Polar Biology

, Volume 35, Issue 5, pp 785–794 | Cite as

Evidence of heterotrophic prokaryotic activity limitation by nitrogen in the Western Arctic Ocean during summer

  • E. Ortega-Retuerta
  • W. H. Jeffrey
  • J. F. Ghiglione
  • F. Joux
Short Note


Global warming in the Arctic Ocean may result in changes to the stock and dynamics of nutrients that drive the activity of heterotrophic prokaryotes, a key component of the microbial food web. We performed 14 enrichment experiments during summer in the Beaufort and Chukchi Seas (Western Arctic Ocean), with C (acetate and/or glucose), N (nitrate and/or ammonium) and P (phosphate) amendments. In 8 out of 11 experiments performed with surface waters, prokaryotic heterotrophic production was limited by N, either alone (5 experiments) or in co-limitation with C (3 experiments). This contrasted with the experiments performed using waters from the chlorophyll maxima, where N was never limiting. Diversity analyses (DNA- and RNA-based fingerprinting) suggest that limitation was not restricted to specific operational taxonomic units but common to the different groups. This is the first report of N limitation of prokaryotic heterotrophic production in Arctic surface waters. This control by N may gain importance in future scenarios of higher productivity in the area.


Heterotrophic prokaryotes Production Abundance Community structure Nutrient limitation Arctic Ocean 



This work was supported by the French National Research Agency, under the grant no. ANR-BLAN08-1_310980 to the MALINA project, the LEFE-CYBER and CNES TOSCA programs, and the European Space Agency. W.H.J was supported by a University of West Florida faculty scholarly and creative activity award. Research in the Chukchi Sea was possible thanks to the logistic offered by the NASA Icescape program. We thank R. Benner Y. Shen and C. Fichot for DOC data, S. Bélanger and K.R. Arrigo for chl a data, Y. Gratton and J. Swift for CTD data, J.E. Tremblay, P. Raimbault and J. Swift for nutrients data and D. Marie for in situ bacteria counts in 2009. We thank the editor and three anonymous reviewers for constructive comments in a previous version of this MS.


  1. Abboudi M, Jeffrey WH, Ghiglione JF, Pujo-Pay M, Oriol L, Sempéré R, Charrière B, Joux F (2008) Effects of photochemical transformations of dissolved organic matter on bacterial metabolism and diversity in three contrasting coastal sites in the Northwestern Mediterranean sea during summer. Microb Ecol 55:344–357PubMedCrossRefGoogle Scholar
  2. Allen AE, Howard-Jones MH, Booth MG, Frischer ME, Verity PG, Bronk DA, Sanderson MP (2002) Importance of heterotrophic bacterial assimilation of ammonium and nitrate in the Barents Sea during summer. J Mar Syst 38:93–108CrossRefGoogle Scholar
  3. Arrigo KR, van Dijken G, Pabi S (2008) Impact of a shrinking Arctic ice cover on marine primary production. Geophys Res Lett 35:6. doi: L1960310.1029/2008gl035028 Google Scholar
  4. Azam F, Fenchel T, Field JG, Gray JS, Meyerreil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263CrossRefGoogle Scholar
  5. Carmack EC, Macdonald RW, Jasper S (2004) Phytoplankton productivity on the Canadian Shelf of the Beaufort Sea. Mar Ecol Prog Ser 277:37–50CrossRefGoogle Scholar
  6. Church MJ (2008) Resource control of bacterial dynamics in the sea. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, New York, pp 335–382CrossRefGoogle Scholar
  7. Conan P, Sondergaard M, Kragh T, Thingstad F, Pujo-Pay M, Williams P, Markager S, Cauwet G, Borch NH, Evans D, Riemann B (2007) Partitioning of organic production in marine plankton communities: the effects of inorganic nutrient ratios and community composition on new dissolved organic matter. Limnol Oceanogr 52:753–765CrossRefGoogle Scholar
  8. Cuevas L, Egge J, Thingstad T, Töpper B (2011) Organic carbon and mineral nutrient limitation of oxygen consumption, bacterial growth and efficiency in the Norwegian Sea. Polar Biol 34:871–882CrossRefGoogle Scholar
  9. Dittmar T, Kattner G (2003) The biogeochemistry of the river and shelf ecosystem of the Arctic Ocean: a review. Mar Chem 83:103–120CrossRefGoogle Scholar
  10. Ducklow HW, Kirchman DL, Quinby HL (1992) Bacterioplankton cell growth and macromolecular synthesis in seawater cultures during the North Atlantic Spring Phytoplankton Bloom, May, 1989. Microb Ecol 24:125–144CrossRefGoogle Scholar
  11. Frey KE, Smith LC (2005) Amplified carbon release from vast West Siberian peatlands by 2100. Geophys Res Lett 32:4. doi: L0940110.1029/2004gl022025 Google Scholar
  12. Garneau M-È, Roy S, Lovejoy C, Gratton Y, Vincent WC (2008) Seasonal dynamics of bacterial biomass and production in a coastal arctic ecosystem: Franklin Bay, western Canadian Arctic. J Geophys Res 113:C07S91. doi: 10.1029/2007JC004281 CrossRefGoogle Scholar
  13. Ghiglione JF, Conan P, Pujo-Pay M (2009) Diversity of total and active free-living vs. particle-attached bacteria in the euphotic zone of the NW Mediterranean Sea. FEMS Microbiol Lett 299:9–21PubMedCrossRefGoogle Scholar
  14. Goldman JC, Caron DA, Dennett MR (1987) Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate c-n ratio. Limnol Oceanogr 32:1239–1252CrossRefGoogle Scholar
  15. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862PubMedCrossRefGoogle Scholar
  16. 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
  17. Kirchman DL (1990) Limitation of bacterial growth by dissolved organic matter in the subarctic Pacific. Mar Ecol Prog Ser 62:47–54CrossRefGoogle Scholar
  18. Kirchman DL (1994) The uptake of inorganic nutrients by heterotrophic bacteria. Microb Ecol 28:255–271CrossRefGoogle Scholar
  19. Kirchman DL, Wheeler PA (1998) Uptake of ammonium and nitrate by heterotrophic bacteria and phytoplankton in the sub-Arctic Pacific. Deep Sea Res I Oceanogr Res Pap 45:347–365CrossRefGoogle Scholar
  20. Kirchman DL, Malmstrom RR, Cottrell MT (2005) Control of bacterial growth by temperature and organic matter in the Western Arctic. Deep Sea Res II Top Stud Oceanogr 52:3386–3395CrossRefGoogle Scholar
  21. Kirchman DL, Hill V, Cottrell MT, Gradinger R, Malmstrom RR, Parker A (2009a) Standing stocks, production, and respiration of phytoplankton and heterotrophic bacteria in the western Arctic Ocean. Deep Sea Res II Top Stud Oceanogr 56:1237–1248CrossRefGoogle Scholar
  22. Kirchman DL, Moran XAG, Ducklow H (2009b) Microbial growth in the polar oceans—role of temperature and potential impact of climate change. Nat Rev Microb 7:451–459Google Scholar
  23. Kirchman DL, Cottrell MT, Lovejoy C (2010) The structure of bacterial communities in the western Arctic Ocean as revealed by pyrosequencing of 16S rRNA genes. Environ Microbiol 12:1132–1143PubMedCrossRefGoogle Scholar
  24. Matear RJ, Hirst AC (1999) Climate change feedback on the future oceanic CO2 uptake. Tellus Ser B Chem Phys Meteorol 51:722–733CrossRefGoogle Scholar
  25. Meon B, Amon RMW (2004) Heterotrophic bacterial activity and fluxes of dissolved free amino acids and glucose in the Arctic rivers Ob, Yenisei and the adjacent Kara Sea. Aquat Microb Ecol 37:121–135CrossRefGoogle Scholar
  26. Middelboe M, Lundsgaard C (2003) Microbial activity in the Greenland Sea: role of DOC lability, mineral nutrients and temperature. Aquat Microb Ecol 32:151–163CrossRefGoogle Scholar
  27. Mills MM, Moore CM, Langlois R, Milne A, Achterberg E, Nachtigall K, Lochte K, Geider RJ, La Roche J (2008) Nitrogen and phosphorus co-limitation of bacterial productivity and growth in the oligotrophic subtropical North Atlantic. Limnol Oceanogr 53:824–834CrossRefGoogle Scholar
  28. Perovich DK, Richter-Menge JA (2009) Loss of Sea Ice in the Arctic. Annu Rev Mar Sci 1:417–441CrossRefGoogle Scholar
  29. Peterson BJ, Holmes RM, McClelland JW, Vorosmarty CJ, Lammers RB, Shiklomanov AI, Shiklomanov IA, Rahmstorf S (2002) Increasing river discharge to the Arctic Ocean. Science 298:2171–2173PubMedCrossRefGoogle Scholar
  30. Rivkin RB, Anderson MR (1997) Inorganic nutrient limitation of oceanic bacterioplankton. Limnol Oceanogr 42:730–740CrossRefGoogle Scholar
  31. Schwalbach MS, Tripp HJ, Steindler L, Smith DP, Giovannoni SJ (2010) The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity. Environ Microbiol 12:490–500PubMedCrossRefGoogle Scholar
  32. Slagstad D, Ellingsen IH, Wassmann P (2011) Evaluating primary and secondary production in an Arctic Ocean void of summer sea ice: an experimental simulation approach. Prog Oceanogr 90:117–131CrossRefGoogle Scholar
  33. 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
  34. Springer AM, McRoy CP (1993) The paradox of pelagic food webs in the Northern Bering Sea. Patterns of primary production. Cont Shelf Res 13:575–599CrossRefGoogle Scholar
  35. Stolte W, Riemann R (1995) Effect of phytoplankton cell size on transient-state ammonium and nitrate kinetics. Microbiol 141:1221–1229CrossRefGoogle Scholar
  36. Thingstad TN, Cuevas LA (2010) Nutrient pathways through the microbial food web: principles and predictability discussed, based in five different experiments. Aquat Microb Ecol 61:249–260CrossRefGoogle Scholar
  37. Töpper B, Larsen A, Thingstad T, Thyrhaug R, Sandaa R-A (2011) Bacterial community composition in an Arctic phytoplankton mesocosm bloom: the impact of silicate and glucose. Polar Biol 33:1557–1565CrossRefGoogle Scholar
  38. Tovar-Sanchez A, Duarte CM, Alonso JC, Lacorte S, Tauler R, Galban-Malagon C (2010) Impacts of metals and nutrients released from melting multiyear Arctic sea ice. J Geophys Res Oceans 115:7. doi: 10.1029/2009jc005685 Google Scholar
  39. Tremblay JE, Gagnon J (2009) The effects of irradiance and nutrient supply on the productivity of Arctic waters: a perspective on climate change. In: Nihoul JCJ, Kostianoy AG (eds) Influence of climate change on the changing arctic and sub-arctic conditions. Nato Science for Peace and Security Series C Environmental Security. pp 73–93Google Scholar
  40. Vallières C, Retamal L, Ramlal P, Osburn CL, Vincent WF (2008) Bacterial production and microbial food web structure in a large arctic river and the coastal Arctic Ocean. J Mar Syst 74:756–773CrossRefGoogle Scholar
  41. Van Wambeke F, Bonnet S, Moutin T, Raimbault P, Alarcon G, Guieu C (2008) Factors limiting heterotrophic bacterial production in the southern Pacific Ocean. Biogeosciences 5:833–845CrossRefGoogle Scholar
  42. Yamamoto-Kawai M, Carmack E, McLaughlin F (2006) Nitrogen balance and Arctic throughflow. Nature 443:43PubMedCrossRefGoogle Scholar
  43. Zemb O, Haegeman B, Delgenes JP, Lebaron P, Godon JJ (2007) SAFUM: statistical analysis of SSCP fingerprints using PCA projections, dendrograms and diversity estimators. Mol Ecol Notes 7:767–770CrossRefGoogle Scholar
  44. Zhang JL (2005) Warming of the arctic ice-ocean system is faster than the global average since the 1960 s. Geophys Res Lett 32(19):4. doi: 10.1029/2005gl024216 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • E. Ortega-Retuerta
    • 1
    • 2
  • W. H. Jeffrey
    • 3
  • J. F. Ghiglione
    • 1
    • 2
  • F. Joux
    • 1
    • 2
  1. 1.Laboratoire d’Océanographie Microbienne, Observatoire OcéanologiqueUPMC Univ Paris 06, UMR 7621Banyuls/merFrance
  2. 2.Laboratoire d’Océanographie Microbienne, Observatoire OcéanologiqueCNRS, UMR 7621Banyuls/merFrance
  3. 3.Center for Environmental Diagnostics and BioremediationUniversity of West FloridaPensacolaUSA

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