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Seasonal Variation of Inorganic Nutrient Uptake by Heterotrophic Bacterioplankton in Jiaozhou Bay, North China

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Water, Air, & Soil Pollution: Focus

Abstract

The distribution patterns and factors affecting uptake rates and turnover times of dissolved inorganic nutrients by heterotrophic bacterioplankton (HB) in Jiaozhou Bay were studied based on in situ surveys and laboratory culturing. The uptake rates of dissolved inorganic phosphorus (DIP) and dissolved inorganic nitrogen (DIN) by HB are limited by the temperature of the water and the concentration of dissolved organic carbon. The turnover times of DIP and DIN by HB are regulated by the concentrations of the nutrients and the numbers of HB, which show significant spatiotemporal variability in Jiaozhou Bay. HB may aggravate the P-limitation of phytoplankton by competing for phosphorus in summer in Jiaozhou Bay. HB play an important role in the biogeochemical cycling of nutrients and may increase the N:P ratio and the accumulation of DIN, thereby accelerating the imbalance of the N:P ratio in Jiaozhou Bay.

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References

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

    Article  CAS  Google Scholar 

  • Azam, F., Fenchel, T., & Gray, J. G. (1983). The ecological role of water-column microbes in the sea. Marine Ecology. Progress Series, 10, 257.

    Article  Google Scholar 

  • Bai, J., Zhang, H. F., Li, K. R., Zhang, J., Liu, D. Y., Gao, D. M. et al. (2004). Distribution and relationship between bacterioplankton and inorganic nutrients in the Jiaozhou Bay in winter. Marine Sciences, 28, 31–24 (in Chinese, with English abstract).

    Google Scholar 

  • Benitez-Nelson, C. R., & Buesseler, K. O. (1999). Temporal variability of inorganic and organic phosphorus turnover rates in the coastal ocean. Nature, 398, 502–505.

    Article  CAS  Google Scholar 

  • Benitez-Nelson, C. R. (2000). The biogeochemical cycling of phosphorus in marine systems. Earth-Science Reviews, 51, 109–135.

    Article  CAS  Google Scholar 

  • Bjorkman, K., & Karl, D. M. (1994). Bioavailability of inorganic and organic phosphorus compounds to natural assemblages of microorganisms in Hawaiian coastal waters. Marine Ecology. Progress Series, 111, 265–273.

    Article  Google Scholar 

  • Capblancq, J. (1990). Nutrient dynamics and pelagic food web interactions in oligotrophic and eutrophic environments – An overview. Hydrobiologia, 207, 1–14.

    Article  CAS  Google Scholar 

  • Cherrier, J., Bauer, J. E., & Druffel, E. R. M. (1996). Utilization and turnover of labile dissolved organic matter by bacterial heterotrophs in eastern North Pacific surface waters. Marine Ecology. Progress Series, 139, 267–279.

    Article  Google Scholar 

  • Cochlan, W. P., Wikner, J., & Steward, G. F. (1993). Spatial distribution of viruses, bacteria, and chlorophyll-a in neritic, oceanic and estuarine environments. Marine Ecology. Progress Series, 92, 77–87.

    Article  Google Scholar 

  • Cotner, J. B., & Wetzel, R. G. (1992). Uptake of dissolved inorganic and organic phosphorus compounds by phytoplankton and bacterioplankton. Limnology and Oceanography, 37, 232–243.

    Article  CAS  Google Scholar 

  • Cristine, F. P., Markus, K., & Fereidoum, R. (1998). Release of dissolved amino acids by flagellates and ciliates grazing on bacteria. Oceanologica Acta, 21, 485–494.

    Article  Google Scholar 

  • David, A. C., Ee, L. L., Robert, W. S., Mark, R. D., & Ulrike-G., B. (2000). Responses of bacterioplankton and phytoplankton to organic carbon and inorganic nutrient additions in contrasting oceanic ecosystems. Aquatic Microbial Ecology, 22, 175–184.

    Article  Google Scholar 

  • Dugdale, R. C. (1967). Nutrient limitation in the sea: Dynamics,identification and significance. Limnology and Oceanography, 12, 685–695.

    Google Scholar 

  • Gasol, J. M., Del Giorgio, P. A., & Duarte, C. M. (1997). Biomass distribution in marine planktonic communities. Limnology and Oceanography, 42, 1353–1363.

    Article  CAS  Google Scholar 

  • Grasshoff, K. (1976). Determination of nitrate. In K. Grasshoff (Eds.), Methods of seawater analysis (pp. 137–145). Weinheim: Verlag Chemie.

    Google Scholar 

  • Hoch, M. P., & Kirchman, D. L. (1995). Ammonium uptake by heterotrophic bacteria in the Delaware estuary and adjacent coastal waters. Limnology and Oceanography, 40, 886–897.

    Article  CAS  Google Scholar 

  • Hoppe, H. G., Gocke, K., Koppe, R., & Begler, C. (2002). Bacterial growth and primary production along a north–south transect of the Atlantic Ocean. Nature, 416, 168–171.

    Article  CAS  Google Scholar 

  • James, B. C., Rosa, H. S., Harvey, B., Thomas, J., Joann, F. C., & Wayne S. G. (2000). Nutrient limitation of heterotrophic bacteria in Florida Bay. Estuaries, 23, 611–620.

    Article  Google Scholar 

  • Jiao, N. Z., & Xiao, T. (1995). The microbial secondary production in the Jiaozhou Bay. Chinese Science Bulletin, 40, 829–832.

    Google Scholar 

  • Katarina, V., Mikal, H., Svein, N., & Gunnar, B. (2002). Elemental Composition (C, N, P) and Cell Volume of Exponentially Growing and Nutrient-Limited Bacterioplankton. Applied and Environmental Microbiology, 68, 2965–2971.

    Article  CAS  Google Scholar 

  • Katrin, T., Crosbie, N. D., Donabaum, K., Kabas, W., Kirschner, A. K. T., Pfister, G., et al. (2003). Enhanced phosphorus accumulation efficiency by the pelagic community at reduced phosphorus supply: A lake experiment from bacteria to metazoan zooplankton. Limnology and Oceanography, 48, 1141–1149.

    Article  Google Scholar 

  • Lauren, L. C., Ellery, D. I., & Ronald, B. (1998). Marine phosphorus is selectively remineralized. Nature, 393, 426.

    Article  CAS  Google Scholar 

  • Lee, S., & Fuhrman, J. A. (1987). Relationships between biovolume and biomass of naturally derived marine bacterioplankton1. Applied and Environmental Microbiology, 53, 1298–1303.

    CAS  Google Scholar 

  • Liu, S. M., Zhang, J., Chen, S. Z., Chen, H. T., Hong, G. H., Wei, H. et al. (2003). Inventory of nutrient compounds in the Yellow Sea. Continental Shelf Research, 23, 1161–1174.

    Article  Google Scholar 

  • Liu, S. M., Zhang, J., Chen, H. T., & Zhang, G. S. (2005). Factors influencing nutrient dynamics in the eutrophic Jiaozhou Bay, North China. Progress in Oceanography, 66, 66–85.

    Article  Google Scholar 

  • Liu, Z., Wei, H., Bai, J., Zhang, J., Liu, D. Y., & Liu, S. M. (2007). Nutrients seasonal variation and budget in Jiaozhou Bay, China: A 3-dimensional physical-biological coupled model study. (this volume).

  • Middelburg, J. J., & Nieuwenhuize, J. (2000). Uptake of dissolved inorganic nitrogen in turbid,tidal estuaries. Marine Ecology. Progress Series, 192, 79–88.

    Article  CAS  Google Scholar 

  • Perry, M. J., & Eppley, R. W. (1981). Phosphate uptake by phytoplankton in the central North Pacific Ocean. Deep-Sea Res, 28, 39–49.

    Article  CAS  Google Scholar 

  • Porter, K. G., & Feig, Y. S. (1980). The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography, 25, 943–948.

    Google Scholar 

  • Richard, B. R. (1997). Inorganic nutrient limitation of oceanic bacterioplankton. Limnology and Oceanography, 42, 730–740.

    Article  Google Scholar 

  • Redfield, A. C. (1958). The biological control of chemical factors in the environment. American Scientist, 46, 205–222.

    CAS  Google Scholar 

  • Samuelsson, K., Berglund, J., Haecky, P., & Andersson, A. (2002). Structural changes in an aquatic microbial food web caused by inorganic nutrient addition. Aquatic Microbial Ecology, 29, 29–38.

    Article  Google Scholar 

  • Shen, Z. L. (2002). Long-term changes in nutrients structure and its influences on ecology and environment in Jiaohou Bay. Chinese Journal of Oceanology and Limnology, 33, 322–330 (in Chinese, with English abstract).

    CAS  Google Scholar 

  • Tezuka, Y. (1990). Bacterial regeneration of ammonium and phosphate as affected by the carbon: nitrogen: Phosphorus ratio of organic substrates. Microbial Ecology, 19, 227–238.

    Article  CAS  Google Scholar 

  • Thingstad, T. F., Krom, M. D., Mantoura, R. F. C., Flaten, G. A. F., Groom, S., Herut, B., et al. (2005). Nature of phosphorus limitation in the ultraoligotrophic eastern mediterranean. Science, 309, 1068–1071.

    Article  CAS  Google Scholar 

  • Thingstad, T. F., Zweifel, U. L., & Rassoulzadegan, F. (1998). P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnology and Oceanography, 43, 88–94.

    Article  CAS  Google Scholar 

  • Tsuneo, T., & Fereidoun, R. (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. Limnology and Oceanography, 49, 1063–1072.

    Article  Google Scholar 

  • Weisse, T. (1991). The microbial food web and its sensitivity to eutrophication and contaminant enrichment: A cross-system overview. Internationale Revue der gesamten Hydrobiologie, 76, 327–337.

    Article  Google Scholar 

  • Williams, P. C., & Deborah, A. B. (1998). Nitrogen uptake kinetics in the Ross Sea, Antarctica. Deep-Sea Res. II, 48, 4127–4153.

    Google Scholar 

  • Wu, Y. L., Sun, S., Zhang, Y. S., & Zhang, F. (2004). Quantitative study on long-term variation of phytoplankton in the JZB. Oceanologia et Limnologia Sinica, 35, 518–523 (in Chinese, with English abstract).

    Google Scholar 

  • Zheng, P. Y. (1994). The function and area division of JZB. Coastal Engineering Sinica, 13, 63–69 (in Chinese, with English abstract).

    Google Scholar 

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Acknowledgements

This research was supported by the National Natural Science Foundation of China (No. 40036010), the Chinese Ministry of Science and Technology (No. 2006CB400602), and the Shandong Province Environmental Protection Administration of China (No. 2004040-1). We thank Dr J. Sun for assistance in the field observations and express our gratitude to the referees for the time and effort taken to improve our original manuscript.

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Correspondence to K. R. Li.

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Bai, J., Li, K.R., Liu, D.Y. et al. Seasonal Variation of Inorganic Nutrient Uptake by Heterotrophic Bacterioplankton in Jiaozhou Bay, North China. Water Air Soil Pollut: Focus 7, 673–681 (2007). https://doi.org/10.1007/s11267-007-9124-z

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  • DOI: https://doi.org/10.1007/s11267-007-9124-z

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