Microbial Ecology

, Volume 63, Issue 2, pp 324–333 | Cite as

High Contribution of SAR11 to Microbial Activity in the North West Mediterranean Sea

  • Mélissa Laghdass
  • Philippe Catala
  • Jocelyne Caparros
  • Louise Oriol
  • Philippe Lebaron
  • Ingrid ObernostererEmail author
Notes and Short Communications


We investigated the abundance and activity of SAR11 on a monthly time scale between January 2008 and October 2008 in the oligotrophic NW Mediterranean Sea. Applying MICRO-CARD-FISH, we observed that SAR11 had a large contribution to bulk abundance (37 ± 6% of DAPI-stained cells) and to bulk bacterial heterotrophic production (BHP), as estimated from leucine incorporation (55 ± 15% of DAPI-cells assimilating leucine) in surface waters (5 m) throughout the study period. SAR11 contributed also substantially to the assimilation of glucose, ATP, and a combination of amino acids (44 ± 17%, 37 ± 14%, and 43 ± 12% of DAPI cells assimilating these compounds, respectively), organic compounds that provide either single or combined sources of C, P, and N. Temporal changes in the abundance of SAR11 cells that assimilated leucine, glucose, amino acids, and ATP revealed a pattern consistent with that of substrate-active DAPI cells, suggesting that the activity of SAR11 can explain to a large extent the variability in total cells contributing to the utilization of these compounds. Short-term nutrient enrichment experiments performed on each sampling date revealed a strong co-limitation of at least two of the three elements analyzed (C, N, P), in particular, during summer and early autumn. The in situ abundance of SAR11 cells assimilating leucine appeared to increase with P limitation as determined in the nutrient enrichment experiments (r = 0.81, p = 0.015). Our results demonstrate that SAR11 is an important component of the active bacterial community in the NW Mediterranean Sea. Our observations further indicate that the activity of the bulk bacterial community is linked to the activity of SAR11, possibly due to its adaptation to nutrient limitation.


Particulate Organic Carbon Dissolve Organic Nitrogen Dissolve Organic Matter Delaware Estuary Bacterial Heterotrophic Production 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank the captain and the crew of the R/V Nereis for their enthusiasm and support aboard. We also thank the members of the Service d'Observation of the Observatoire Océanologique in Banyuls for their help in sample collection. L. Zudaire provided the CTD profiles for all cruises. We also thank four reviewers for their critical comments on a previous version of this manuscript. This work was conducted as part of the national project MEDEA (INSU-LEFE-CYBER).


  1. 1.
    Carlson C (2002) Production and removal processes. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic, San DiegoGoogle Scholar
  2. 2.
    Thingstad T, Zweifel U, Rassoulzadegan F (1998) P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnol Oceanogr 43:88–94CrossRefGoogle Scholar
  3. 3.
    Joint I, Henriksen P, Fonnes GA, Bourne D, Thingstad TF, Riemann B (2002) Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquat Microb Ecol 29:145–159CrossRefGoogle Scholar
  4. 4.
    Teira E, Martínez-García S, Carreira C, Morán XAG (2011) Changes in bacterioplankton and phytoplankton community composition in response to nutrient additions in coastal waters off the NW Iberian Peninsula. Mar Ecol Prog Ser 426:87–104CrossRefGoogle Scholar
  5. 5.
    Pinhassi J, Gómez-Consarnau L, Alonso-Sáez L, Sala M, Vidal M, Pedrós-Alió C, Gasol J (2006) Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquat Microb Ecol 44:241–252CrossRefGoogle Scholar
  6. 6.
    Zohary T, Robarts R (1998) Experimental study of microbial P limitation in the eastern Mediterranean. Limnol Oceanogr 43:387–395CrossRefGoogle Scholar
  7. 7.
    Van Wambeke F, Christaki U, Giannakourou A, Moutin T, Souvemerzoglou K (2002) Longitudinal and vertical trends of bacterial limitation by phosphorus and carbon in the Mediterranean Sea. Microb Ecol 43:119–133PubMedCrossRefGoogle Scholar
  8. 8.
    Cotner J, Ammerman J, Peele E, Bentzen E (1997) Phosphorus-limited bacterioplankton growth in the Sargasso Sea. Aquat Microb Ecol 13:141–149CrossRefGoogle Scholar
  9. 9.
    Obernosterer I, Kawasaki N, Benner R (2003) P-limitation of respiration in the Sargasso Sea and uncoupling of bacteria from P-regeneration in size-fractionation experiments. Aquat Microb Ecol 32:229–237CrossRefGoogle Scholar
  10. 10.
    Van Wambeke F, Obernosterer I, Moutin T, Duhamel S, Ulloa O, Claustre H (2008) Heterotrophic bacterial production in the eastern South Pacific: longitudinal trends and coupling with primary production. Biogeosciences 5:157–169CrossRefGoogle Scholar
  11. 11.
    Rivkin R, Anderson M (1997) Inorganic nutrient limitation of oceanic bacterioplankton. Limnol Oceanogr 42:730–740CrossRefGoogle Scholar
  12. 12.
    Carlson CA, Ducklow HW (1996) Growth of bacterioplankton and consumption of dissolved organic carbon in the Sargasso Sea. Aquat Microb Ecol 10:69–85CrossRefGoogle Scholar
  13. 13.
    Kirchman D, Rich J (1997) Regulation of bacterial growth rates by dissolved organic carbon and temperature in the equatorial Pacific Ocean. Microb Ecol 33:11–20PubMedCrossRefGoogle Scholar
  14. 14.
    Elifantz H, Malmstrom R, Cottrell M, Kirchman D (2005) Assimilation of polysaccharides and glucose by major bacterial groups in the Delaware Estuary. Appl Environ Microb 71:7799–7805CrossRefGoogle Scholar
  15. 15.
    Teira E, Lebaron P, Van Aken H, Herndl G (2006) Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic. Limnol Oceanogr 51:2131CrossRefGoogle Scholar
  16. 16.
    Cottrell M, Kirchman D (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga–Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66:1692–1697PubMedCrossRefGoogle Scholar
  17. 17.
    Alonso-Sáez L, Gasol JM (2007) Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in northwestern Mediterranean coastal waters. Appl Environ Microbiol 73:3528–3535PubMedCrossRefGoogle Scholar
  18. 18.
    Zubkov M, Mary I, Woodward E, Warwick P, Fuchs B, Scanlan D, Burkill P (2007) Microbial control of phosphate in the nutrient-depleted North Atlantic subtropical gyre. Environ Microbiol 9:2079–2089PubMedCrossRefGoogle Scholar
  19. 19.
    Longnecker K, Lomas M, Van Mooy B (2010) Abundance and diversity of heterotrophic bacterial cells assimilating phosphate in the subtropical North Atlantic Ocean. Environ Microbiol 2:2773–2782Google Scholar
  20. 20.
    Morris RM, Rappé MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, Giovannoni SJ (2002) SAR 11 clade dominates ocean surface bacterioplankton communities. Nature 420:806–810PubMedCrossRefGoogle Scholar
  21. 21.
    Mary I, Heywood J, Fuchs B, Amann R, Tarran G, Burkill P, Zubkov M (2006) SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic meridional transect. Aquat Microb Ecol 45:107–113CrossRefGoogle Scholar
  22. 22.
    Malmstrom RR, Kiene RP, Cottrell MT, Kirchman DL (2004) Contribution of SAR11 bacteria to dissolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic ocean. Appl Environ Microbiol 70:4129–4135PubMedCrossRefGoogle Scholar
  23. 23.
    Vila-Costa M, Pinhassi J, Alonso C, Pernthaler J, Simo R (2007) An annual cycle of dimethylsulfoniopropionate-sulfur and leucine assimilating bacterioplankton in the coastal NW Mediterranean. Environ Microbiol 9:2451–2463PubMedCrossRefGoogle Scholar
  24. 24.
    Wilhelm L, Tripp H, Givan S, Smith D, Giovannoni S (2007) Natural variation in SAR 11 marine bacterioplankton genomes inferred from metagenomic data. Biology Direct 2:27PubMedCrossRefGoogle Scholar
  25. 25.
    Sowell S, Wilhelm L, Norbeck A, Lipton M, Nicora C, Barofsky D, Carlson C, Smith R, Giovannoni S (2008) Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. The ISME Journal 3:93–105PubMedCrossRefGoogle Scholar
  26. 26.
    Giovannoni S, Bibbs L, Cho J, Stapels M, Desiderio R, Vergin K, Rappé M, Laney S, Wilhelm L, Tripp H (2005) Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438:82–85PubMedCrossRefGoogle Scholar
  27. 27.
    Gilbert J, Mühling M, Joint I (2008) A rare SAR11 fosmid clone confirming genetic variability in the ‘Candidatus Pelagibacter ubique’genome. The ISME Journal 2:790–793PubMedCrossRefGoogle Scholar
  28. 28.
    Lami R, Cottrell M, Campbell B, Kirchman D (2009) Light-dependent growth and proteorhodopsin expression by Flavobacteria and SAR11 in experiments with Delaware coastal waters. Environ Microbiol 11:3201–3209PubMedCrossRefGoogle Scholar
  29. 29.
    Laghdass M, West NJ, Batailler N, Caparros J, Catala P, Lantoine F, Oriol L, Lebaron P, Obernosterer I (2010) Impact of lower salinity waters on bacterial heterotrophic production and community structure in the offshore NW Mediterranean Sea. Environ Microbiol Rep 2:761–769CrossRefGoogle Scholar
  30. 30.
    Tréguer P, Le Corre P (1975) Manuel d'analyse des sels nutritifs dans l'eau de mer. Laboratoire d’Océanographie Chimique, Université de Bretagne Occidentale, Brest, p 110Google Scholar
  31. 31.
    Pujo-Pay M, Raimbault P (1994) Improvement of the wet-oxidation procedure for simultaneous determination of particulate organic nitrogen and phosphorus collected on filters. Mar Ecol Prog Ser 105:203–207CrossRefGoogle Scholar
  32. 32.
    Benner R, Strom M (1993) A critical evaluation of the analytical blank associated with DOC measurements by high-temperature catalytic oxidation. Mar Chem 41:153–160CrossRefGoogle Scholar
  33. 33.
    Pernthaler A, Pernthaler J, Amann R (2002) Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68:3094–3101PubMedCrossRefGoogle Scholar
  34. 34.
    Sekar R, Pernthaler A, Pernthaler J, Warnecke F, Posch T, Amann R (2003) An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization. Appl Environ Microbiol 69:2928–2935PubMedCrossRefGoogle Scholar
  35. 35.
    Amann R, Krumholz L, Stahl D (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–770PubMedGoogle Scholar
  36. 36.
    Daims H, Brühl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB 338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444PubMedCrossRefGoogle Scholar
  37. 37.
    Glöckner FO, Fuchs BM, Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65:3721–3726PubMedGoogle Scholar
  38. 38.
    Cottrell MT, Kirchman DL (2003) Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary. Limnol Oceanogr 48:168–178CrossRefGoogle Scholar
  39. 39.
    Lebaron P, Parthuisot N, Catala P (1998) Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems. Appl Environ Microbiol 64:1725–1730PubMedGoogle Scholar
  40. 40.
    Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microb 64:3352–3358Google Scholar
  41. 41.
    Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6:107–114Google Scholar
  42. 42.
    Kirchman D (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, Boca Raton, pp 509–512Google Scholar
  43. 43.
    Lemée R, Rochelle-Newall E, Van Wambeke F, Pizay MD, Rinaldi P, Gattuso JP (2002) Seasonal variation of bacterial production, respiration and growth efficiency in the open NW Mediterranean Sea. Aquat Microb Ecol 29:227–237CrossRefGoogle Scholar
  44. 44.
    Lami R, Ghiglione JF, Desdevises Y, West NJ, Lebaron P (2009) Annual patterns of presence and activity of marine bacteria monitored by 16S rDNA–16S rRNA fingerprints in the coastal NW Mediterranean Sea. Aquat Microb Ecol 54:199–210CrossRefGoogle Scholar
  45. 45.
    Tanaka T, Rassoulzadegan F, Thingstad T (2004) Orthophosphate uptake by heterotrophic bacteria, cyanobacteria, and autotrophic nanoflagellates in Villefranche Bay, northwestern Mediterranean: vertical, seasonal, and short-term variations of the competitive relationship for phosphorus. Limnol Oceanogr 49:1063–1072CrossRefGoogle Scholar
  46. 46.
    Thingstad T, Krom M, Mantoura R, Flaten G, Groom S, Herut B, Kress N, Law C, Pasternak A, Pitta P (2006) Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science 309:1068CrossRefGoogle Scholar
  47. 47.
    Dolan J, Thingstad T, Rassoulzadegan F (1995) Phosphate transfer between microbial size-fractions in Villefranche Bay (NW Mediterranean Sea), France in autumn 1992. Ophelia 41:71–85Google Scholar
  48. 48.
    Copin-Montégut G, Avril B (1993) Vertical distribution and temporal variation of dissolved organic carbon in the North-Western Mediterranean Sea. Deep-Sea Res I 40:1963–1972CrossRefGoogle Scholar
  49. 49.
    Carlson C, Giovannoni S, Hansell D, Goldberg S, Parsons R, Otero M, Vergin K, Wheeler B (2002) Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquat Microb Ecol 30:19–36CrossRefGoogle Scholar
  50. 50.
    Alonso-Sáez L, Balagué V, Sa EL, Sanchez O, Gonzalez JM, Pinhassi J, Massana R, Pernthaler J, Pedrós-Alió C, Gasol JM (2007) Seasonality in bacterial diversity in north-west Mediterranean coastal waters: assessment through clone libraries, fingerprinting and FISH. FEMS Microbiol Ecol 60:98–112PubMedCrossRefGoogle Scholar
  51. 51.
    Malmstrom RR, Cottrell MT, Elifantz H, Kirchman DL (2005) Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the Northwest Atlantic Ocean. Appl Environ Microbiol 71:2979–2986PubMedCrossRefGoogle Scholar
  52. 52.
    Teira E, Martínez-García S, Lønborg C, Álvarez-Salgado X (2009) Growth rates of different phylogenetic bacterioplankton groups in a coastal upwelling system. Environ Microbiol Rep 1:545–554CrossRefGoogle Scholar
  53. 53.
    Rappé M, Connon S, Vergin K, Giovannoni S (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630–633PubMedCrossRefGoogle Scholar
  54. 54.
    Hamasaki K, Taniguchi A, Tada Y, Long RA, Azam F (2007) Actively growing bacteria in the Inland Sea of Japan, identified by combined bromodeoxyuridine immunocapture and denaturing gradient gel electrophoresis. Appl Environ microb 73:2787CrossRefGoogle Scholar
  55. 55.
    Alonso C, Pernthaler J (2006) Roseobacter and SAR11 dominate microbial glucose uptake in coastal North Sea waters. Environ Microbiol 8:2022–2030PubMedCrossRefGoogle Scholar
  56. 56.
    Malmstrom R, Kiene R, Kirchman D (2004) Identification and enumeration of bacteria assimilating dimethylsulfoniopropionate (DMSP) in the North Atlantic and Gulf of Mexico. Limnol Oceanogr 49:597–606CrossRefGoogle Scholar
  57. 57.
    Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, Vergin K (2009) Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. The ISME Journal 3:283–295PubMedCrossRefGoogle Scholar
  58. 58.
    Alonso-Sáez L, Sanchez O, Gasol J, Balagué V, Pedrós-Alió C (2008) Winter-to-summer changes in the composition and single-cell activity of near-surface Arctic prokaryotes. Environ Microbiol 10:2444–2454PubMedCrossRefGoogle Scholar
  59. 59.
    Sintes E, Herndl GJ (2006) Quantifying substrate uptake by individual cells of marine bacterioplankton by catalyzed reporter deposition fluorescence in situ hybridization combined with microautoradiography? Appl Environ Microbiol 72:7022–7028PubMedCrossRefGoogle Scholar
  60. 60.
    Garcia-Martinez J, Rodriguez-Valera F (2000) Microdiversity of uncultured marine prokaryotes: the SAR11 cluster and the marine Archaea of Group I. Mol Ecol 9:935–948PubMedCrossRefGoogle Scholar
  61. 61.
    Schwalbach M, Tripp H, Steindler L, Smith D, Giovannoni S (2010) The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity. Environ Microbiol 12:490–500PubMedCrossRefGoogle Scholar
  62. 62.
    Lauro FM, McDougald D, Thomas T, Williams TJ, Egan S, Rice S, DeMaere MZ, Ting L, Ertan H, Johnson J, Ferriera S, Lapidus A, Anderson I, Kyrpides N, Munk AC, Detter C, Han CS, Brown MV, Robb FT, Kjelleberg S, Cavicchioli R (2009) The genomic basis of trophic strategy in marine bacteria. PNAS 106:15527–15533PubMedCrossRefGoogle Scholar
  63. 63.
    Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, Bibbs L, Eads J, Richardson TH, Noordewier M, Rappe MS, Short JM, Carrington JC, Mathur EJ (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242–1245PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Mélissa Laghdass
    • 1
    • 2
  • Philippe Catala
    • 1
    • 2
  • Jocelyne Caparros
    • 1
    • 2
  • Louise Oriol
    • 1
    • 2
  • Philippe Lebaron
    • 1
    • 2
  • Ingrid Obernosterer
    • 1
    • 2
    Email author
  1. 1.UPMC Univ Paris 06, UMR 7621, LOMIC, Observatoire OcéanologiqueBanyuls/merFrance
  2. 2.CNRS, UMR 7621, LOMIC, Observatoire OcéanologiqueBanyuls/merFrance

Personalised recommendations