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Dynamic of Virioplankton Abundance and Its Environmental Control in the Charente Estuary (France)

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Abstract

The Charente River provides nutrient- and virus-rich freshwater input to the Marennes Oléron Basin, the largest oyster-producing region in Europe. To evaluate virioplankton distribution in the Charente Estuary and identify which environmental variables control dynamic of virioplankton abundance, five stations defined by a salinity gradient (0–0.5, 0.6–5, 13–17, 20–24, and higher than 30 PSU) were surveyed over a year. Viral abundance was related to bacterioplankton abundance and activities, photosynthetic pigments, nutrient concentration, and physical parameters (temperature and salinity). On a spatial scale, virus displayed a decreasing pattern seaward with abundance ranging over the sampling period from 1.4 × 107 to 20.8 × 107 viruses mL−1 making virioplankton the most abundant component of planktonic microorganisms in the Charente Estuary. A good correlation was found between viral and bacterial abundance (r s = 0.85). Furthermore, bacterial abundance was the most important predictor of viral abundance explaining alone between 66% (winter) and 76% (summer) of viral variability. However, no relation existed between viral abundance and chlorophyll a. Temporal variations in viral distributions were mainly controlled by temperature through the control of bacterial dynamics. Spatial variations of viral abundance were influenced by hydrodynamic conditions especially during the winter season where virioplankton distribution was entirely driven by mixing processes.

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References

  1. MA Almeida MA Cunha F Alcantara (2001) ArticleTitleFactors influencing bacterial production in a shallow estuarine system Microb Ecol 42 416–426 Occurrence Handle1:CAS:528:DC%2BD38XkslQ%3D Occurrence Handle12024266

    CAS  PubMed  Google Scholar 

  2. MA Almeida MA Cunha F Alcantara (2001) ArticleTitleLoss of estuarine bacteria by viral infection and predation in microcosm conditions Microb Ecol 42 562–571 Occurrence Handle1:CAS:528:DC%2BD38XntFWqtQ%3D%3D Occurrence Handle12024239

    CAS  PubMed  Google Scholar 

  3. Aminot, A (1983) Mesure des matières en suspension, Manuel des analyses physico-chimiques en milieu marin (Aminot A and Chaussepied M), CNEXO, BNDO/Documentation, Brest, pp 169–175

  4. O Bergh KY Borsheim G Bratbak M Heldal (1989) ArticleTitleHigh abundance of viruses found in aquatic environments Nature 340 467–468 Occurrence Handle10.1038/340467a0 Occurrence Handle1:STN:280:DyaL1MzjtVGqsw%3D%3D Occurrence Handle2755508

    Article  CAS  PubMed  Google Scholar 

  5. G Billen P Servais S Becquevort (1990) ArticleTitleDynamics of bacterioplankton in oligotrophic and eutrophic aquatic environments: bottom-up or top-down control? Hydrobiologia 207 37–42 Occurrence Handle10.1007/BF00041438

    Article  Google Scholar 

  6. TL Bott (1975) ArticleTitleBacterial growth rates and temperature optima in a stream with a fluctuating thermal regime Limnol Oceanogr 20 191–197

    Google Scholar 

  7. G Bratbak M Heldal (1995) Viruses—the new players in the game: their ecological role could they mediate genetic exchange by transduction? I Joint (Eds) Molecular Ecology of Aquatic Microbes, vol 38 Springer-Verlag KG Berlin, Germany 249–264

    Google Scholar 

  8. G Bratbak TF Thingstad M Heldal (1994) ArticleTitleViruses and the microbial loop Microb Ecol 28 209–221 Occurrence Handle10.1007/BF00166811

    Article  Google Scholar 

  9. WP Cochlan J Wikner GF Steward DC Smith F Azam (1993) ArticleTitleSpatial distribution of viruses, bacteria and chlorophyll a in neritic, oceanic and estuarine environments Mar Ecol Prog Ser 92 77–87

    Google Scholar 

  10. PK Cochran JH Paul (1998) ArticleTitleSeasonal abundance of lysogenic bacteria in a subtropical estuary Appl Environ Microbiol 64 2308–2312 Occurrence Handle1:CAS:528:DyaK1cXjslWhtLo%3D Occurrence Handle9603858

    CAS  PubMed  Google Scholar 

  11. C Corinaldesi E Crevatin P Negro ParticleDel M Marini A Russo S Fonda-Umani R Danovaro (2003) ArticleTitleLarge-scale spatial distribution of virioplankton in the Adriatic Sea: testing the trophic state control hypothesis Appl Environ Microbiol 69 2664–2673 Occurrence Handle10.1128/AEM.69.5.2664-2673.2003 Occurrence Handle1:CAS:528:DC%2BD3sXjslOlsLo%3D Occurrence Handle12732535

    Article  CAS  PubMed  Google Scholar 

  12. MT Cottrell CA Suttle (1995) ArticleTitleDynamics of a lytic virus infecting the photosynthetic marine picoflagellate Micromonas pusilla Limnol Oceanogr 40 730–739

    Google Scholar 

  13. D Delmas MJ Garet (1995) ArticleTitleSDS-preservation for deferred measurement of exoproteolytic kinetics in marine samples J Microbiol Methods 22 243–248 Occurrence Handle10.1016/0167-7012(95)00008-9 Occurrence Handle1:CAS:528:DyaK2MXmvFCitbg%3D

    Article  CAS  Google Scholar 

  14. D Delmas C Legrand C Bechemin C Collinot (1994) ArticleTitleExoproteolytic activity determined by flow injection analysis: Its potential importance for bacterial growth in coastal marine ponds. Aquatic living resources/Ressources vivantes aquatiques Nantes 7 17–24

    Google Scholar 

  15. HW Ducklow CA Carlson (1992) Oceanic bacterial production KC Marshall (Eds) Advances in Microbial Ecology, vol 12 Plenum Press New York 207–217

    Google Scholar 

  16. HW Ducklow FK Shiah (1993) Estuarine bacterial production T Ford (Eds) Aquatic Microbiology: An Ecological Approach Blackwell London 261–284

    Google Scholar 

  17. JA Fuhrman (1999) ArticleTitleMarine viruses and their biogeochemical and ecological effects Nature 399 541–548 Occurrence Handle10.1038/21119 Occurrence Handle1:CAS:528:DyaK1MXjvFeiurk%3D Occurrence Handle10376593

    Article  CAS  PubMed  Google Scholar 

  18. JA Fuhrman F Azam (1982) ArticleTitleThymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results Mar Biol 66 109–120 Occurrence Handle10.1007/BF00397184

    Article  Google Scholar 

  19. JA Fuhrman CA Suttle (1993) ArticleTitleViruses in marine planktonic systems Oceanography 6 51–63

    Google Scholar 

  20. DR Garza CA Suttle (1995) ArticleTitleLarge double-stranded DNA viruses which causes the lysis of a marine heterotrophic nanoflagellate (Bodo sp.) occur in natural marine communities Aquat Microb Ecol 9 203–210

    Google Scholar 

  21. CJ Gobler DA Hutchins NS Fisher EM Cosper S Sanudo-Wilhelmy (1997) ArticleTitleRelease and bioavailability of C, N, P, Se and Fe following viral lysis of a marine Chrysophyte Limnol Oceanogr 42 1492–1504 Occurrence Handle1:CAS:528:DyaK1cXisVGhs7Y%3D Occurrence Handle10.4319/lo.1997.42.7.1492

    Article  CAS  Google Scholar 

  22. M Heldal G Bratbak (1991) ArticleTitleProduction and decay of viruses in aquatic environments Mar Ecol Prog Ser 72 205–212

    Google Scholar 

  23. I Hewson JM O'Neil JA Fuhrman WC Dennison (2001) ArticleTitleVirus-like particle distribution and abundance in sediments and overlying waters along eutrophication gradients in two subtropical estuaries Limnol Oceanogr 46 1734–1746 Occurrence Handle10.4319/lo.2001.46.7.1734

    Article  Google Scholar 

  24. HG Hoppe (1983) ArticleTitleSignificance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates Mar Ecol Prog Ser 11 299–308 Occurrence Handle1:CAS:528:DyaL3sXhvVGitbs%3D

    CAS  Google Scholar 

  25. SC Jiang JH Paul (1994) ArticleTitleSeasonal and diel abundance of viruses and occurrence of lysogeny/bacteriocinogeny in the marine environment Mar Ecol Prog Ser 104 163–172 Occurrence Handle10.3354/meps104163

    Article  Google Scholar 

  26. SC Jiang JH Paul (1998) ArticleTitleGene transfer by transduction in the marine environment Appl Environ Microbiol 64 2780–2787 Occurrence Handle1:CAS:528:DyaK1cXlsVKhsrw%3D Occurrence Handle9687430

    CAS  PubMed  Google Scholar 

  27. DL Kirchman MP Hoch (1988) ArticleTitleBacterial production in the Delaware Bay estuary estimated from thymidine and leucine incorporation rates Mar Ecol Prog Ser 45 169–178 Occurrence Handle1:CAS:528:DyaL1cXltlCmtrY%3D

    CAS  Google Scholar 

  28. DL Kirchman RG Keil M Simon NA Welschmeyer (1993) ArticleTitleBiomass and production of heterotrophic bacterioplankton in the oceanic subarctic Pacific Deep-Sea Res 40 967–988

    Google Scholar 

  29. S Lee JA Fuhrman (1987) ArticleTitleRelationships between biovolume and biomass of naturally derived marine bacterioplankton Appl Environ Microbiol 53 1298–1303 Occurrence Handle1:CAS:528:DyaL2sXksVGrtr4%3D Occurrence Handle16347362

    CAS  PubMed  Google Scholar 

  30. P Legendre L Legendre (1998) Numerical Ecology EditionNumber2nd English ed. Elsevier Science Amsterdam

    Google Scholar 

  31. CR Lovell A Konopka (1985) ArticleTitleThe effects of temperature on bacterial production in a dimictic eutrophic lake FEMS Microbiol Ecol 31 135–140 Occurrence Handle10.1016/0378-1097(85)90014-X Occurrence Handle1:CAS:528:DyaL28XhtVajsg%3D%3D

    Article  CAS  Google Scholar 

  32. R Maranger DF Bird (1995) ArticleTitleViral abundance in aquatic systems: a comparison between marine and fresh waters Mar Ecol Prog Ser 121 217–226

    Google Scholar 

  33. R Maranger DF Bird (1996) ArticleTitleHigh concentrations of viruses in the sediments of Lac Gilbert, Quebec Microb Ecol 31 141–151 Occurrence Handle10.1007/BF00167860

    Article  Google Scholar 

  34. M Middelboe NOG Jorgensen N Kroer (1996) ArticleTitleEffects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton Appl Environ Microbiol 62 1991–1997 Occurrence Handle16535334 Occurrence Handle1:STN:280:DC%2BC3crotlyhtA%3D%3D

    PubMed  CAS  Google Scholar 

  35. RT Noble JA Fuhrman (1998) ArticleTitleUse of SYBR Green I, for rapid epifluorescence counts of marine viruses and bacteria Aquat Microb Ecol 14 113–118

    Google Scholar 

  36. J Pages F Gadel (1990) ArticleTitleDissolved organic matter and UV absorption in a tropical hyperhaline estuary Sci Total Environ 99 173–204 Occurrence Handle10.1016/0048-9697(90)90222-G Occurrence Handle1:CAS:528:DyaK3MXmvVOgtg%3D%3D

    Article  CAS  Google Scholar 

  37. J Pages JP Torreton R Sempere (1997) ArticleTitleDissolved organic carbon in coral reef lagoons, by high temperature catalytic oxidation and UV spectrometry C R Acad Sci Paris Ser 2a 324 915–922 Occurrence Handle1:CAS:528:DyaK2sXks1WqsLc%3D

    CAS  Google Scholar 

  38. AV Palumbo RL Ferguson (1978) ArticleTitleDistribution of suspended bacteria in the Newport River Estuary, North Carolina Estuar Coast Mar Sci 7 251–259 Occurrence Handle10.1016/0302-3524(78)90062-2

    Article  Google Scholar 

  39. LM Proctor JA Fuhrman (1991) ArticleTitleRoles of viral infection in organic particle flux Mar Ecol Prog Ser 69 133–142

    Google Scholar 

  40. LM Proctor JA Fuhrman MC Ledbetter (1988) ArticleTitleMarine bacteriophages and bacterial mortality Eos 69 1111–1112

    Google Scholar 

  41. Ravail-Legrand, B (1993) Incidence des débits de la Charente sur la capacité biotique du bassin de Marennes-Oléron. PhD thesis. Université de Nantes, Nantes

  42. M Revilla A Iriarte I Madariaga E Orive (2000) ArticleTitleBacterial and phytoplankton dynamics along a trophic gradient in a shallow temperate estuary Estuar Coast Shelf Sci 50 297–313 Occurrence Handle10.1006/ecss.1999.0576

    Article  Google Scholar 

  43. GE Schultz H Ducklow (2000) ArticleTitleChanges in bacterioplankton metabolic capabilities along a salinity gradient in the York River estuary, Virginia, USA Aquat Microb Ecol 22 163–174

    Google Scholar 

  44. FK Shiah HW Ducklow (1994) ArticleTitleTemperature and substrate regulation of bacterial abundance, production and specific growth rate in Chesapeake Bay, USA Mar Ecol Prog Ser 103 297–308

    Google Scholar 

  45. GS Stent (1963) Molecular Biology of Bacterial Viruses Freeman and Company San Francisco

    Google Scholar 

  46. GF Steward DC Smith F Azam (1996) ArticleTitleAbundance and production of bacteria and viruses in the Bering and Chukchi Seas Mar Ecol Prog Ser 131 287–300

    Google Scholar 

  47. Strickland, JDH, Parsons, TR (1972) A practical handbook of seawater analysis. Bull Fish Res Board Can 167

  48. CA Suttle (1994) ArticleTitleThe significance of viruses to mortality in aquatic microbial communities Microb Ecol 28 237–243 Occurrence Handle10.1007/BF00166813

    Article  Google Scholar 

  49. CA Suttle (1999) The ecological, evolutionary and geochemical consequences of viral infection of cyanobacteria and eukaryotic algae C Hurst (Eds) Viral Ecology Academic Press New York

    Google Scholar 

  50. CA Suttle AM Chan (1994) ArticleTitleDynamics and distribution of cyanophages and their effect on marine Synechococcus spp Appl Environ Microbiol 60 3167–3174 Occurrence Handle16349372 Occurrence Handle1:STN:280:DC%2BC3crot1Oksw%3D%3D

    PubMed  CAS  Google Scholar 

  51. CA Suttle F Chen (1992) ArticleTitleMechanisms and rates of decay of marine viruses in seawater Appl Environ Microbiol 58 3721–3729 Occurrence Handle16348812 Occurrence Handle1:STN:280:DC%2BC3crot1aisQ%3D%3D

    PubMed  CAS  Google Scholar 

  52. BG Tabachnick LS Fidell (2001) Using Multivariate Statistics, vol 60 EditionNumber3 Allyn and Bacon Boston

    Google Scholar 

  53. TF Thingstad M Heldal G Bratbak I Dundas (1993) ArticleTitleAre viruses important partners in pelagic food webs? Trends Ecol Evol 8 209–212 Occurrence Handle10.1016/0169-5347(93)90101-T

    Article  Google Scholar 

  54. M Troussellier H Schafer N Batailler L Bernard C Courties P Lebaron G Muyzer P Servais J Vives Rego (2002) ArticleTitleBacterial activity and genetic richness along an estuarine gradient (Rhone River plume, France) Aquat Microb Ecol 28 13–24

    Google Scholar 

  55. M Weinbauer M Höfle (1998) ArticleTitleSignificance of viral lysis and flagellate grazing as factors controlling bacterioplankton in a eutrophic lake Appl Environ Microbiol 64 431–438 Occurrence Handle1:CAS:528:DyaK1cXpsVSltg%3D%3D Occurrence Handle16349497

    CAS  PubMed  Google Scholar 

  56. MG Weinbauer D Fuks S Puskaric P Peduzzi (1995) ArticleTitleDiel, seasonal, and depth-related variability of viruses and dissolved DNA in the northern Adriatic Sea Microb Ecol 30 25–41 Occurrence Handle10.1007/BF00184511

    Article  Google Scholar 

  57. PA White J Kalff JB Rasmussen JM Gasol (1991) ArticleTitleThe effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats Microb Ecol 21 99–118

    Google Scholar 

  58. SW Wilhelm CA Suttle (1999) ArticleTitleViruses and nutrient cycles in the sea Bioscience 49 781–788

    Google Scholar 

  59. KE Wommack RR Colwell (2000) ArticleTitleViruses in aquatic ecosystems Microbiol Mol Biol Rev 64 69–114 Occurrence Handle1:STN:280:DC%2BD3c7ntF2jsw%3D%3D Occurrence Handle10704475

    CAS  PubMed  Google Scholar 

  60. KE Wommack RT Hill M Kessel E Russek-Cohen RR Colwell (1992) ArticleTitleDistribution of viruses in the Chesapeake Bay Appl Environ Microbiol 58 2965–2970 Occurrence Handle1:STN:280:DyaK3s%2Fntlyquw%3D%3D Occurrence Handle1444409

    CAS  PubMed  Google Scholar 

  61. CS Yentsch DW Menzel (1963) ArticleTitleA method for the determination of phytoplankton chlorophyll and pheophytin by fluorescence Deep-Sea Res 10 221–231 Occurrence Handle1:CAS:528:DyaF3sXkvVelu78%3D

    CAS  Google Scholar 

  62. JH Zar (1999) Biostatistical Analysis EditionNumber4 Prentice Hall Upper Saddle River, NJ

    Google Scholar 

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Acknowledgments

This work was supported by grants coming from the French Programme National en Environnement Côtier (PNEC, ART 5), the Contrat de Plan Etat Région (CPER 2000–2003), and the Conseil Général de Charente-Maritime (PhD grant to J.C. Auguet). We gratefully acknowledge F. Mornet for nutrients analysis, D. Munaron, and the DIREN Bordeaux for river discharge data.

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  1. Laboratoire de Biologie et Environnements Marins (LBEM), FRE 2727 CNRS-Université de La Rochelle, Avenue Michel Crépeau, 17042, La Rochelle, France

    J. C. Auguet, H. Montanié, H. J. Hartmann & V. Huet

  2. Centre de Recherche sur les Ecosystèmes Marins et Aquacoles (CREMA, UMR 10), CNRS-IFREMER, BP5, 17137, L'Houmeau, France

    J. C. Auguet & D. Delmas

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  1. J. C. Auguet
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Correspondence to J. C. Auguet.

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Auguet, J.C., Montanié, H., Delmas, D. et al. Dynamic of Virioplankton Abundance and Its Environmental Control in the Charente Estuary (France). Microb Ecol 50, 337–349 (2005). https://doi.org/10.1007/s00248-005-0183-2

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