Oceanography The Official Magazine of
The Oceanography Society
Volume 28 Issue 03

View Issue TOC
Volume 28, No. 3
Pages 84 - 99

OpenAccess

Abundance and Production Rates of Heterotrophic Bacterioplankton in the Context of Sediment and Water Column Processes in the Chukchi Sea

By Lee W. Cooper , Alexander S. Savvichev, and Jacqueline M. Grebmeier  
Jump to
Article Abstract Citation References Copyright & Usage
Article Abstract

Bacterial production and abundance are linked to areas of high biological production in the water column and in the underlying benthos in the Chukchi Sea. Process measurements taken during the Russian American Long-term Census of the Arctic (RUSALCA) program, such as the carbon isotope composition of sinking particulate organic matter and sediment organic matter, are used to put bacterial production and abundance in context. These measurements show that there are vertical gradients in the water column and that the stable carbon isotope composition of organic materials in the sediments is significantly different from sedimenting materials in the overlying water column. Differences within the water column likely reflect late summer declines in productivity that increase discrimination against 13C and also provide indications of carbon metabolism in the water column and underlying sediments. Temporal changes in the stable carbon isotope composition of organic matter in surface sediments, as well as C/N ratios in organic matter during the RUSALCA program, are also being observed, specifically higher ratios of 13C/12C at some stations near the Chukotka coast, and lower ratios of 13C/12C near Point Hope, Alaska. C/N ratios have increased since 2004 at productive sites in the south central Chukchi Sea, suggesting changes in organic material deposition. Other parameters studied on some or all of the decadal series of joint Russia-US cruises include sediment oxygen demand, the nitrogen isotopic composition of organic matter, sediment grain size, chlorophyll content in surface sediments, and elemental ratios of carbon and nitrogen in surface sediments. These process measurements support interpretations that the ecosystem shows strong coupling between bacterial and primary production and the underlying benthos.

Citation

Cooper, L.W., A.S. Savvichev, and J.M. Grebmeier. 2015. Abundance and production rates of heterotrophic bacterioplankton in the context of sediment and water column processes in the Chukchi Sea. Oceanography 28(3):84–99, https://doi.org/10.5670/oceanog.2015.59.

References
    Altabet, M.A., and R. François. 1994. Sedimentary nitrogen isotope ratio as a recorder for surface ocean nitrate utilization. Global Biogeochemical Cycles 8:103–116, https://doi.org/10.1029/​93GB03396.
  1. Amon, R.M.W., and B. Meon. 2004. The biogeochemistry of dissolved organic matter and nutrients in two large Arctic estuaries and potential implications for our understanding of the Arctic Ocean system. Marine Chemistry 92:311–330, https://doi.org/10.1016/j.marchem.2004.06.034.
  2. Bauer, J.E., W.-J. Cai, P.A. Raymond, T.S. Bianchi, C.S. Hopkinson, and P.A.G. Regnier. 2013. The changing carbon cycle of the coastal ocean. Nature 504:61–70, https://doi.org/10.1038/nature12857.
  3. Belyaev, N.A., V.I. Peresypkin, and M.S. Ponyaev. 2010. The organic carbon in the water, the particulate matter, and the upper layer of the bottom sediments of the west Kara Sea. Oceanology 50(5):706–715, https://doi.org/​10.1134/S0001437010050085.
  4. Benner, R., B. Benitez-Nelson, K. Kaiser, and R.M.W. Amon. 2004. Export of young terrigenous dissolved organic carbon from rivers to the Arctic Ocean. Geophysical Research Letters 31, L05305, https://doi.org/10.1029/2003GL019251
  5. Blair, N.E., and R.C. Aller. 2012. The fate of terrestrial organic carbon in the marine environment. Annual Review of Marine Science 4:401–423, https://doi.org/10.1146/annurev-marine-120709-142717.
  6. Børsheim, K.Y. 2000. Bacterial production rates and concentrations of organic carbon at the end of the growing season in the Greenland Sea. Aquatic Microbial Ecology 21:116–123, https://doi.org/​10.3354/ame021115.
  7. Brown, Z.W., K.E. Lowry, M.A. Palmer, G.L. van Dijken, M.M. Mills, R.S. Pickart, and K.R. Arrigo. 2015. Characterizing the subsurface chlorophyll a maximum in the Chukchi Sea and Canada Basin. Deep Sea Research Part II 118:88–104, https://doi.org/​10.1016/j.dsr2.2015.02.010.
  8. Chang, B.X., and A.H. Devol. 2009. Seasonal and spatial patterns of sedimentary denitrification rates in the Chukchi Sea. Deep Sea Research Part II 56(17):1,339–1,350, https://doi.org/10.1016/​j.dsr2.2008.10.024.
  9. Codispoti, L.A., C. Flagg, V. Kelly, and J.H. Swift. 2005. Hydrographic conditions during the 2002 SBI process experiments. Deep Sea Research Part II 52:3,199–3,226, https://doi.org/10.1016/​j.dsr2.2005.10.007.
  10. Cooper, L.W., R. Benner, L.A. Codispoti, V. Kelly, J.W. McClelland, B.J. Peterson, R. Holmes, and J.M. Grebmeier. 2005. Linkages among runoff, dissolved organic carbon, and the stable oxygen isotope composition of seawater and other water mass indicators in the Arctic Ocean. Journal of Geophysical Research 110, G02013, https://doi.org/10.1029/2005JG000031.
  11. Cooper, L.W., G.F. Cota, L.R. Pomeroy, J.M. Grebmeier, and T.E. Whitledge. 1999. Modification of NO, PO, and NO/PO during flow across the Bering and Chukchi shelves: Implications for use as Arctic water mass tracers. Journal of Geophysical Research 104(C4):7,827–7,836, https://doi.org/​10.1029/1999JC900010.
  12. Cooper, L.W., J.M. Grebmeier, I.L. Larsen, V.G. Egorov, C. Theodorakis, H.P. Kelly, and J.R. Lovvorn. 2002. Seasonal variation in sedimentation of organic materials in the St. Lawrence Island polynya region, Bering Sea. Marine Ecology Progress Series 226:13–26, https://doi.org/10.3354/meps226013.
  13. Cooper, L.W., C. Lalande, R.S. Pirtle-Levy, I.L. Larsen, and J.M. Grebmeier. 2009. Seasonal and decadal shifts in particulate organic matter processing and sedimentation in the Bering Strait shelf region. Deep Sea Research, Part II 56:1,316–1,325, https://doi.org/10.1016/j.dsr2.2008.10.025.
  14. Cooper, L.W., I.L. Larsen, T.M. Beasley, S.S. Dolvin, J.M. Grebmeier, J.M. Kelley, M. Scott, and A. Johnson-Pyrtle. 1998. The distribution of radiocesium and plutonium in sea ice-entrained Arctic sediments in relation to potential sources and sinks. Journal of Environmental Radioactivity 39(3):279–303, https://doi.org/​10.1016/S0265-931X(97)00058-1.
  15. del Giorgio, P.A., and J. Davis. 2003. Patterns in dissolved organic matter lability and consumption across aquatic ecosystems. Pp. 399–424 in Aquatic Ecosystems: Interactivity of Dissolved Organic Matter. S.E.G. Findlay and R.L. Sinsabaugh, eds, Academic Press, Burlington.
  16. Devol, A.H., L.A. Codispoti, and J.P. Christensen. 1997. Summer and winter denitrification rates in western Arctic shelf sediments. Continental Shelf Research 17(9):1,029–1,050, https://doi.org/​10.1016/S0278-4343(97)00003-4.
  17. Ducklow, H. 2000. Bacterial production and biomass in the oceans. Pp. 85–120 in Microbial Ecology of the Oceans. D. Kirchman, ed., Wiley-Liss, New York.
  18. Dunton, K.H., S.V. Schonberg, and L.W. Cooper. 2012. Food web structure of the Alaskan nearshore shelf and estuarine lagoons of the Beaufort Sea. Estuaries and Coasts 35(2):416–435, https://doi.org/10.1007/s12237-012-9475-1.
  19. Emmer, E., and R.C. Thunell. 2000. Nitrogen isotope variations in Santa Barbara Basin Sediments: Implications for denitrification in the eastern tropical North Pacific during the last 50,000 years. Paleoceanography 15(4):377–387, https://doi.org/​10.1029/1999PA000417.
  20. Fahl, K., H. Cremer, H. Erlenkeuser, H. Hansserr, J. Hölemann, H. Kassens, K. Knickmeier, K. Kosobokova, M. Kunz-Pirrung, F. Lindemann, and others. 1999. Sources and pathways of organic carbon in the modern Laptev Sea (Arctic Ocean): Implications from biological, geochemical and geological data. Polarforschung 69:193–205, http://epic.awi.de/28470/1/Polarforsch1999_24.pdf.
  21. Garneau, M.-E., S. Roy, C. Lovejoy, Y. Gratton, and W. Vincent. 2008. Seasonal dynamics of bacterial biomass and production in a coastal Arctic ecosystem: Franklin Bay, western Canadian Arctic. Journal of Geophysical Research 113, C07S91, https://doi.org/10.1029/2007JC004281.
  22. Grebmeier, J.M. 2012. Shifting patterns of life in the Pacific Arctic and sub-Arctic seas. Annual Review of Marine Science 4:63–78, https://doi.org/10.1146/annurev-marine-120710-100926.
  23. Grebmeier, J.M., B.A. Bluhm, L.W. Cooper, S. Danielson, K.R. Arrigo, A.L. Blanchard, J.T. Clark, R.H. Day, K.E. Frey, R.R. Gradinger, and others. 2015a. Ecosystem characteristics and processes facilitating persistent macrobenthic biomass hotspots and associated benthivory in the Pacific Arctic. Progress In Oceanography 136:92–114, https://doi.org/10.1016/j.pocean.2015.05.006.
  24. Grebmeier, J.M., B.A. Bluhm, L.W. Cooper, S.G. Denisenko, K. Iken, M. Kędra, and C. Serratos. 2015. Time-series benthic community composition and biomass and associated environmental characteristics in the Chukchi Sea during the RUSALCA 2004–2012 Program. Oceanography 28(3):116–133, https://doi.org/​10.5670/​oceanog.2015.61.
  25. Grebmeier, J.M., L.W. Cooper, H.M. Feder, and B.I. Sirenko. 2006. Ecosystem dynamics of the Pacific-influenced Northern Bering and Chukchi Seas in the Amerasian Arctic. Progress in Oceanography 71:331–361, https://doi.org/​10.1016/j.pocean.2006.10.001.
  26. Grebmeier, J.M., C.P. McRoy, and H.M. Feder. 1988. Pelagic-benthic coupling on the shelf of the northern Bering and Chukchi Seas: Part I. Food supply source and benthic biomass. Marine Ecology Progress Series 48:57–67, https://doi.org/​10.3354/meps051253.
  27. Guo, L., C.-L. Ping, and R.W. Macdonald. 2007. Mobilization pathways of organic carbon from permafrost to arctic rivers in a changing climate. Geophysical Research Letters 34, L13603, https://doi.org/10.1029/2007GL030689.
  28. Hobbie, J.E., R.J. Daley, and S. Jasper. 1977. Use of nuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology 33(5):1,225–1,228.
  29. Ivanov, M.V., A.Yu. Lein, A.S. Savvichev, I.I. Rusanov, E.F. Weslopolova, E.E. Zakcharova, and T.S. Prusakova. 2013. Abundance and activity of microorganisms at the water-sediment interface and their effect on the carbon isotopic composition of suspended organic matter and sediments of the Kara Sea. Microbiology 82(6):723–730, https://doi.org/10.1134/S0026261713060064.
  30. Ivanov, M.V., A.Yu. Lein, E.E. Zakharova, and A.S. Savvichev. 2012. Carbon isotopic composition in suspended organic matter and bottom sediments of the east Arctic seas. Microbiology 81(5):596–605, https://doi.org/​10.1134/S0026261712050086.
  31. Jones, E.P., and L.G. Anderson. 1986. On the origin of the chemical properties of the Arctic Ocean halocline. Journal of Geophysical Research 91(C9):759–767, https://doi.org/10.1029/JC091iC09p10759.
  32. Jones, E.P., L.G. Anderson, and J.H. Swift. 1998. Distribution of Atlantic and Pacific waters in the upper Arctic Ocean: Implications for circulation. Geophysical Research Letters 25(6):765–768, https://doi.org/10.1029/98GL00464.
  33. Kirchman, D.L., V. Hill, M.T. Cottrell, R. Gradinger, R.R. Malmstrom, and A. Parker. 2009a. Standing stocks, production, and respiration of phytoplankton and heterotrophic bacteria in the western Arctic Ocean. Deep Sea Research Part II 56(17):1,237–1,248, https://doi.org/10.1016/​j.dsr2.2008.10.018.
  34. Kirchman, D.L., X.A.G. Morán, and H. Ducklow. 2009b. Microbial growth in the polar oceans: Role of temperature and potential impact of climate change. Nature Reviews Microbiology 7:451–459, https://doi.org/10.1038/nrmicro2115.
  35. Lalande, C., J.M. Grebmeier, P. Wassmann, L.W. Cooper, M.V. Flint, and V.M. Sergeeva. 2007. Export fluxes of biogenic matter in the presence and absence of seasonal sea ice cover in the Chukchi Sea. Continental Shelf Research 27:2,051–2,065, https://doi.org/​10.1016/j.csr.2007.05.005
  36. Lee, S.H., H.-U. Dahms, Y. Kim, E.J. Choy, S.-H. Kang, and C.-K. Kang. 2014. Spatial distribution of small phytoplankton composition in the Chukchi Sea. Polar Biology 37(1):99–109, https://doi.org/​10.1007/s00300-013-1413-6.
  37. Lee, S.H., D. Stockwell, and T.E. Whitledge. 2010. Uptake rates of dissolved inorganic carbon and nitrogen by under-ice phytoplankton in the Canada Basin in summer 2005. Polar Biology 33(8):1,027–1,036, https://doi.org/10.1007/s00300-010-0781-4.
  38. Lee, S.H., T.E. Whitledge, and S.-H. Kang. 2007. Recent carbon and nitrogen uptake rates of phytoplankton in Bering Strait and the Chukchi Sea. Continental Shelf Research 27(17):2,231–2,249, https://doi.org/10.1016/j.csr.2007.05.009.
  39. Lein, A.Yu., M.D. Kravchishina, N.V. Politova, A.S. Savvichev, E.F. Veslopolova, I.N. Mitskevich, N.V. Ul’yanova, V.P. Shevchenko, and M.V. Ivanov. 2012. Transformation of particulate organic matter at the water-bottom boundary in the Russian Arctic seas: Evidence from isotope and radioisotope data. Lithology and Mineral Resources 47(2):99–128, https://doi.org/10.1134/S0024490212020034.
  40. Lein, A.Yu., A.S. Savvichev, I.I. Rusanov, G.A. Pavlova, N.A. Belyaev, K. Crane, N.V. Pimenov, and M.V. Ivanov. 2007. Biogeochemical processes in the Chukchi Sea. Lithology and Mineral Resources 42(3):221–239, https://doi.org/10.1134/S0024490207030029.
  41. Lovvorn, J.R., L.W. Cooper, M.L. Brooks, C.C. De Ruyck, J.K. Bump, and J.M. Grebmeier. 2005. Organic matter pathways to zooplankton and benthos under pack ice in late winter and open water in late summer in the north-central Bering Sea. Marine Ecology Progress Series 291:135–150, https://doi.org/10.3354/meps291135.
  42. Marty, J., and D. Planas. 2008. Comparison of methods to determine algal δ13C in freshwater. Limnology and Oceanography: Methods 6:51–63, https://doi.org/10.4319/lom.2008.6.51.
  43. Mathis, J.T., J.M. Grebmeier, D.A. Hansell, R.R. Hopcroft, D. Kirchman, S.H. Lee, and S.B. Moran. 2014. Carbon biogeochemistry of the Western Arctic: Production, export and ocean acidification. Pp. 223–268 in The Pacific Arctic Region: Ecosystem Status and Trends in a Rapidly Changing Environment. J. Grebmeier and W. Maslowski, eds, Springer, Dordrecht.
  44. Meon, B., and R.M. Amon. 2004. Heterotrophic bacterial activity and fluxes of dissolved free amino acids and glucose in the Arctic rivers Ob, Yenisei and the adjacent Kara Sea. Aquatic Microbial Ecology 37(2):121–135, https://doi.org/10.3354/ame037121.
  45. Moritz, R.E., C.M. Bitz, and E.J. Steig. 2002. Dynamics of recent climate change in the Arctic. Science 297:1,497–1,502, https://doi.org/10.1126/science.1076522.
  46. North, C.A., J.R. Lovvorn, J.M. Kolts, M.L. Brooks, L.W. Cooper, and J.M. Grebmeier. 2014. Deposit-feeder diets in the Bering Sea: Potential effects of climatic loss of sea ice-related microalgal blooms. Ecological Applications 24(6):1,525–1,542, https://doi.org/10.1890/13-0486.1.
  47. Perminova, I.V., I.V. Dubinenkov, A.S. Kononikhin, A.I. Konstantinov, A.Y. Zherebker, M.A. Andzhushev, V.A. Lebedev, E. Bulygina, R.M. Holmes, Y.I. Kostyukevich, and others. 2014. Molecular mapping of sorbent selectivities with respect to isolation of Arctic dissolved organic matter as measured by Fourier transform mass spectrometry. Environmental Science & Technology 48(13):7,461–7,468, https://doi.org/​10.1021/es5015423.
  48. Piccolo, M.C., C. Neill, and C.C. Cerri. 1994. Natural abundance of 15N in soils along forest-to-pasture chronosequences in the western Brazilian Amazon Basin. Oecologia 99(1–2):112–117, https://doi.org/10.1007/BF00317090.
  49. Pomeroy, L.R., P.J.leB. Williams, F. Azam, and J.E. Hobbie. 2007. The microbial loop. Oceanography 20(2):28–33, https://doi.org/10.5670/oceanog.2007.45.
  50. Riemann, B., and M. Søndergaard. 1984. Measurements of diel rates of bacterial secondary production in aquatic environments. Applied and Environmental Microbiology 47(4):632–638.
  51. Rusanov, I.I., A.S. Savvichev, S.K. Yusupov, N.V. Pimenov, and M.V. Ivanov. 1998. Production of exometabolites in the microbial oxidation of methane in marine ecosystems. Microbiology 67(5):590–596.
  52. Savvichev, A.S., I.I. Rusanov, N.V. Pimenov, E.E. Zakharova, E.F. Veslopolova, A.Yu. Lein, K. Crane, and M.V. Ivanov. 2007. Microbial processes of the carbon and sulfur cycles in the Chukchi Sea. Microbiology 76(5):603–613, https://doi.org/10.1134/S0026261707050141.
  53. Savvichev, A.S., E.E. Zakcharova, E.F. Weslopolova, I.I. Rusanov, A.Yu. Lein, and M.V. Ivanov. 2010. Microbial processes of the carbon and sulfur cycles in the Kara Sea. Oceanology 50(6):893–906, https://doi.org/10.1134/S0001437010060093.
  54. Sherr, B.F., and E.B. Sherr. 2003. Community respiration/production and bacterial activity in the upper water column of the central Arctic Ocean. Deep Sea Research Part I 50(4):529–542, https://doi.org/10.1016/S0967-0637(03)00030-X.
  55. Sirenko, B.I., and S.Y. Gagaev. 2007. Unusual abundance of macrobenthos and biological invasions in the Chukchi Sea. Russian Journal of Marine Biology 33(6):355–364, https://doi.org/10.1134/S1063074007060016.
  56. Sorokin, Y.I. 1998. Radioisotopic Methods in Hydrobiology. Springer-Verlag, Berlin Heidelberg New York, 321 pp.
  57. Stein, R., and R.W. Macdonald, eds. 2004. The Organic Carbon Cycle in the Arctic Ocean. Springer-Verlag, Heidelberg, 349 pp. 
  58. Steward, G.F., D.C. Smith, and F. Azam. 1996. Abundance and production of bacteria and viruses in the Bering and Chukchi Seas. Marine Ecology Progress Series 131:287–300, https://doi.org/​10.3354/meps131287.
  59. Stroeve, J.C., M.C. Serreze, M.M. Holland, J.E. Kay, J. Malanik, and A.P. Barrett. 2012. The Arctic’s rapidly shrinking sea ice cover: A research synthesis. Climatic Change 110:1,005–1,027, https://doi.org/​10.1007/s10584-011-0101-1.
  60. Vallières, C., L. Retamal, P. Ramlal, C.L. Osburn, and W.F. Vincent. 2008. Bacterial production and microbial food web structure in a large arctic river and the coastal Arctic Ocean. Journal of Marine Systems 74:756–773, https://doi.org/10.1016/​j.jmarsys.2007.12.002.
  61. Yun, M.S., T.E. Whitledge, M. Kong, and S.H. Lee. 2014. Low primary production in the Chukchi Sea shelf, 2009. Continental Shelf Research 76:1–11, https://doi.org/10.1016/j.csr.2014.01.001.
Copyright & Usage

This is an open access article made available under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution, and reproduction in any medium or format as long as users cite the materials appropriately, provide a link to the Creative Commons license, and indicate the changes that were made to the original content. Images, animations, videos, or other third-party material used in articles are included in the Creative Commons license unless indicated otherwise in a credit line to the material. If the material is not included in the article’s Creative Commons license, users will need to obtain permission directly from the license holder to reproduce the material.