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Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem

Abstract

Predicting the ocean’s role in the global carbon cycle requires an understanding of the stoichiometric coupling between carbon and growth-limiting elements in biogeochemical processes. A recent addition to such knowledge is that the carbon/nitrogen ratio of inorganic consumption and release of dissolved organic matter may increase in a high-CO2 world1. This will, however, yield a negative feedback on atmospheric CO2 only if the extra organic material escapes mineralization within the photic zone. Here we show, in the context of an Arctic pelagic ecosystem, how the fate and effects of added degradable organic carbon depend critically on the state of the microbial food web. When bacterial growth rate was limited by mineral nutrients, extra organic carbon accumulated in the system. When bacteria were limited by organic carbon, however, addition of labile dissolved organic carbon reduced phytoplankton biomass and activity and also the rate at which total organic carbon accumulated, explained as the result of stimulated bacterial competition for mineral nutrients. This counterintuitive ‘more organic carbon gives less organic carbon’ effect was particularly pronounced in diatom-dominated systems where the carbon/mineral nutrient ratio in phytoplankton production was high. Our results highlight how descriptions of present and future states of the oceanic carbon cycle require detailed understanding of the stoichiometric coupling between carbon and growth-limiting mineral nutrients in both autotrophic and heterotrophic processes.

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Figure 1: Idealized microbial food web used to illustrate some of the interactions believed to be important in controlling the autotroph–heterotroph balance in the photic zone.
Figure 2: Time course of bloom development.
Figure 3: Ecosystem responses to glucose.

References

  1. 1

    Riebesell, U. et al. Enhanced biological carbon consumption in a high CO2 ocean. Nature 450, 545–548 (2007)

    ADS  CAS  Article  Google Scholar 

  2. 2

    delGiorgio, P. A., Cole, J. J. & Cimbleris, A. Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385, 148–151 (1997)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Thingstad, T. F., Hagstrom, A. & Rassoulzadegan, F. Accumulation of degradable DOC in surface waters: is it caused by a malfunctioning microbial loop? Limnol. Oceanogr. 42, 398–404 (1997)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Thingstad, T. F., Nielsen, T. G., Hansen, A. S. & Levinsen, H. Control of bacterial production in cold waters. A theoretical analysis of mechanisms relating bacterial production and zooplankton biomass in Disko Bay, Western Greenland. Mar. Ecol. Prog. Ser. 228, 15–24 (2002)

    ADS  CAS  Article  Google Scholar 

  5. 5

    Børsheim, K. Y. et al. Photosynthetic algal production, accumulation and release of phytoplankton storage carbohydrates and bacterial production in a gradient in daily nutrient supply. J. Plankton Res. 27, 743–755 (2005)

    Article  Google Scholar 

  6. 6

    Pomeroy, L. R. & Deibel, D. Temperature regulation of bacterial activity during the spring bloom in Newfoundland coastal waters. Science 233, 359–361 (1986)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Rose, J. M. & Caron, D. A. Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters. Limnol. Oceanogr. 52, 886–895 (2007)

    ADS  Article  Google Scholar 

  8. 8

    Stroeve, J., Holland, M. M., Meier, W., Scambos, T. & Serreze, M. Arctic sea ice decline: faster than forecast. Geophys. Res. Lett. 34, L24501 (2007)

    Article  Google Scholar 

  9. 9

    Bellerby, R. G. J., Olsen, A., Furevik, T. & Anderson, L. A. in Climate Variability in the Nordic Seas (eds Drange, H., Dokken, T. M., Furevik, T., Gerdes, R. & Berger, W.) Geophysical Monograph Series 189–198 (AGU, 2005)

    Google Scholar 

  10. 10

    Ducklow, H. W. et al. Constraining bacterial production, conversion efficiency and respiration in the Ross Sea, Antarctica, January–February, 1997. Deep-Sea Res. Part II-Top. Stud. Oceanogr. 47, 3227–3247 (2000)

    CAS  Article  Google Scholar 

  11. 11

    Fagerbakke, K. M., Heldal, M. & Norland, S. Content of carbon, nitrogen, oxygen, sulfur and phosphorus in native aquatic and cultured bacteria. Aquat. Microb. Ecol. 10, 15–27 (1996)

    Article  Google Scholar 

  12. 12

    Martinussen, I. & Thingstad, T. F. Utilization of N, P, and organic C by heterotrophic bacteria. II. Comparison of experiments and a mathematical model. Mar. Ecol. Prog. Ser. 37, 285–293 (1987)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Holmes, R. M. et al. Lability of DOC transported by Alaskan rivers to the arctic ocean. Geophys. Res. Lett. 35, L03402 (2008)

    ADS  Article  Google Scholar 

  14. 14

    Graneli, W., Carlsson, P. & Bertilsson, S. Bacterial abundance, production and organic carbon limitation in the Southern Ocean (39–62 degrees S, 4–14 degrees E) during the austral summer 1997/1998. Deep-Sea Res. Part II-Top. Stud. Oceanogr. 51, 2569–2582 (2004)

    CAS  Article  Google Scholar 

  15. 15

    Church, M. J., Hutchins, D. A. & Ducklow, H. W. Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean. Appl. Environ. Microbiol. 66, 455–466 (2000)

    CAS  Article  Google Scholar 

  16. 16

    Rivkin, R. & Anderson, M. Inorganic nutrient limitation of oceanic bacterioplankton. Limnol. Oceanogr. 42, 730–740 (1997)

    ADS  CAS  Article  Google Scholar 

  17. 17

    Stets, E. G. & Cotner, J. B. The influence of dissolved organic carbon on bacterial phosphorous uptake and bacteria-phytoplankton dynamics in two Minnesota lakes. Limnol. Oceanogr. 53, 137–147 (2008)

    ADS  CAS  Article  Google Scholar 

  18. 18

    Carmack, E. & Wassmann, P. Food webs and physical–biological coupling on pan-Arctic shelves: Unifying concepts and comprehensive perspectives. Prog. Oceanogr. 71, 446–477 (2006)

    ADS  Article  Google Scholar 

  19. 19

    Rey, F. & Skjoldal, H. R. Consumption of silicic-acid below the euphotic zone by sedimenting diatom blooms in the Barents Sea. Mar. Ecol. Prog. Ser. 36, 307–312 (1987)

    ADS  CAS  Article  Google Scholar 

  20. 20

    Wassmann, P. et al. Spring bloom development in the marginal ice zone and the central Barents Sea. PSZN I: Mar. Ecol. 20, 321–346 (1999)

    Google Scholar 

  21. 21

    Koroleff, F. in Methods of Seawater Analysis 2nd revised and extended edn (eds Grasshoff, K., Ehrhardt, M. & Kremling, K.) 125–131 (Chemie, 1983)

    Google Scholar 

  22. 22

    Valderrama, J. C. in Manual on Harmful Marine Microalgae IOC Manuals and Guides number 33 (eds Hallegraeff, G. M. Anderson, D. M. & Cembella, A. D.) 262–265 (UNESCO, 1995)

    Google Scholar 

  23. 23

    Holmes, R. M., Aminot, A., Kéroul, R., Hooker, A. H. & Peterson, B. J. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can. J. Aquat. Sci. 56, 1801–1808 (1999)

    CAS  Article  Google Scholar 

  24. 24

    Thingstad, T. F., Skjoldal, E. F. & Bohne, R. A. Phosphorus cycling and algal–bacterial competition in Sandsfjord, western Norway. Mar. Ecol. Prog. Ser. 99, 239–259 (1993)

    CAS  Article  Google Scholar 

  25. 25

    Hobbie, J. E. & Crawford, C. C. Bacterial uptake of organic substrate: new methods of study and application t o eutrophication. Verh. Internat. Verein. Limnol. 17, 725–730 (1969)

    Google Scholar 

  26. 26

    Havskum, H. et al. Silicate and labile DOC interfere in structuring the microbial food web via algal-bacterial competition for mineral nutrients: Results of a mesocosm experiment. Limnol. Oceanogr. 48, 129–140 (2003)

    ADS  Article  Google Scholar 

  27. 27

    Parsons, T. R., Maita, Y. & Lalli, C. M. A Manual of Chemical and Biological Methods for Seawater Analysis 107–110 (Pergamon, 1984)

    Google Scholar 

  28. 28

    Eriksen, N. T., Riisgard, F. K., Gunther, W. S. & Iversen, J. J. L. On-line estimation of O2 production, CO2 uptake, and growth kinetics of microalgal cultures in a gas-tight photobioreactor. J. Appl. Phycol. 19, 161–174 (2007)

    CAS  Article  Google Scholar 

  29. 29

    Marie, D., Brussaard, C. P. D., Thyrhaug, R., Bratbak, G. & Vaulot, D. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl. Environ. Microbiol. 65, 45–52 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30

    Simon, M. & Azam, F. Protein content and protein synthesis rates of planktonic marine bacteria. Mar. Ecol. Prog. Ser. 51, 201–213 (1989)

    ADS  CAS  Article  Google Scholar 

  31. 31

    Smith, D. & Azam, F. A simple, economical method for measuring bacterial protein synthesis in seawater using 3H-leucine. Mar. Microb. Food Webs 6, 107–114 (1992)

    Google Scholar 

  32. 32

    Børsheim, K. Y. Bacterial production rates and concentrations of organic carbon at the end of the growing season in the Greenland Sea. Aquat. Microb. Ecol. 21, 115–123 (2000)

    Article  Google Scholar 

Download references

Acknowledgements

This work was financed by the Research Council of Norway through the International Polar Year project 175939/S30 ‘PAME-Nor’ (IPY activity ID no. 71), with additional support from the strategic institution project 158936/I10 ‘Patterns in microbial diversity’, Bjerknes Centre of Climate Research Centre of Excellence Project 146003/V30, project 178441/S40 ‘Interact’ and project 184860/S30 ‘MERCLIM’. Support was received also from Norsk Hydro Produksjon AS project number 5404889, and from the Svalbard Science Forum as ‘Arktisstipend’. We thank Kings Bay A/S and the staff at Ny Ålesund for help with logistics.

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Correspondence to T. F. Thingstad.

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The file contains Supplementary Data, Supplementary Methods and Supplementary Discussion, Supplementary Figures S1-S7, Supplementary Table 1 and additional references. (PDF 1758 kb)

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Thingstad, T., Bellerby, R., Bratbak, G. et al. Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455, 387–390 (2008). https://doi.org/10.1038/nature07235

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