Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The Effects of Oxygen Transition on Community Respiration and Potential Chemoautotrophic Production in a Seasonally Stratified Anoxic Estuary

Abstract

To assess the effects of seasonal oxygen transition on microbial metabolism, we measured spatiotemporal changes in total dissolved inorganic carbon, respiratory products, and geochemical constituents in the mesohaline region of Chesapeake Bay from May to October 2010. Vertical redox zonation was examined, and a spatial transect survey was also conducted from the southern to northern limit of the mesohaline region in July providing an alternative approach for assessing the temporal dynamics of oxygen transition. The transitions from oxic to hypoxic to anoxic and back to oxic were illustrated by the pattern of nitrogen redox species. Respiration, measured from changes in total dissolved inorganic carbon (∆DIC) and dissolved oxygen (∆DO) during incubations, had an average respiratory quotient (∆DIC/∆DO) of 1.04 ± 0.06 under oxic conditions and 1.58 ± 0.48 under hypoxic conditions. The difference in the respiratory quotients suggested that oxygen-based respiration measurements would underestimate community respiration rates in hypoxic conditions. In the present study, we observed within the surface-mixed layer three- to sevenfold differences in temporal and vertical variation of community respiration, while net respiration across oxyclines and anaerobic respiration in deep waters had lower rates and variability. In some anoxic samples, there was a net decrease in dissolved inorganic carbon that was exacerbated with experimental augmentation of terminal electron acceptors. Potential carbon fixation rates of chemoautotrophs within and below oxyclines were estimated and ranged from 0.63 to 116.9 mg C m−2 day−1 depending on growth conditions. These results indicate that anaerobic metabolism during the seasonal anoxic transition and at oxic/anoxic interface can play an important role in the estuarine carbon cycle.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

References

  1. Abril, G., M. Nogueira, H. Etcheber, G. Cabeçadas, E. Lemaire, and M.J. Brogueira. 2002. Behaviour of organic carbon in nine contrasting European estuaries. Estuarine, Coastal and Shelf Science 54: 241–262.

  2. Anderson, L.G., P.O.J. Hall, A. Iverfeldt, M.M.R. van der Loeff, B. Sundby, and S.F.G. Westerlund. 1986. Benthic respiration measured by total carbonate production. Limnology and Oceanography 31: 319–329.

  3. Andersson, M.G.I., N. Brion, and J.J. Middelburg. 2006. Comparison of nitrifier activity versus growth in the Scheldt estuary—a turbid, tidal estuary in northern Europe. Aquatic Microbial Ecology 42: 149–158.

  4. Apple, J.K., P.A. del Giorgio, and W.M. Kemp. 2006. Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary. Aquatic Microbial Ecology 43: 243–254.

  5. Bever, A.J., M.A.M. Friedrichs, C.T. Friedrichs, M.E. Scully, and L.W.J. Lanerolle. 2013. Combining observations and numerical model results to improve estimates of hypoxic volume within the Chesapeake Bay, USA. Journal of Geophysical Research: Oceans 118: 4924–4944.

  6. Bochdansky, A.B.., and S.M. Bollens. 2009. Thin layer formation during runaway stratification in the tidally dynamic San Francisco Estuary. Journal of Plankton Research 31: 1385–1390.

  7. Bourgault, D., F. Cyr, P.S. Galbraith, and E. Pelletier. 2012. Relative importance of pelagic and sediment respiration in causing hypoxia in a deep estuary. Journal of Geophysical Research 117, C08033.

  8. Boynton, W.R., and W.M. Kemp. 2000. Influence of river flow and nutrient loads on selected ecosystem processes. In Estuarine science: a synthetic approach to research and practice, 269–298. Washington, DC: Island.

  9. Brewer, P.G., and D.W. Spencer. 1971. Colorimetric determination of manganese in anoxic waters. Limnology and Oceanography 16: 107–110.

  10. Burdige, D.J. 1993. The biogeochemistry of manganese and iron reduction in marine sediments. Earth-Science Reviews 35: 249–284.

  11. Cai, W.-J., and Y. Wang. 1998. The chemistry, fluxes, and sources of carbon dioxide in the estuarine waters of the Satilla and Altamaha Rivers, Georgia. Limnology and Oceanography 43: 657–668.

  12. Capone, D.G., and R.P. Kiene. 1988. Comparison of microbial dynamics in marine and freshwater sediments: contrasts in anaerobic carbon catabolism. Limnology and Oceanography 33: 725–749.

  13. Casamayor, E.O., J. Garcia-Cantizano, J. Mas, and C. Pedros-Alio. 2001. Primary production in estuarine oxic/anoxic interfaces: contribution of microbial dark CO2 fixation in the Ebro River salt wedge estuary. Marine Ecology Progress Series 215: 49–56.

  14. Cloern, J.E., B.E. Cole, and R.S. Oremland. 1983. Autotrophic processes in meromictic Big Soda Lake, Nevada. Limnology and Oceanography 28: 1049–1061.

  15. Colt, J. (1984). Computation of dissolved gas concentrations in water as functions of temperature, salinity, and pressure. American Fisheries Society special publication no. 14.

  16. Cooper, S.R., and G.S. Brush. 1993. A 2,500-year history of anoxia and eutrophication in Chesapeake Bay. Estuaries 16: 617.

  17. Cornwell, J.C., and P.A. Sampou. (1995). Environmental controls on iron sulfide mineral formation in a coastal plain estuary. In Geochemical Transformations of Sedimentary Sulfur, 612:224–242. ACS Symposium Series 612. American Chemical Society.

  18. Cornwell, J.C., D.J. Conley, M.S. Owens, and J.C. Stevenson. 1996. A sediment chronology of the eutrophication of Chesapeake Bay. Estuaries 19: 488.

  19. Cowan, J.I., and W.R. Boynton. 1996. Sediment-water oxygen and nutrient exchanges along the longitudinal axis of Chesapeake Bay: seasonal patterns, controlling factors and ecological significance. Estuaries 19: 562–580.

  20. Cronin, W.B., and D.W. Pritchard. (1975). Additional statics on the dimensions of the Chesapeake Bay and its tributaries: cross-section widths and segment volumes per meter depth. Chesapeake Bay Institute Special Report 42, Reference 75–3.

  21. Crump, B.C., C. Peranteau, B. Beckingham, and J.C. Cornwell. 2007. Respiratory succession and community succession of bacterioplankton in seasonally anoxic estuarine waters. Applied and Environmental Microbiology 73: 6802–6810.

  22. Diaz, R.J., and R. Rosenberg. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321: 926–929.

  23. Epping, E.H.G., V. Schoemann, and H. de Heij. 1998. Manganese and iron oxidation during benthic oxygenic photosynthesis. Estuarine, Coastal and Shelf Science 47: 753–767.

  24. Etemad-Shahidi, A., and J. Imberger. 2002. Anatomy of turbulence in a narrow and strongly stratified estuary. Journal of Geophysical Research: Oceans 107: 7–1–7–16.

  25. Fortunato, C.S., and B.C. Crump. 2011. Bacterioplankton community variation across river to ocean environmental gradients. Microbial Ecology 62: 374–382.

  26. Gattuso, J.-P., M. Frankignoulle, and R. Wollast. 1998. Carbon and carbonate metabolism in coastal aquatic ecosystems. Annual Review of Ecology and Systematics 29: 405–434.

  27. Giblin, A.E., N.B. Weston, G.T. Banta, J. Tucker, and C.S. Hopkinson. 2010. The effects of salinity on nitrogen losses from an oligohaline estuarine sediment. Estuaries and Coasts 33: 1054–1068.

  28. Goyet, C., and S.D. Hacker. 1992. Procedure for calibration of a coulometric system used for total inorganic carbon measurements of seawater. Marine Chemistry 38: 37–51.

  29. Goyet, C., and A.K. Snover. 1993. High-accuracy measurements of total dissolved inorganic carbon in the ocean: comparison of alternate detection methods. Marine Chemistry 44: 235–242.

  30. Hagy, J.D., W.R. Boynton, C.W. Keefe, and K.V. Wood. 2004. Hypoxia in Chesapeake Bay, 1950–2001: long-term change in relation to nutrient loading and river flow. Estuaries 27: 634–658.

  31. Hamdan, L.J., and R.B. Jonas. 2006. Seasonal and interannual dynamics of free-living bacterioplankton and microbially labile organic carbon along the salinity gradient of the Potomac River. Estuaries and Coasts 29: 40–53.

  32. Harding, L.W. 1994. Long-term trends in the distribution of phytoplankton in Chesapeake Bay: roles of light, nutrients and streamflow. Marine Ecology Progress Series 104: 267–291.

  33. Hargrave, B.T., and G.A. Phillips. 1981. Annual in situ carbon dioxide and oxygen flux across a subtidal marine sediment. Estuarine, Coastal and Shelf Science 12: 725–737.

  34. Holland, A., A. Shaughnessy, and M. Hiegel. 1987. Long-term variation in mesohaline Chesapeake Bay macrobenthos: spatial and temporal patterns. Estuaries and Coasts 10: 227–245.

  35. Hopkinson, C.S., and E.M. Smith. 2005. Estuarine respiration: an overview of benthic, pelagic, and whole system respiration. In Respiration in aquatic ecosystems, ed. P.A. del Giogio and P.J. leb Williams, 122–146. New York: Oxford University Press.

  36. Horrigan, S.G., J.P. Montoya, J.L. Nevins, J.J. McCarthy, H. Ducklow, R. Goericke, and T. Malone. 1990. Nitrogenous nutrient transformations in the spring and fall in the Chesapeake Bay. Estuarine, Coastal and Shelf Science 30: 369–391.

  37. Huang, W.-J., Y. Wang, and W.-J. Cai. 2012. Assessment of sample storage techniques for total alkalinity and dissolved inorganic carbon in seawater. Limnology and Oceanography: Methods 10: 711–717.

  38. Jiang, L.-Q., W.-J. Cai, and Y. Wang. 2008. A comparative study of carbon dioxide degassing in river- and marine-dominated estuaries. Limnology and Oceanography 53: 2603–2615.

  39. Jiang, L.-Q., W.-J. Cai, Y. Wang, J. Diaz, P.L. Yager, and X. Hu. 2010. Pelagic community respiration on the continental shelf off Georgia, USA. Biogeochemistry 98: 101–113.

  40. Jonas, R.B. 1997. Bacteria, dissolved organics and oxygen consumption in salinity stratified Chesapeake Bay, an anoxia paradigm. American Zoologist 37: 612–620.

  41. Jonas, R.B., and J.H. Tuttle. 1990. Bacterioplankton and organic carbon dynamics in the lower mesohaline Chesapeake Bay. Applied Environmental Microbiology 56: 747–757.

  42. Jordan, T.E., J.C. Cornwell, W.R. Boynton, and J.T. Anderson. 2008. Changes in phosphorus biogeochemistry along an estuarine salinity gradient: the iron conveyer belt. Limnology and Oceanography 53: 172–184.

  43. Joye, S.B., and J.T. Hollibaugh. 1995. Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270: 623–625.

  44. Kan, J., C.C. Byron, K. Wang, and F. Chen. 2006. Bacterioplankton community in Chesapeake Bay: predictable or random assemblages. Limnology and Oceanography 51: 2157–2169.

  45. Kana, T.M., C. Darkangelo, M.D. Hunt, J.B. Oldham, G.E. Bennett, and J.C. Cornwell. 1994. Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Analytical Chemistry 66: 4166–4170.

  46. Kemp, W.M., P.A. Sampou, J. Garber, J. Tuttle, and W.R. Boynton. 1992. Seasonal depletion of oxygen from bottom waters of Chesapeake Bay: roles of benthic and planktonic respiration and physical exchange processes. Marine Ecology Progress Series 85: 137–152.

  47. Kemp, W.M., E.M. Smith, M. Marvin-Dipasquale, and W.R. Boynton. 1997. Organic carbon balance and net ecosystem metabolism in Chesapeake Bay. Marine Ecology Progress Series 150: 229–248.

  48. Labrenz, M., G. Jost, C. Pohl, S. Beckmann, W. Martens-Habbena, and K. Jurgens. 2005. Impact of different in vitro electron donor/acceptor conditions on potential chemolithoautotrophic communities from marine pelagic redoxclines. Applied and Environmental Microbiology 71: 6664–6672.

  49. Lane, L., S. Rhoades, C. Thomas, and L. Van Heukelem. 2000. Standard operating procedures 2000. University of Maryland Horn Point Laboratory Technical Report No. TS-264-00.

  50. leB Williams, P.J., and P.A. del Giorgio. 2005. Respiration in aquatic ecosystems: history and background. In Respiration in aquatic ecosystems, 1–17. New York: Oxford University Press.

  51. Li, M., L. Zhong, W.C. Boicourt, S. Zhang, and D.-L. Zhang. 2007. Hurricane-induced destratification and restratification in a partially-mixed estuary. Journal of Marine Research 65: 169–192.

  52. Lin, X., M.I. Scranton, A.Y. Chistoserdov, R. Varela, and G.T. Taylor. 2008. Spatiotemporal dynamics of bacterial populations in the anoxic Cariaco Basin. Limnology and Oceanography 53: 37–51.

  53. Lipschultz, F., S.C. Wofsy, and L.E. Fox. 1986. Nitrogen metabolism of the eutrophic Delaware River ecosystem. Limnology and Oceanography 31: 701–716.

  54. Llirós, M., L. Alonso‐Sáez, F. Gich, A. Plasencia, O. Auguet, E.O. Casamayor, and C.M. Borrego. 2011. Active bacteria and archaea cells fixing bicarbonate in the dark along the water column of a stratified eutrophic lagoon. FEMS Microbiology Ecology 77: 370–384.

  55. Lomas, M.W., and F. Lipschultz. 2006. Forming the primary nitrite maximum: nitrifiers or phytoplankton? Limnology and Oceanography 51: 2453–2467.

  56. Malone, T.C., W.M. Kemp, H.W. Ducklow, W.R. Boynton, J.H. Tuttle, and R.B. Jonas. 1986. Lateral variation in the production and fate of phytoplankton in a partially stratified estuary. Marine Ecology Progress Series 32: 149–160.

  57. Malone, T.C., D.J. Conley, T.R. Fisher, P.M. Glibert, L.W. Harding, and K.G. Sellner. 1996. Scales of nutrient-limited phytoplankton productivity in Chesapeake Bay. Estuaries and Coasts 19: 371–385.

  58. Martens-Habbena, W., P.M. Berube, H. Urakawa, J.R. de la Torre, and D.A. Stahl. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461: 976–979.

  59. Marvin-DiPasquale, M.C., and D.G. Capone. 1998. Benthic sulfate reduction along the Chesapeake Bay central channel. I. Spatial trends and controls. Marine Ecology Progress Series 168: 213–228.

  60. McCallister, S.L., J.E. Bauer, H.W. Ducklow, and E.A. Canuel. 2006. Sources of estuarine dissolved and particulate organic matter: a multi-tracer approach. Organic Geochemistry 37: 454–468.

  61. McCarthy, J.J., W. Kaplan, and J.L. Nevins. 1984. Chesapeake Bay nutrient and plankton dynamics. 2. Sources and sinks of nitrite. Limnology and Oceanography 29: 84–98.

  62. McDonough, R.J., R.W. Sanders, K.G. Porter, and D.L. Kirchman. 1986. Depth distribution of bacterial production in a stratified lake with an anoxic hypolimnion. Applied and Environmental Microbiology 52: 992–1000.

  63. Middelburg, J.J., and L.A. Levin. 2009. Coastal hypoxia and sediment biogeochemistry. Biogeosciences 6: 1273–1293.

  64. Nealson, K.H., and C.R. Myers. 1992. Microbial reduction of manganese and iron: new approaches to carbon cycling. Applied and Environmental Microbiology 58: 439–443.

  65. Oviatt, C.A., D.T. Rudnick, A.A. Keller, P.A. Sampou, and G.T. Almquist. 1986. A comparison of system (O2 and CO2) and C-14 measurements of metabolism in estuarine mesocosms. Marine Ecology Progress Series 28: 57–67.

  66. Parsons, T.R., Y. Maita, and C.M. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. Elmsford: Pergamon.

  67. Pierson, J.J., M.R. Roman, D.G. Kimmel, W.C. Boicourt, and X. Zhang. 2009. Quantifying changes in the vertical distribution of mesozooplankton in response to hypoxic bottom waters. Journal of Experimental Marine Biology and Ecology 381: S74–S79.

  68. Pomeroy, L.R., and W.J. Wiebe. 2001. Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquatic Microbial Ecology 23: 187–204.

  69. Robinson, C. 2008. Heterotrophic bacterial respiration. In Microbial ecology of the oceans, ed. D.L. Kirchman, 299–334. Hoboken: Wiley.

  70. Roden, E.E., and J.H. Tuttle. 1992. Sulfide release from estuarine sediments underlying anoxic bottom water. Limnology and Oceanography 37: 725–738.

  71. Roden, E.E., J.H. Tuttle, W.R. Boynton, and W.M. Kemp. 1995. Carbon cycling in mesohaline Chesapeake Bay sediments. 1. POC deposition rates and mineralization pathways. Journal of Marine Research 53: 799–819.

  72. Sampou, P., and W.M. Kemp. 1994. Factors regulating plankton community respiration in Chesapeake Bay. Marine Ecology Progress Series 110: 249–258.

  73. Scully, M.E. 2010. Wind modulation of dissolved oxygen in Chesapeake Bay. Estuaries and Coasts 33: 1164–1175.

  74. Shiah, F.-K., and H.W. Ducklow. 1994. Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate in Chesapeake Bay. Limnology and Oceanography 39: 1243–1258.

  75. Smith, S.V., and J. Hollibaugh. 1993. Coastal metabolism and the oceanic organic carbon balance. Review of Geophysics. 31: 75–89.

  76. Smith, E.M., and W.M. Kemp. 1995. Seasonal and regional variations in plankton community production and respiration for Chesapeake Bay. Marine Ecology Progress Series 116: 217–231.

  77. Smith, E.M., and W.M. Kemp. 2001. Size structure and the production/respiration balance in a coastal plankton community. Limnology and Oceanography 46: 473–485.

  78. Sun, M.-Y., C. Lee, and R.C. Aller. 1993. Laboratory studies of oxic and anoxic degradation of chlorophyll-a in Long Island Sound sediments. Geochimica et Cosmochimica Acta 57: 147–157.

  79. Trouwborst, R.E., B.G. Clement, B.M. Tebo, B.T. Glazer, and G.W. Luther. 2006. Soluble Mn (III) in suboxic zones. Science 313: 1955–1957.

  80. Veuger, B., A. Pitcher, S. Schouten, J.S. Sinninghe Damsté, and J.J. Middelburg. 2013. Nitrification and growth of autotrophic nitrifying bacteria and Thaumarchaeota in the coastal North Sea. Biogeosciences 10: 1775–1785.

  81. Watson, S.W., E. Bock, F.W. Valois, J.B. Waterbury, and U. Schlosser. 1986. Nitrospira marina gen. nov. sp. nov.: a chemolithotrophic nitrite-oxidizing bacterium. Archives of Microbiology 144: 1–7.

  82. Wienke, S.M., and J.E. Cloern. 1987. The phytoplankton component of seston in San Francisco Bay. Netherlands Journal of Sea Research 21: 25–33.

  83. Wissel, B., J. Zoraida Quiones-Rivera, and F. Brian. 2008. Combined analyses of O2 and CO2 for studying the coupling of photosynthesis and respiration in aquatic systems. Canadian Journal of Fisheries and Aquatic Sciences 65: 2378–2388.

  84. Wright, J.J., K.M. Konwar, and S.J. Hallam. 2012. Microbial ecology of expanding oxygen minimum zones. Nature Reviews Microbiology 10: 381–394.

  85. Zaikova, E., D.A. Walsh, C.P. Stilwell, W.W. Mohn, P.D. Tortell, and S.J. Hallam. 2010. Microbial community dynamics in a seasonally anoxic fjord: Saanich Inlet, British Columbia. Environmental Microbiology 12: 172–191.

  86. Zhai, W., M. Dai, and X. Guo. 2007. Carbonate system and CO2 degassing fluxes in the inner estuary of Changjiang (Yangtze) River, China. Marine Chemistry 107: 342–356.

  87. Zimmerman, A.R., and E.A. Canuel. 2000. A geochemical record of eutrophication and anoxia in Chesapeake Bay sediments: anthropogenic influence on organic matter composition. Marine Chemistry 69: 117–137.

  88. Zopfi, J., T.G. Ferdelman, B.B. Jørgensen, A. Teske, and B. Thamdrup. 2001. Influence of water column dynamics on sulfide oxidation and other major biogeochemical processes in the chemocline of Mariager Fjord (Denmark). Marine Chemistry 74: 29–51.

Download references

Acknowledgments

We thank Bernadette Gross, Molly George, Debbie Hinkle, and the captain and crew of the R/V Hugh R. Sharp for their assistance in collecting the samples and analyzing the data. We also thank Todd Kana, Alyson Santoro, and two anonymous reviewers for providing helpful suggestions and many useful comments on the manuscript. Yongchen Wang who dedicated his scientific career to the understanding of carbon cycles provided invaluable help with DIC analysis and greatly improved the quality of our DIC measurement. This work was supported by the National Science Foundation (Grant OCE-0961920). This is UMCES contribution 4882.

Author information

Correspondence to Dong Y. Lee.

Additional information

Communicated by Alberto Vieira Borges

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lee, D.Y., Owens, M.S., Doherty, M. et al. The Effects of Oxygen Transition on Community Respiration and Potential Chemoautotrophic Production in a Seasonally Stratified Anoxic Estuary. Estuaries and Coasts 38, 104–117 (2015). https://doi.org/10.1007/s12237-014-9803-8

Download citation

Keywords

  • Respiration
  • Hypoxia
  • Dissolved inorganic carbon
  • Chemoautotrophy
  • Chesapeake Bay