Garcia-Martinez, J, Rodriguez-Valera, F (2000) Microdiversity of uncultured marine prokaryotes: the SAR11 cluster and the marine Archaea of Group 1. Mol Ecol 9: 935–948

    Article  PubMed  CAS  Google Scholar 

  16. Giovannoni, SJ, Britschgi, TB, Moyer, CL, Field, KG (1990) Genetic diversity in Sargasso Sea bacterioplankton. Nature 345: 60–63

    Article  PubMed  CAS  Google Scholar 

  17. Giovannoni, SJ, Rappe, M (2000) Evolution, diversity and molecular ecology of marine prokaryotes, In: Kirchman DL (Ed.) Microbial Ecology of the Oceans. Wiley-Liss, New York, p. 47–84

    Google Scholar 

  18. Hewson, I, Fuhrman, JA (2004) Bacterioplankton species richness and diversity along an estuarine gradient in Moreton Bay, Australia. Appl Environ Microbiol 70: 3425–3433

    Article  PubMed  CAS  Google Scholar 

  19. Hewson, I, Fuhrman, JA (2006) Viral impacts upon marine bacterioplankton assemblage structure. J Mar Biol Assoc UK 86: 577–589

    Article  CAS  Google Scholar 

  20. Hewson, I, Fuhrman, JA (2006) Improved strategy for comparing microbial assemblage fingerprints. Microb Ecol 51: 147–153

    Article  PubMed  Google Scholar 

  21. Hewson, I, Fuhrman, JA (2006) Spatial and vertical biogeography of coral reef sediment bacterial and diazotroph communities. Mar Ecol, Prog Ser 306: 79–86

    CAS  Google Scholar 

  22. Hewson, I, Govil, SR, Capone, DG, Carpenter, EJ, Fuhrman, JA (2004) Evidence for Trichodesmium viral lysis and potential significance for biogeochemical cycling in the oligotrophic ocean. Aquat Microb Ecol 36: 1–8

    Google Scholar 

  23. Hewson, I, O’Neil, JM, Dennison, WC (2001) Virus-like particles associated with Lyngbya majuscula (Cyanophyta; Oscillatoriacea) bloom decline in Moreton Bay, Australia. Aquat Microb Ecol 25: 207–213

    Google Scholar 

  24. Hewson, I, O’Neil, JM, Heil, CA, Bratbak, G, Dennison, WC (2001) Effects of concentrated natural viral communities on photosynthesis and community composition of co-occuring benthic microalgae and phytoplankton. Aquat Microb Ecol 25: 1–10

    Google Scholar 

  25. Hewson, I, Vargo, GA, Fuhrman, JA (2003) Bacterial diversity in shallow oligotorphic marine benthos and overlying waters: effects of virus infection, containment and nutrient enrichment. Microb Ecol 46: 322–336

    Article  PubMed  CAS  Google Scholar 

  26. Jiang, S, Fu, W, Chu, W, Fuhrman, JA (2003) The vertical distribution and diversity of marine bacteriophage at a station off Southern California. Microb Ecol 45: 399–410

    Article  PubMed  CAS  Google Scholar 

  27. Jiang, SC, Kellogg, CA, Paul, JH (1998) Characterization of marine temperate phage–host systems isolated from Mamala Bay, Oahu, Hawaii. Appl Environ Microbiol 64: 535–542

    PubMed  CAS  Google Scholar 

  28. Jiang, SC, Paul, JH (1996) Occurrence of lysogenic bacteria in marine microbial communities as determined by prophage induction. Mar Ecol, Prog Ser 142: 27–38

    Google Scholar 

  29. Jiang, SC, Paul, JH (1994) Seasonal and diel abundance of viruses and occurrence of lysogeny/bacteriocinogeny in the marine environment. Mar Ecol, Prog Ser 104: 163–172

    Article  Google Scholar 

  30. Legendre, P, Legendre, L (1998) Numerical Ecology, vol. 1. Elsevier, Amsterdam

    Google Scholar 

  31. Lenski, RE (1988) Dynamics of interactions between bacteria and virulent bacteriophage. Adv Microb Ecol 10: 1–44

    CAS  Google Scholar 

  32. Lenski, RE (1988) Experimental studies of pleiotropy and epistasis in Escherichia coli. 1. Variation in competitive fitness among mutants resistant to virus T4. Evolution 42: 425–432

    Article  Google Scholar 

  33. Lenski, RE (1988) Experimental studies of pleiotropy and epistasis in Escherichia coli. 2. Compensation for maladaptive effects associated with resistance to virus T4. Evolution 42: 433–440

    Article  Google Scholar 

  34. Leuders, T, Friedrich, MW (2003) Evaluation of PCR amplification bias by terminal restriction fragment length polymorphism analysis of small-subunit rRNA and mcrA genes by using defined template mixtures of methanogenic pure cultures and soil DNA extracts. Appl Environ Microbiol 69: 320–326

    Article  CAS  Google Scholar 

  35. Levin, BR, Lenski, RE (1983) Coevolution in bacteria and their viruses and plasmids. In: Futuyma, DJ Slatkin, M (Eds.) Coevolution. Sinauer, Sunderland, MA

    Google Scholar 

  36. McDaniel, L, Houchin, LA, Williamson, SJ, Paul, JH (2002) Lysogeny in marine Synechococcus. Nature 415: 496

    Article  PubMed  CAS  Google Scholar 

  37. Morris, RM, Rappé, M, Connon, SA, Vergin, KL, Siebold, WA, Carlson, CA, Giovannoni, SJ (2002) SAR11 clade dominated ocean surface bacterioplankton communities. Nature 420: 806–810

    Article  PubMed  CAS  Google Scholar 

  38. Noble, RT, Fuhrman, JA (1998) Use of SYBR Green I rapid epifluoresence counts of marine viruses and bacteria. Aquat Microb Ecol 14: 113–118

    Google Scholar 

  39. Rappé, M, Connon, SA, Vergin, KL, Giovannoni, SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418: 630–633

    Article  PubMed  CAS  Google Scholar 

  40. Schwalbach, MS, Hewson, I, Fuhrman, JA (2004) Viral effects on bacterial community composition in marine plankton microcosms. Aquat Microb Ecol 34: 117–127

    Google Scholar 

  41. Simu, K, Hagstrom, A (2004) Oligotrophic bacterioplankton with a novel single-cell life strategy. Appl Environ Microbiol 70: 2445–2451

    Article  PubMed  CAS  Google Scholar 

  42. Sode, K, Oonari, R, Oozeki, M (1997) Induction of a temperate marine cyanophage by heavy metal. J Mar Biotechnol 5: 178–180

    CAS  Google Scholar 

  43. Sokal, RR, Rohlf, FJ (1995) Biometry. The Principles and Practice of Statistics in Biological Research, vol. 3. Freeman, New York

    Google Scholar 

  44. Stolt, P, Zillig, W (1994) Transcription of the halophage phiH repressor gene is abolished by transcription from an inversely oriented lytic promoter. FEBS Lett 344: 125–128

    Article  PubMed  CAS  Google Scholar 

  45. Sullivan, MB, Waterbury, JB, Chisholm, SW (2003) Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424: 1047–1051

    Article  PubMed  CAS  Google Scholar 

  46. 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

    Google Scholar 

  47. Suttle, CA, Chan, AM, Cottrell, MT (1990) Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347: 467–469

    Article  Google Scholar 

  48. Suzuki, MT, Giovannoni, SJ (1996) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62: 625–630

    PubMed  CAS  Google Scholar 

  49. Suzuki, MT, Rappé, M, Giovannoni, SJ (1998) Kinetic bias in estimates of picoplankton community structure obtained by measurements of small-subunit rRNA gene PCR amplicon length heterogeneity. Appl Environ Microbiol 64: 4522–4529

    PubMed  CAS  Google Scholar 

  50. Thingstad, TF (2000) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45: 1320–1328

    Article  Google Scholar 

  51. Thingstad, TF, Lignell, R (1997) A theoretical approach to the question of how trophic interactions control carbon demand, growth rate, abundance and diversity. Aquat Microb Ecol 13: 19–27

    Google Scholar 

  52. Venter, JC, Remington, K, Heidelberg, JF, Halpern, AL, Rusch, D, Eisen, JA, Wu, D, Paulsen, I, Nelson, KE, Nelson, W, Fouts, DE, Levy, S, Knap, AH, Lomas, MW, Nealson, K, White, O, Peterson, J, Hoffman, J, Parsons, R, Baden-Tillson, H, Pfannkock, C, Rogers, Y, Smith, HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66–74

    Article  PubMed  CAS  Google Scholar 

  53. Waterbury, JB, Valois, FW (1993) Resistance to co-occurring phages enables marine Synechococus communities to coexist with cyanophages abundant in seawater. Appl Environ Microbiol 59: 3393–3399

    PubMed  CAS  Google Scholar 

  54. Weinbauer, MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28: 127–181

    Article  PubMed  CAS  Google Scholar 

  55. Weinbauer, MG, Brettar, I, Hofle, MG (2003) Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol Oceanogr 48: 1457–1465

    Article  Google Scholar 

  56. Weinbauer, MG, Suttle, CA (1996) Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the Gulf of Mexico. Appl Environ Microbiol 62: 4374–4380

    PubMed  CAS  Google Scholar 

  57. Wen, K, Ortmann, A, Suttle, C (2004) Accurate estimation of viral abundance by epifluorescence microscopy. Appl Environ Microbiol 70: 3862–3867

    Article  PubMed  CAS  Google Scholar 

  58. Whittaker, RH (1952) A study of summer foliage insect communities in the Great Smoky Mountains. Ecol Monogr 22: 1–44

    Article  Google Scholar 

  59. Wilcox, RM, Fuhrman, JA (1994) Bacterial viruses in coastal seawater: lytic rather than lysogenic production. Mar Ecol, Prog Ser 114: 35–45

    Google Scholar 

  60. 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: 4307–4314

    Article  PubMed  CAS  Google Scholar 

  61. Williamson, SJ, McLaughlin, MR, Paul, JH (2001) Interaction of the phiHSIC virus with its host: lysogeny or pseudolysogeny. Appl Environ Microbiol 67: 1682–1688

    Article  PubMed  CAS  Google Scholar 

  62. Williamson, SJ, Paul, JH (2004) Nutrient stimulation of lytic phage production in bacterial populations of the Gulf of Mexico. Aquat Microb Ecol 36: 9–17

    Google Scholar 

  63. Wilson, WH, Francis, I, Ryan, K, Davy, SK (2001) Temperature induction of viruses in symbiotic dinoflagellates. Aquat Microb Ecol 25: 99–102

    Google Scholar 

  64. Wilson, WH, Mann, NH (1997) Lysogenic and lytic viral production in marine microbial communities. Aquat Microb Ecol 13: 95–100

    Google Scholar 

  65. Winter, C, Smit, A, Herndl, GJ, Weinbauer, MG (2004) Impact of virioplankton on archaeal and bacterial community richness as assessed in seawater batch cultures. Appl Environ Microbiol 70: 803–813

    Article  CAS  Google Scholar 

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Acknowledgments

The authors wish to thank M. Schwalbach, J. Steele, A. Patel, E. Royker, L. Sargsyan, and the crew of the R/V Point Sur for their assistance with field work. Helpful comments were provided on an early manuscript draft by D. Caron, D. Keifer, D. Capone, and D. Hammond. Helpful conversations on interpretation were conducted with J. Zehr. This research was supported by National Science Foundation grant OCE0241723 awarded to J.A. Fuhrman and grant MCB0084231 awarded to J.A.F. and D. Caron. The work is in partial fulfillment of a Ph.D. by I. Hewson at the University of Southern California.

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  1. Ian Hewson

    Present address: Department of Ocean Sciences, University of Southern California, Santa Cruz, 1156 High St E & MS D446, Santa Cruz, CA, 90089-0371, USA

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  1. Wrigley Institute for Environmental Studies, University of Southern California, 3616 Trousdale Pkwy AHF 107, Los Angeles, CA, 90089-0371, USA

    Ian Hewson & Jed A. Fuhrman

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Hewson, I., Fuhrman, J.A. Characterization of Lysogens in Bacterioplankton Assemblages of the Southern California Borderland. Microb Ecol 53, 631–638 (2007). https://doi.org/10.1007/s00248-006-9148-3

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