Comparison of nutrient and microbial dynamics over a seasonal cycle in a mid-Atlantic coastal lagoon prone to Aureococcus anophagefferens (brown tide) blooms

Estuaries and Coasts

Volumn 32, Issue 6, 2009, Pages 1176-1194

  Mulholland, Margaret R ^a   Boneillo, George E ^a   Bernhardt, Peter W ^a   Minor, Elizabeth C ^b  

^a OLD DOMINION UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA DULUTH   (United States)

Author keywords

Aureococcus anophagefferens; Brown tide; Dissolved organic matter; Nutrients

Indexed keywords

ABUNDANCE; BACTERIUM; BICARBONATE; BROWN TIDE; COASTAL LAGOON; COMPARATIVE STUDY; DISSOLVED ORGANIC MATTER; HYDROLYSIS; MICROBIAL ACTIVITY; NUTRIENT DYNAMICS; PEPTIDE; SEASONAL VARIATION; UREA;

CHINCOTEAGUE BAY; NORTH AMERICA; UNITED STATES;

AUREOCOCCUS ANOPHAGEFFERENS; BACTERIA (MICROORGANISMS);

EID: 70449602702     PISSN: 15592723     EISSN: 15592731     Source Type: Journal    
DOI: 10.1007/s12237-009-9218-0     Document Type: Article

References (61)

1. Allen, T. R., H. Tolvanen, G. F. Oertel, and G. McLeod. 2005. Spatial Analysis and Ecological Applications of Tidal Flushing and Wave Exposure in Chincoteague Bay, Virginia, USA. Presented at the Estuarine Research Federation Biannual Meeting, 16-21 Oct 2005, Norfolk, Virginia.
2. Anderson, D. M., D. M. Kulis, and E. M. Cosper. 1989. Immunofluorescent detection of the 'brown tide' organism, Aureococcus anophagefferens. In Novel phytoplankton blooms: Causes and impacts of recurrent brown tides and other unusual blooms. Lecture notes on coastal and estuarine studies, ed. E. M. Cosper, V. M. Bricelj, and E. J. Carpenter, 213-228. New York: Springer.
3. Bell, R. T. 1993. Estimating production of heterotrophic bacterioplankton via incorporation of tritiated thymidine. In Handbook of methods in aquatic microbial ecology, ed. P. F. Kemp, B. F. Sherr, E. B. Sherr, and J. J. Cole, 495-504. Boca Raton: Lewis.
4. Benner, R. 2002. Chemical composition and reactivity. In Biogeochemistry of marine dissolved organic matter, ed. D. A. Hansell and C. A. Carlson, 59-90. New York: Academic.
5. Berg, G. M., P. M. Glibert, M. W. Lomas, and M. Burford. 1997. Organic nitrogen uptake and growth by the chrysophyte Aureococcus anophagefferens during a brown tide event. Marine Biology 227: 377-387.
6. Berg, G. M., D. J. Repeta, and J. Laroche. 2002. Dissolved organic nitrogen hydrolysis rates in axenic cultures of Aureococcus anophagefferens (Pelagophyceae): Comparison with heterotrophic bacteria. Applied Environmental Microbiology 68: 401-404.
7. Berg, G. M., D. J. Repeta, and J. Laroche. 2003. The role of the picoeukaryote Aureococcus anophagefferens in cycling of marine high-molecular weight dissolved organic nitrogen. Limnology and Oceanography 48: 1825-1830.
8. Berman, T. and D. A. Bronk. 2003. Dissolved organic nitrogen: A dynamic participant in aquatic ecosystems. Aquatic Microbial Ecology 31: 279-305.
9. Bouvier, T. C. and P. A. del Giorgio. 2002. Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnology and Oceanography 47: 453-470.
10. Breuer, E., S. A. Sañudo-Wilhelmy, and R. C. Aller. 1999. Trace metals and dissolved organic carbon in an estuary with restricted river flow and a brown tide. Estuaries 22: 603-615.
11. Bronk, D. A. 2002. Dynamics of DON. In Biogeochemistry of marine dissolved organic matter, ed. D. A. Hansell and C. A. Carlson, 153-249. New York: Academic.
12. Burdige, D. J. and J. Homstead. 1994. Fluxes of dissolved organic carbon from Chesapeake Bay sediments. Geochimica Cosmochimica Acta 58: 3407-3424.
13. Burkholder, J. M., P. M. Glibert, and H. M. Skelton. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8: 77-93.
14. Caron, D. A., M. R. Dennett, D. M. Moran, R. A. Schaffner, D. J. Lonsdale, C. J. Gobler, R. Nuzzi, and T. I. McLean. 2003. Development and application of a monoclonal-antibody technique for counting Aureococcus anophagefferens, an alga causing recurrent brown tides in the mid-Atlantic United States. Applied Environmental Microbiology 69: 5492-5502.
15. Cole, J. J., S. Findlay, and M. L. Pace. 1988. Bacterial production in fresh and saltwater ecosystems: A cross-system overview. Marine Ecology Progress Series 43: 1-10.
16. Cottrell, M. T. and D. L. Kirchman. 2003. Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary. Limnology and Oceanography 48: 168-178.
17. Cowie, G. L. and J. I. Hedges. 1992. Improved amino acid quantification in environmental samples: Charged-matched recovery standards and reduced analysis time. Marine Chemistry 37: 223-238.
18. Del Giorgio, P. A. and J. J. Cole. 1998. Bacterial growth efficiency in natural aquatic systems. Annual Review of Ecology Systematics 29: 503-541.
19. Ducklow, H. W. 2000. Bacterial production and biomass in the oceans. In Microbial ecology of the oceans, ed. D. L. Kirchman, 85-120. New York: Wiley-Liss.
20. Dzurica, S., C. Lee, E. M. Cosper, and E. J. Carpenter. 1989. Role of environmental variables, specifically organic compounds and micronutrients, in the growth of the chrysophyte Aureococcus anophagefferens. In Novel phytoplankton blooms: Causes and impacts of recurrent brown tides and other unusual blooms, ed. E. M. Cosper, V. M. Bricelj, and E. J. Carpenter, 229-252. New York: Springer.
21. Fandino, L. B., L. Riemann, G. F. Steward, R. A. Long, and F. Azam. 2001. Variations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16S rDNA sequencing. Aquatic Microbial Ecology 23: 119-130.
22. Gastrich, M. D., O. R. Anderson, S. S. Benmayor, and E. M. Cosper. 1998. Ultrastructural analysis of viral infection in the brown-tide alga, Aureococcus anophagefferens (Pelagophyceae). Phycologia 37: 300-306.
23. Glibert, P. M. and D. G. Capone. 1993. Mineralization and assimilation in aquatic, sediment, and wetland systems. In Nitrogen isotope techniques, ed. R. Knowles and T. H. Blackburn, 243-271. San Diego: Academic.
24. Glibert, P. M., R. Magnien, M. W. Lomas, J. Alexander, C. Fan, E. Haramoto, M. Trice, and T. M. Kana. 2001. Harmful algal blooms in the Chesapeake and coastal bays of Maryland, USA: Comparison of 1997, 1998, and 1999 events. Estuaries 24: 875-883.
25. Gobler, C. J., D. A. Hutchins, N. S. Fisher, E. M. Cosper, and S. A. Sañudo-Wilhelmy. 1997. Release and bioavailability of C, N, P, Se, and Fe following viral lysis of a marine chrysophyte. Limnology and Oceanography 42: 1492-1504.
26. Gobler, C. J. and S. A. Sañudo-Wilhelmy. 2001a. Effects of organic carbon, organic nitrogen, inorganic nutrients, and iron additions on the growth of phytoplankton and bacteria during a brown tide bloom. Marine Ecology Progress Series 209: 19-34.
27. Gobler, C. J. and S. A. Sañudo-Wilhelmy. 2001b. Temporal variability of groundwater seepage and brown tide blooms in a Long Island embayment. Marine Ecology Progress Series 217: 299-309.
28. Gobler, C. J., M. J. Renaghan, and N. J. Buck. 2002. Impacts of nutrient and grazing mortality on the abundance of Aureococcus anophagefferens during a New York brown tide bloom. Limnology and Oceanography 47: 129-141.
29. Gobler, C. J., S. Deonarine, J. Leigh-Bell, M. D. Gastrich, O. R. Anderson, and S. W. Wilhelm. 2004. Ecology of phytoplankton communities dominated by Aureococcus anophagefferens: The role of viruses, nutrients, and microzooplankton grazing. Harmful Algae 3: 471-483.
30. Gobler, C. J., D. J. Lonsdale, and G. L. Boyer. 2005. A review of the causes, effects, and potential management of harmful brown tide blooms caused by Aureococcus anophagefferens (Hargraves et Sieburth). Estuaries 28: 726-749.
31. Kana, T. M., M. W. Lomas, H. L. MacIntyre, J. C. Cornwell, and C. J. Gobler. 2004. Stimulation of the brown tide organism, Aureococcus anophagefferens, by selective nutrient additions to in situ mesocosms. Harmful Algae 3: 377-388.
32. Kelly, K. M. and A. Y. Chistoserdov. 2001. Phylogenetic analysis of the succession of bacterial communities in the Great South Bay (Long Island). FEMS Microbiol Ecology 35: 85-95.
33. Kirchman, D. L. 1993. Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In Handbook of methods in aquatic microbial ecology, ed. P. F. Kemp, B. F. Sherr, E. B. Sherr, and J. J. Cole, 509-512. Boca Raton: Lewis.
34. Kirchman, D. L. 2000. Uptake and regeneration of inorganic nutrients by marine heterotrophic bacteria. In Microbial ecology of the oceans, ed. D. L. Kirchman, 261-288. New York: Wiley-Liss.
35. Kirchman, D. L., A. I. Dittel, S. E. G. Findlay, and D. Fischer. 2004. Changes in bacterial activity and community structure in response to dissolved organic matter in the Hudson River, New York. Aquatic Microbial Ecology 35: 243-257.
36. Kristiansen, J. 1990. Phylum Chrysophyta. In Handbook of protista, ed. L. Margulis, J. O. Corliss, M. Melkonian, and D. J. Chapman, 438-453. Sudbury: Jones and Bartlett.
37. LaRoche, J., R. Nuzzi, R. Waters, K. Wyman, P. G. Falkowski, and D. W. R. Wallace. 1997. Brown tide blooms in Long Island's coastal waters linked to variability in groundwater flow. Global Change Biology 3: 397-410.
38. Lewitus, A. J. 2006. Osmotrophy in marine microalgae. In Algal cultures, analogues and blooms, ed. D. V. Subba Rao, 343-383. Enfield: Science.
39. Lomas, M. W., P. M. Glibert, G. M. Berg, and M. Burford. 1996. Characterization of nitrogen uptake by natural populations of Aureococcus anophagefferens (Chrysophyceae) as a function of incubation duration, substrate concentration, light and temperature. Journal of Phycology 32: 907-916.
40. Lomas, M. W., P. M. Glibert, D. A. Clougherty, D. R. Huber, J. Jones, J. Alexander, and E. Haramoto. 2001. Elevated organic nutrient ratios associated with brown tide algal blooms of Aureococcus anophagefferens (Pelagophyceae). Journal of Plankton Research 23: 1339-1344.
41. Lomas, M. W., T. M. Kana, H. L. MacIntyre, J. C. Cornwell, R. Nuzzi, and R. Waters. 2004. Interannual variability of Aureococcus anophagefferens in Quantuck Bay, Long Island: Natural test of the DON hypothesis. Harmful Algae 3: 389-402.
42. Milligan, A. J. and E. M. Cosper. 1997. Growth and photosynthesis of the "brown tide" microalga Aureaococcus anophagefferens in subsaturating constant and fluctuating irradiance. Marine Ecology Progress Series 153: 67-75.
43. Minor, E. C., J. P. Simjouw, and M. R. Mulholland. 2006. Seasonal variations in dissolved organic carbon concentrations and characteristics in a shallow coastal bay. Marine Chemistry 101: 166-179.
44. Mulholland, M. R., P. M. Glibert, and C. Lee. 2003. Nitrogen cycling along a nutrient and salinity gradient in the Pocomoke River, Maryland: Amino acid oxidation, peptide hydrolysis and uptake of inorganic and organic nitrogen. Marine Ecology Progress Series 258: 3-17.
45. Mulholland, M. R., C. J. Gobler, and C. Lee. 2002. Peptide hydrolysis, amino acid oxidation and n uptake in communities seasonally dominated by Aureococcus anophagefferens. Limnology and Oceanography 47: 1094-1108.
46. Mulholland, M. R., G. Boneillo, and E. C. Minor. 2004. A comparison of n and c uptake during brown tide (Aureococcus anophagefferens) blooms from two coastal bays on the east coast of the USA. Harmful Algae 3: 361-376.
47. Mulholland, M. R. and C. Lee. 2009. Peptide hydrolysis and dipeptide uptake in cultures and natural communities dominated by phytoplankton mixotrophs. Limnology and Oceanography 54: 856-868.
48. Pantoja, S., C. Lee, and J. F. Marecek. 1997. Hydrolysis of peptides in seawater and sediments. Marine Chemistry 57: 25-40.
49. Parsons, T. R., Y. Maita, and C. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. New York: Pergamon.
50. Porter, K. G. and Y. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25: 943-948.
51. Price, N. and P. J. Harrison. 1987. Comparison of methods for the analysis of dissolved urea in seawater. Marine Biology 94: 307-317.
52. Rooney-Varga, J. N., M. W. Giewat, M. C. Savin, S. Sood, M. LeGresley, and J. L. Martin. 2005. Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microbial Ecology 49: 163-175.
53. Sieracki, M. E., C. J. Gobler, T. L. Cucci, E. C. Thier, I. C. Gilg, and M. D. Keller. 2004. Pico-and nanoplankton dynamics during bloom initiation of Aureococcus in a Long Island, NY bay. Harmful Algae 3: 459-470.
54. Simjouw, J. P., M. R. Mulholland, and E. C. Minor. 2004. Molecular-level characteristics of dissolved organic matter in Chincoteague Bay prior to and during an Aureococcus anophagefferens bloom. Estuaries 27: 986-998.
55. Stauffer, B. A., R. A. Schaffner, C. Wazniak, and D. A. Caron. 2008. An immunofluorescent flow cytometric technique for counting the brown tide alga, Aureococcus anophagefferens. Applied and Environmental Microbiology. doi: 10. 1128/AEM. 00996-08.
56. Tango, P., W. Butler, and C. Wazniak. 2004. Analysis of phytoplankton populations in the Maryland Coastal Bays. In Maryland's Coastal Bays: An ecosystem health assessment 2004. DNR-12-1202-0009, ed. C. E. Wazniak and M. R. Hall. Annapolis: Maryland Department of Natural Resources, Tidewater Ecosystem Assessment.
57. Taylor, G. T., C. J. Gobler, and S. A. Sañudo-Wilhelmy. 2006. Speciation and concentrations of dissolved nitrogen as determinants of brown tide Aureococcus anophagefferens bloom initiation. Marine Ecology Progress Series 312: 67-83.
58. Trice, T. M., P. M. Glibert, C. Lea, and L. van Heukelem. 2004. HPLC pigment records provide evidence of past blooms of Aureococcus anophagefferens in the Coastal Bays of Maryland and Virginia, USA. Harmful Algae 3: 295-304.
59. Valderrama, J. C. 1981. The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Marine Chemistry 10: 109-122.
60. Wazniak, C. E. and P. M. Glibert. 2004. Potential impacts of brown tide, Aureococcus anophagefferens, on juvenile hard clams, Mercenaria mercenaria, in the Coastal Bays of Maryland, USA. Harmful Algae 3: 321-329.
61. Welschmeyer, N. A. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography 39: 1985-1992.