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Diel and Seasonal Variations in Abundance, Activity, and Community Structure of Particle-Attached and Free-Living Bacteria in NW Mediterranean Sea

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Abstract

Diel and seasonal variations in abundance, activity, and structure of particle-attached vs free-living bacterial communities were investigated in offshore NW Mediterranean Sea (0–1000 m). Attached bacteria were always less abundant and less diverse but generally more active than free-living bacteria. The most important finding of this study was that the activity of attached bacteria showed pronounced diel variations in the upper mixed water column with higher activities at night. Under mesotrophic conditions, the contribution of attached bacteria to total bacterial activity increased from less than 10% at day time to 83% at night time. At high chlorophyll a concentration, the highest cell-specific activities and contribution to total bacterial activity were due to free-living bacteria at day and to attached bacteria at night. Under summer oligotrophic conditions, free-living bacteria dominated and contributed to the most important part of the bacterial activity at both day and night, whereas attached bacteria were much less abundant but presented the highest cell-specific activities. These diel and seasonal variations in activities were concomitant to changes in bacterial community structure, mainly in the upper layer. The number of attached ribotypes was fairly constant suggesting that particles are colonized by a relatively limited number of ubiquitous ribotypes. Most of these ribotypes were also free-living ribotypes suggesting that attached bacteria probably originate from colonization of newly formed particles by free-living bacteria in the upper layer. These results reinforce the biogeochemical role of attached bacteria in the cycling of particulate organic carbon in the NW Mediterranean Sea and the importance of diel variability in these processes.

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References

  1. Aas, P, Lyons, MM, Pledger, R, Mitchell, DL, Jeffrey, WH (1996) Inhibition of bacterial activities by solar radiation in nearshore waters and the Gulf of Mexico. Aquat Microb Ecol 11: 229–238

    Google Scholar 

  2. Acinas, SG, Anton, J, Rodriguez-Valera, F (1999) Diversity of free-living and attached bacteria in offshore western Mediterranean waters as depicted by analysis of genes encoding 16S rRNA. Appl Environ Microbiol 65: 514–522

    PubMed  CAS  Google Scholar 

  3. Acinas, SG, Rodriguez-Valera, F, Pedros-Alio, C (1997) Spatial and temporal variation in marine bacterioplankton diversity as shown by RFLP fingerprinting of PCR amplified 16S rDNA. FEMS Microbiol Ecol 24: 27–40

    Article  CAS  Google Scholar 

  4. Alldredge, AL, Gotschalk, C (1990) The relative contribution of marine snow of different origins to biological processes in coastal waters. Cont Shelf Res 10: 41–58

    Article  Google Scholar 

  5. Andersen, V, Prieur, L (2000) One-month study in the open NW Mediterranean Sea (DYNAPROC experiment, May 1995): overview of the hydrobiogeochemical structures and effects of wind events. Deep-Sea Res II 47: 397–422

    Article  CAS  Google Scholar 

  6. Arrieta, JM, Weinbauer, MG, Lute, C, Herndl, GJ (2004) Response of bacterioplankton to iron fertilization in the Southern Ocean. Limnol Oceanogr 49: 799–808

    CAS  Google Scholar 

  7. Azam, F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280: 694–696

    Article  CAS  Google Scholar 

  8. Azam, F, Fenchel, T, Field, JG, Gray, JS, Meyer-Reil, LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10: 257–263

    Google Scholar 

  9. Bligh, EG, Dyer, W (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37: 911–917

    PubMed  CAS  Google Scholar 

  10. Brosius, J, Dull, TJ, Sleeter, DD, Noller, HF (1981) Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. J Mol Biol 148: 107–127

    Article  PubMed  CAS  Google Scholar 

  11. Cauwet, G (1994) HTCO method for dissolved organic carbon analysis in seawater: influence of catalyst on blank estimation. Mar Chem 47: 5564

    Article  Google Scholar 

  12. Cho, BC, Azam, F (1988) Major role of bacteria in biogeochemical fluxes in the ocean’s interior. Nature 332: 441–443

    Article  CAS  Google Scholar 

  13. Cole, JJ, Findlay, S, Pace, ML (1988) Bacterial production in fresh and saltwater ecosystems: a cross-system over-view. Mar Ecol Prog Ser 43: 1–10

    Google Scholar 

  14. Covert, JS, Moran, MA (2001) Molecular characterization of estuarine bacterial communities that use high- and low molecular weight fractions of dissolved organic carbon. Aquat Microb Ecol 25: 127–139

    Google Scholar 

  15. Crump, BC, Armbrust, EV, Baross, JA (1999) Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl Environ Microbiol 65: 3192–3204

    PubMed  CAS  Google Scholar 

  16. Delbès, C, Moletta, R, Godon, JJ (2000) Monitoring of activity dynamics of an anaerobic digester bacterial community using 16S rRNA polymerase chain reaction-single-strand conformation polymorphism analysis. Environ Microbiol 2: 506–515

    Article  PubMed  Google Scholar 

  17. DeLong, EF, Franks, DG, Alldredge, AL (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38: 924–934

    Article  Google Scholar 

  18. Dolan, JR, Marrasé, C (1995) Planktonic ciliate distribution relative to a deep chlorophyll maximum: Catalan Sea, N.W. Mediterranean, June 1993. Deep-Sea Res 42: 1965–1987

    Article  Google Scholar 

  19. Dunbar, J, Ticknor, LO, Kuske, CR (2000) Assessment of microbial diversity in four southwestern United States soils by 16S rRNA gene terminal restriction fragment analysis. Appl Environ Microbiol 66: 2943–2950

    Article  PubMed  CAS  Google Scholar 

  20. Estrada, M, Salat, J (1989) Phytoplankton assemblages of deep and surface water layers in Mediterranean frontal zone. Sci Mar 53: 203–214

    Google Scholar 

  21. Fandino, LB, Riemann, L, Steward, GF, Long, RA, Azam, F (2001) Variations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16S rDNA sequencing. Aquat Microb Ecol 23: 119–130

    Google Scholar 

  22. Farrelly, V, Rainey, FA, Stackebrandt, E (1995) Effect of genome size and rrn gene copy number on PCR amplification of 16S ribosomal-RNA genes from a mixture of bacterial species. Appl Environ Microbiol 61: 2798–2801

    PubMed  CAS  Google Scholar 

  23. Faugeras, B, Levy, M, Mémery, L, Verron, J, Blum, J, Charpentier, I (2003) Can biogeochemical fluxes be recovered from nitrate and chlorophyll data? A case study assimilating data in the Northwestern Mediterranean Sea at the JGOFS-DYFAMED station. J Mar Syst 40–41: 99–125

    Article  Google Scholar 

  24. Gasol, JM, Doval, MD, Pinhassi, J, Calderón-Paz, JI, Guixa-Boixareu, N, Vaqué, D, Pedrós-Alió, C (1998) Diel variations in bacterial heterotrophic activity and growth in the northwestern Mediterranean Sea. Mar Ecol Prog Ser 164: 107–124

    Google Scholar 

  25. Gasol, JM, Morán, XAG (1999) Effects of filtration on bacterial activity and picoplankton community structure as assessed by flow cytometry. Aquat Microb Ecol 16: 251–264

    Google Scholar 

  26. Ghiglione, JF, Larcher, M, Lebaron, P (2005) Spatial and temporal variation scales of bacterioplankton community structure in NW Mediterranean Sea. Aquat Microb Ecol 40: 229–240

    Google Scholar 

  27. Goutx, M, Gérin, C, Bertrand, JC (1990) An application of Iatroscan thin-layer chromatography with flame ionization detection—Lipids classes of microorganisms as biomarkers in the marine environment. Org Geochem 16: 1231–1237

    Article  CAS  Google Scholar 

  28. Grossart, HP, Simon, M (1998) Bacterial colonization and microbial decomposition of limnetic organic aggregates (lake snow). Aquat Microb Ecol 15: 127–140

    Google Scholar 

  29. Hansen, B, Bech, G (1996) Bacteria associated with a marine planktonic copepod in culture. I. Bacterial genera in seawater, body surface, intestines and fecal pellets and succession during fecal pellet degradation. J Plankton Res 18: 257–273

    Article  Google Scholar 

  30. Herndl, GJ (1988) Ecology of amorphous aggregations (marine snow) in the northern Adriatic Sea. Microbial density and activity in marine snow and its implication to overall pelagic processes. Mar Ecol Prog Ser 48: 265–275

    Google Scholar 

  31. Herndl, GJ, Miller-Niklas, G, Frick, J (1993) Major role of ultraviolet-B in controlling bacterioplankton growth in the surface layer of the ocean. Nature 361: 71–72

    Article  Google Scholar 

  32. Hobbie, JE, Daley, RJ, Jasper, J (1977) Use of nucleopore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33: 1225–1228

    PubMed  CAS  Google Scholar 

  33. Hollibaugh, T, Wong, PS, Murrell, MC (2000) Similarity of particle- associated and free-living bacterial communities in northern San Francisco Bay, California. Aquat Microb Ecol 21: 102–114

    Google Scholar 

  34. Karl, DM, Knauer, GA, Martin, JH (1988) Downward flux of particulate organic matter in the ocean: a particle decomposition paradox. Nature 332: 438–441

    Article  Google Scholar 

  35. Kirchman, D, K’Nees, E, Hodson, R (1985) Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49: 599–607

    PubMed  CAS  Google Scholar 

  36. Kirchman, DL (1993) Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In: Kemp, PF, Sherr, BF, Sherr, EB, Cole, JJ (Eds.) Handbook of Methods in Aquatic Microbial Ecology, Lewis Publishers, Boca Raton, Fla, pp 509–512

    Google Scholar 

  37. Kuipers, B, Noort, GJ, Vosjan, JH, Herndl, GJ (2000) Diel periodicity of bacterioplankton in the euphotic zone of the subtropical Atlantic Ocean. Mar Ecol Prog Ser 201: 13–25

    Google Scholar 

  38. Lee, DH, Zo, YG, Kim, SJ (1996) Non-radioactive method to study genetic profiles of natural bacterial communities by PCR-single-strand-conformation polymorphism. Appl Environ Microbiol 62: 3112–3120

    PubMed  CAS  Google Scholar 

  39. Lee, RF, Nevenzel, JC, Paffenhöffer, GA (1971) Importance of wax esters and other lipids in the marine food chain: phytoplankton and copepods. Mar Biol 9: 99−108

    Article  CAS  Google Scholar 

  40. Lee, SH, Fuhrman, JA (1991) Spatial and temporal variation of natural bacterioplankton assemblages studied by total genomic DNA cross-hybridization. Limnol Oceanogr 36: 1277–1287

    Article  Google Scholar 

  41. Lee, SH, Kang, YC, Fuhrman, JA (1995) Imperfect retention of natural bacterioplankton studied at the level of community DNA. Mar Ecol Prog Ser 79: 195–201

    Google Scholar 

  42. Long, R, Azam, F (2001) Antagonistic interactions among marine pelagic bacteria. Appl Environ Microbiol 67: 4975–4983

    Article  PubMed  CAS  Google Scholar 

  43. Martinez, J, Smith, DC, Steward, GF, Azam, F (1996) Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea. Aquat Microb Ecol 10: 223–230

    Google Scholar 

  44. Marty, JC, Chiavérini, J, Pizay, MD, Avril, B (2002) Seasonal and interannual dynamics of nutrients and phytoplankton pigments in the western Mediterranean Sea at the DYFAMED time-series station (1991–1999). Deep-Sea Res II 49: 1965–1985

    Article  CAS  Google Scholar 

  45. Moeseneder, M, Winter, C, Herndl, GJ (2001) Horizontal and vertical complexity of attached and free-living bacteria in the eastern Mediterranean Sea, determined by 16S rDNA and 16S rRNA fingerprints. Limnol Oceanogr 46: 95–107

    CAS  Google Scholar 

  46. Murray, AE, Preston, CM, Massana, R, Taylor, LT, Blakis, A, Wu, K, DeLong, EF (1998) Seasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers Island, Antarctica. Appl Environ Microbiol 64: 2585–2595

    PubMed  CAS  Google Scholar 

  47. Muyzer, G, Smalla, K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73: 127–141

    Article  PubMed  CAS  Google Scholar 

  48. Parrish, CC, McKenzie, CH, MacDonald, BA, Hatfield, EA (1995) Seasonal studies of seston lipids in relation to microplankton species composition and scallop growth in South Broad Cove, Newfoundland. Mar Ecol Prog Ser 129: 151–164

    CAS  Google Scholar 

  49. Parrish, CC, Wangersky, PJ (1987) Particulate ad dissolved lipid classes in cultures of Phaeodactylum tricornutum grown in cage culture turbidostats with a range of nitrogen supply rates. Mar Ecol Prog Ser 35: 119–128

    CAS  Google Scholar 

  50. Pinhassi, J, Azam, F, Hemphälä, J, Long, RA, Martinez, J, Zweifel, UL, Hagström, Å (1999) Coupling between bacterioplankton species composition, population dynamics, and organic matter degradation. Aquat Microb Ecol 17: 13–26

    Google Scholar 

  51. Raimbault, P, Diaz, F, Boudjellal, B (1999) Simultaneous determination of particulate forms of carbon, nitrogen and phosphorus collected on filters using a semi-automatic wet-oxidation procedure. Mar Ecol Prog Ser 180: 289–295

    CAS  Google Scholar 

  52. Riemann, L, Steward, GF, Fandino, LB, Campbell, L, Landry, MR, Azam, F (1999) Bacterial community composition during two consecutive NE Monsoon periods in the Arabian Sea studied by denaturing gradient gel electrophoresis (DGGE) of rRNA genes. Deep-Sea Res II 46: 1791–1811

    Article  Google Scholar 

  53. Schauer, M, Balagué, V, Pedros-Alio, C, Massana, R (2003) Seasonal changes in the taxonomic composition of bacterioplankton in a coastal oligotrophic system. Aquat Microb Ecol 31: 163–174

    Google Scholar 

  54. Schmidt, TM (1997) Multiplicity of ribosomal RNA operons in prokaryotic genomes. In: De Bruijn, FJ, Lupski, JR, Weinstock, GM (Eds.) Bacterial Genomes: Physical Structure and Analysis, Chapman Hall, New York, pp 221–229

    Google Scholar 

  55. Simon, M, Alldredge, AL, Azam, F (1990) Bacterial carbon dynamics on marine snow. Mar Ecol Prog Ser 65: 205–211

    CAS  Google Scholar 

  56. Simon, M, Grossart, HP, Schweitzer, B, Ploug, H (2002) Microbial ecology of organic aggregates in aquatic systems. Aquat Microb Ecol 28: 175–211

    Google Scholar 

  57. Smith, DC, Simon, M, Alldredge, AL, Azam, F (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359: 139–142

    Article  CAS  Google Scholar 

  58. Striby, L, Lafont, R, Goutx, M (1999) Improvement in the Iatroscan thin-layer chromatographic-flame ionisation detection analysis of marine lipids. Separation and quantitation of monoacylglycerols and diacylglycerols in standards and natural samples. J Chromatogr 849: 371–380

    Article  CAS  Google Scholar 

  59. Sugimura, Y, Suzuki, Y (1988) A high temperature catalytic oxidation method for the determination of non-volatile dissolved organic carbon in seawater by direct injection of a liquid sample. Mar Chem 24: 105–131

    Article  CAS  Google Scholar 

  60. 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 

  61. Turley, CM, Stutt, ED (2000) Depth-related cell-specific bacterial leucine incorporation rates on particles and its biogeochemical significance in the Northwest Mediterranean. Limnol Oceanogr 45: 419–425

    Article  CAS  Google Scholar 

  62. Velji, MI, Albright, LJ (1993) Improved sample preparation for enumeration of aggregated aquatic substrate bacteria. In: Kemp, PF, Sherr, BF, Sherr, EB, Cole, JJ (Eds.) Handbook of Methods in Aquatic Microbial Ecology, Lewis Publishers, Boca Raton, Fla, pp 139–142

    Google Scholar 

  63. Winter, C, Herndl, G, Weinbauer, MG (2004) Diel cycles in viral infection of bacterioplankton in the North Sea. Aquat Microb Ecol 35: 207–216

    Google Scholar 

  64. Yentsch, CS, Menzel, DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Res 10: 221–231

    CAS  Google Scholar 

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Acknowledgments

This work was supported by PROOF Grant (program “Production and exportation of carbon: control by heterotrophic organisms at small time scales”-PECHE). We thank the captains and the crews of the RV Tethys for their help during sampling, and especially L. Chateau, R. Deshayes, R. Lafont, N. Rey, and M. Saury. We thank P. Raimbault and L. Oriol for their contributions to chlorophyll and nutrients measurements and C. Guigue for her contribution to chemical analysis. We are grateful to F. Joux and I. Obernosterer for helpful discussions.

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Authors and Affiliations

  1. Observatoire Océanographique de Banyuls, Laboratoire d’Océanographie Biologique, Université Pierre et Marie Curie-Paris6, Institut National des Sciences de l’Univers (INSU), CNRS (UMR 7621), BP44, 66651, Banyuls-sur-mer Cedex, France

    J. F. Ghiglione, M. Pujo-Pay & P. Lebaron

  2. Station Biologique de Roscoff, Université Pierre et Marie Curie-Paris6, Institut National des Sciences de l’Univers (INSU), CNRS (UMR 7144), BP 74, 29682, Roscoff Cedex, France

    G. Mevel

  3. Observatoire Océanologique de Villefranche-sur-mer, Université Pierre et Marie Curie-Paris6, Institut National des Sciences de l’Univers (INSU), CNRS (UMR 7093), BP 28, 06234, Villefranche sur mer, France

    L. Mousseau

  4. Laboratoire de Microbiologie, Géochimie et Ecologie Marines, Université de la Méditerranée, Centre d’Océanologie de Marseille, CNRS (UMR 6117), Campus de Luminy, case 901, 13288, Marseille Cedex 09, France

    M. Goutx

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  1. J. F. Ghiglione
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  4. L. Mousseau
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Correspondence to J. F. Ghiglione.

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Ghiglione, J.F., Mevel, G., Pujo-Pay, M. et al. Diel and Seasonal Variations in Abundance, Activity, and Community Structure of Particle-Attached and Free-Living Bacteria in NW Mediterranean Sea. Microb Ecol 54, 217–231 (2007). https://doi.org/10.1007/s00248-006-9189-7

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  • DOI: https://doi.org/10.1007/s00248-006-9189-7

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