Antonie van Leeuwenhoek

, Volume 81, Issue 1–4, pp 487–507 | Cite as

Characterizing man-made and natural modifications of microbial diversity and activity in coastal ecosystems

  • Hans W. PaerlEmail author
  • Julianne Dyble
  • Luke Twomey
  • James L. Pinckney
  • Joshua Nelson
  • Lee Kerkhof


The impacts of growing coastal pollution and habitat alteration accompanying human encroachment are of great concern at the microbial level, where much of the ocean's primary production and biogeochemical cycling takes place. Coastal ecosystems are also under the influence of natural perturbations such as major storms and flooding. Distinguishing the impacts of natural and human stressors is essential for understanding environmentally-induced change in microbial diversity and function. The objective of this paper is to discuss the applications and merits of recently developed molecular, ecophysiological and analytical indicators and their utility in examining anthropogenic and climatic impacts on the structure and function of coastal microbial communities. The nitrogen-limited Neuse River Estuary and Pamlico Sound, North Carolina are used as examples of ecosystems experiencing both anthropogenic (i.e., accelerating eutrophication) and climatic stress (increasing frequencies of tropical storms and hurricanes). Additional examples are derived from a coastal monitoring site (LEO) on the Atlantic coast of New Jersey and Galveston Bay, on the Gulf of Mexico. In order to assess structure, function, and trophic state of these and other coastal ecosystems, molecular (DNA and RNA-based) characterizations of the microbial taxa involved in carbon, nitrogen and other nutrient transformations can be combined with diagnostic pigment-based indicators of primary producer groups. Application of these methods can reveal process-level microbial community responses to environmental variability over a range of scales. Experimental approaches combined with strategic monitoring utilizing these methods will facilitate: (a) understanding organismal and community responses to environmental change, and (b) synthesizing these responses in the context of ecosystem models that integrate physical, chemical and biotic variability with environmental controls.

Bacteria climate change eutrophication microbial consortia nutrient cycling phytoplankton pollution water quality 


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  1. Affourtit J, Zehr JP & Paerl HW (2001) Distribution of nitrogen-fixing microorganisms along the Neuse River Estuary, North Carolina. Microbial Ecol. 41: 114–123.Google Scholar
  2. Amann RI, Ludwig W & Schleifer K-H (1995) Phylogentic identification and in situ detedction of individual microbial cells without cultivation. Microbiol. Rev. 59(1): 143–169.PubMedGoogle Scholar
  3. Ambio (1990) Marine Eutrophication. Ambio 19: 101–176.Google Scholar
  4. Antia NP, Harrison, G & Oliveira L (1991) The role of dissolved organic nitrogen in phytoplankton nutrietion, cell biology and ecology. Phycologia 30: 1–89.Google Scholar
  5. Avaniss-Aghajani E, Jones K, et al. (1994) A molecular technique for identification of bacteria using small subunit ribosomal RNA sequences. Biotechniques 17(1): 144–6.PubMedGoogle Scholar
  6. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA & Thingstadt F (1983) The ecological role of water-column microbes in the sea. Marine Ecol. Prog. Ser. 10: 257–263.Google Scholar
  7. Banse K (1977) Determining the carbon-to-chlorophyll ratio of natural phytoplankton. Marine Biology 41: 199–212.CrossRefGoogle Scholar
  8. Benoit G, Oktay S, Cantu A, Hood ME, Coleman C, Corapcioglu O & Santschi PH (1994) Partitioning of Cu, Pb, Ag, Zn, Fe, Al, and Mn between filter-retained particles, colloids and solution in six Texas estuaries. Marine Chem. 45: 307–336.CrossRefGoogle Scholar
  9. Bowers HA, Tengs T, Glasgow, HBJr, Burkholder JM, Rublee PA & Oldach DW (2000) Development of real-time PCR assays for rapid detection of Pfiesteria piscicida and related dinoflagellates. Appl. Environ. Microbiol. 66: 4641–4648.CrossRefPubMedGoogle Scholar
  10. Boyer JN, Stanley DW, & Christian RR (1994) Dynamics of NH4+ and NO3-uptake in the water column of the Neuse River Estuary, North Carolina. Estuaries 17: 361–371.CrossRefGoogle Scholar
  11. Boyton WR., Garber JH, Summers R & Kemp WM (1995) Inputs, transformations, and transport of nitrogen and phosphorus in Chesapeake Bay and selected tributaries. Estuaries 18: 285–314.CrossRefGoogle Scholar
  12. Collos Y (1989) A linear model of external interactions during uptake of different forms of inorganic nitrogen by microalgae. J. Plankton Res. 11: 521–533.Google Scholar
  13. Copeland BJ & Gray J (1991) Status and Trends Report of the Albemarle-Pamlico Estuary. steel J (Ed), Albemarle-Pamlico Estuarine Study Report 90-01. NC Dept. of Environ. Health & Nat. Resources, Raleigh.Google Scholar
  14. Carmichael WW (1997) The cyanotoxins. Adv. Bot. Res. 27: 211–256.CrossRefGoogle Scholar
  15. Cloern JE, Grenz C & Vidergar-Lucas L (1995) An empirical model of the phytoplankton chlorophyll: carbon ratio - the conversion factor between productivity and growth rate. Limnol. Oceanogr. 40: 1313–1321.Google Scholar
  16. Cosper EM, Dennison WC, Carpenter EJ, Bricelj VM, Mitchell JG, Kuenstner SH, Colflesh D & Dewey M (1987) Recurrent and persistent brown tide blooms perturb coastal marine ecosystem. Estuaries 10: 284–290.CrossRefGoogle Scholar
  17. Cullen JJ (1990) On models of growth and photosynthesis in phytoplankton. Deep-Sea Res. 37: 667–683.CrossRefGoogle Scholar
  18. D'Elia CF, Sanders JG & Boynton WR (1986) Nutrient enrichment studies in a coastal plain estuary: phytoplankton growth in large scale, continuous cultures. Can. J. Fish aquat. Sci. 43: 397–406.CrossRefGoogle Scholar
  19. Degrange V & Bardin R (1995) Detection and counting of Nitrobacter populations in soil by PCR. Appl. Environ. Microbiol. 61(6): 2093–2098.PubMedGoogle Scholar
  20. DeLong EF (1992) Archaea in coastal marine environments. Proc. Natl. Acad. Sci. 89: 5685–5689.CrossRefPubMedGoogle Scholar
  21. DeLong EF, Wickham GS & Pace NR (1989) Phylogenetic strains: Ribosomal RNA-based probes for the identification of single cells. Science 243: 1360–1363.PubMedGoogle Scholar
  22. DeLong EF, Franks DG & Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol. Oceanogr. 38: 924–934.CrossRefGoogle Scholar
  23. Fogg GE (1969) The physiology of an algal nuisance. Proc. Roy. Soc. Lond. B. 173: 175–189.CrossRefGoogle Scholar
  24. Field KG, Gordon D, Wright T, Rappe' M, Urbach E, Vergin K & Giovannoni SJ (1997) Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria. Appl. Environ. Microbiol. 63: 63–70.PubMedGoogle Scholar
  25. Francis G (1878) Poisonous Australian lake. Nature (London) 18: 11–12.Google Scholar
  26. Fuhrman JA, McCallum K & Davis AA (1992) Novel major archaebacterial group from marine plankton. Nature (London) 356: 148–149.CrossRefGoogle Scholar
  27. Fuhrman JA, McCallum K & Davis AA (1993) Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific oceans. Appl. Environ. Microbiol. 59: 1294–1302.PubMedGoogle Scholar
  28. Geider RJ, MacIntyre HL & Kana TM (1997) Dynamic model of phytoplankton growth and acclimation: responses of the balanced growth rate and the chlorophyll a: carbon ratio to light, nutrient-limitation and temperature. Marine Ecology Progress Series 148: 187–200.Google Scholar
  29. Gieskes W & Kraay G (1986) Floristic and physiological differences between the shallow and deep nanophytoplankton community in the eutrophic zone of the open tropical Atlantic revealed by HPLC analysis of pigments. Marine Biol. 91: 567–576.CrossRefGoogle Scholar
  30. Giovannoni SJ, Britschgi TB, Moyer CL & Field KG (1990) Genetic diversity in Sargasso Sea bacterioplankton. Nature (London) 345: 148–149.CrossRefGoogle Scholar
  31. Glenn S, Crowley M, Haidvogel D & Song Y (1996) Underwater observatory captures coastal upwelling events off New Jersey. Eos 77: 233–36.Google Scholar
  32. Goericke R & Welschmeyer N (1993a) The carotenoid-labeling method: measuring specific rates of carotenoid synthesis in natural phytoplankton communities. Marine Ecol. Progr. Ser. 98: 157–171.Google Scholar
  33. Goericke R & Welschmeyer N (1993b) The chlorophyll-labeling method: measuring specific rates of chlorophyll a synthesis in cultures and in the open ocean. Limnol. Oceanogr. 38: 80–95.Google Scholar
  34. Goldenberg SB, Landsea CW, Mestas-NuZes AM & Gray WM (2001) The recent increase in Atlantic Hurricane Activity: Causes and implications. Science 293: 474–479.CrossRefPubMedGoogle Scholar
  35. Gonzalez JM, Sherr EB & Sherr BF (1993) Differential feeding by marine flagellates on growing versus starving, and on motile versus nonmotile, bacterial prey. Marine Ecol. Progr. Ser. 102: 257–267.Google Scholar
  36. Gordon DA & Giovannoni SJ (1996) Detection of stratified microbial populations related to Chlorobium and Fibrobacter species in the Atlantic and Pacific Oceans. Appl. Environ. Microbiol. 2: 1171–1177.Google Scholar
  37. Gray WM, Sheaffer JD & Landsea CW (1996) Climate trends associated with multi-decadal variability of intense Atlantic hurricane activity. In: Diaz HF & Pulwarty PS (Eds) Hurricanes, Climatic Change and Socioeconomic Impacts: A Current Perspective (pp 293–312). Westview Press, Denver, Co.Google Scholar
  38. Gray WM et al. (1999) On the mark prediction caps 1999 season for Colorado State University Hurricane Forecast Team: Five year active trend bears out theory. http: // recasts/1999/press99nov.html.Google Scholar
  39. Gruntzig V, Nold SC, Zhou JZ & Tiedje JM (2001) Pseudomonas stutzeri nitrite reductase gene abundance in environmental samples measured by real-time PCR. Appl. Environ. Microbiol. 67(2): 760–768.CrossRefPubMedGoogle Scholar
  40. Guo L & Santschi PH (1997) Isotopic and elemental characterization of colloidal organic matter from the Chesapeake Bay and Galveston Bay. Marine Chem. 59: 1–15.CrossRefGoogle Scholar
  41. Harrington MB (1999) Responses of natural phytoplankton communities from the Neuse River Estuary, NC to changes in nitrogen supply and incident irradiance. MSc thesis, Univ. of North Carolina, Chapel Hill, North Carolina, 89 p.Google Scholar
  42. Harrison P & Turpin D (1982) The manipulation of physical, chemical, and biological factors to select species from natural phytoplankton populations. In: Grice G & Reeve M (Eds) Marine Mesocosms: Biological and Chemical Research in Experimental Ecosystems (pp 275–287). Springer-Verlag, New York.Google Scholar
  43. Harrison W, Platt T & Lewis M (1987) F-ratio and its relationship to ambient nitrate concentration in coastal waters. J. Plankton Res. 9: 235–245.Google Scholar
  44. Hastings RC, Saunders JR, Hall GH, Pickup RW & McCarthy AJ (1998) Application of molecular biological techniques to a seasonal study of ammonia oxidation in a eutrophic freshwater lake. Appl. Environ. Microbiol. 64: 3674–3682.PubMedGoogle Scholar
  45. Head IM, Saunders JR & Pickup RW (1998) Microbial evolution, diversity, and ecology: a decade of ribosomal RNA analysis of uncultivated microorganisms. Microbial Ecol. 35: 1–21.CrossRefGoogle Scholar
  46. Hicks DC & Miller JR (1980) Meteorological forcing and bottom water movement off the northern New Jersey coast. Estuarine Coastal Sci. 2: 563–571.Google Scholar
  47. Horstmann U (1975) Eutrophication and mass production of bluegreen algae in the Baltic. Havforsk Skr 239: 83–90.Google Scholar
  48. Huber AL (1986) Nitrogen fixation by Nodularia spumigena Martens (Cyanobacteria). I. Field studies on the contribution of blooms to the nitrogen budget of the Peel-Harvey Estuary, Western Australia. Hydrobiologia 131: 193–203.CrossRefGoogle Scholar
  49. Hung C-C, Tang D, Warnken K & Santschi PH (2001) Distributions of carbohydrates, including uronic acids, in estuarine waters of Galveston Bay. Marine Chem. 73: 301–318.CrossRefGoogle Scholar
  50. Jeffrey S, Mantoura R & Wright S (Eds) (1997) Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods. UNESCO, Paris.Google Scholar
  51. Karkhoff-Schweizer RR, Huber DPW & Voordouw G (1995) Conservation of the genes for dissimilatory sulfite reductase from Desulfovibrio vulgaris and Archaeoglobus fulgidus allows their detection by PCR. Appl. Environ. Microbiol. 61: 290–296.PubMedGoogle Scholar
  52. Kerkhof L (1992) A Comparison of substrates for quantifying the signal from a non-radiolabeled DNA probe. Anal. Biochem. 205: 359–364.CrossRefPubMedGoogle Scholar
  53. Kerkhof L & Ward BB (1993) Comparison of nucleic acid hybridization and fluorometry for measurement of the relationship between RNA/DNA ratio and growth rate in a marine bacterium. Appl. Environ. Microbiol. 59: 1303–1309.PubMedGoogle Scholar
  54. Kerkhof L & Kemp P (1999) Small ribosomal RNA content in marine bacteria during non-steady state growth. FEMS Microbial Ecol. 30: 253–260.CrossRefGoogle Scholar
  55. Kerkhof L, Santor, M & Garland J (2000) Response of Soybean Rhizosphere Communities to human hygiene water addition as determined by community-level physiological profiling (CLPP) and terminal restriction fragment length polymorphism (TRFLP). FEMS Microbiol. Lett. 184: 95–101.CrossRefPubMedGoogle Scholar
  56. Kirshtein JD, Paerl HW & Zehr JP (1991) Amplification, cloning, and sequencing of a nifH segment from aquatic microorganisms and natural communities. Appl. Environ. Microbiol. 57: 2645–2650.PubMedGoogle Scholar
  57. Laroche J, Nuzzi R, Waters R, Wyman K, Falkowski PG & Wallace DWR (1997) Brown tide blooms in Long Island's coastal waters linked to interannual variability in groundwater flow. Global Change Biol. 3: 397–410.CrossRefGoogle Scholar
  58. Landsea CW, Pielke RA Jr., Mestaz-Nunez AM & Knaff JA (1999) Atlantic basin hurricanes: Indices of climatic changes. Climatic Changes 42: 89–129.CrossRefGoogle Scholar
  59. Liu WT et al. (1997). Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16s rRNA. Appl. Environ. Microbiol. 63: 4516–4522.PubMedGoogle Scholar
  60. MacGregor BJ, Van Mooy B, Baker BJ, Mellon M, Moisander PH, Paerl HW, Zehr JP, Hollander D & Stahl DA (2001) Microbiological, molecular biological, and stable isotopic evidence for nitrogen fixation in the open waters of Lake Michigan. Environ. Microbiol. 3: 205–219.CrossRefPubMedGoogle Scholar
  61. Mackey M, Mackey D, Higgins H & Wright S (1996) CHEMTAX - a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Marine Ecol. Progr. Ser. 144: 265–283.Google Scholar
  62. Massana R, Taylor LT, Murray AE, Wu KY, Jeffrey WH & DeLong EF (1998) Vertical distribution and temporal variation of marine planktonic Archaea in the Gerlache Strait, Antarctica, during early spring. Limnol. Oceanogr. 43: 607–617.Google Scholar
  63. McBride R & Moslow T (1991) Origin, evolution, and distribution of shoreface sand ridges, Atlantic inner shelf. USA. Marine Geol. 97: 57–85.CrossRefGoogle Scholar
  64. McCarthy J (1981) The kinetics of nutrient utilization. In: Platt T (Ed.) Physiological Bases of Phytoplankton Ecology. Can. Bull. Fish. aquat. Sci. 210: 211–233.Google Scholar
  65. McDonald IR & Murrell JC (1997) The particulate methane monoxigenase gene pmoA and its use as a functional gene probe for methanotrophs. FEMS Microbiol. Lett. 156: 205–210.CrossRefPubMedGoogle Scholar
  66. Millie DF, Paerl HW & Hurley J (1993) Microalgal pigment assessments using high performance liquid chromatography: A synopsis of organismal and ecological applications. Can. J. Fish. aquat. Sci. 50: 2513–2527.CrossRefGoogle Scholar
  67. Moisander PH, Kononen K & Paerl HW (2000) Growth, primary productivity, and nitrogen fixation potential of Nodularia spp. (Cyanophyceae) in water from a subtropical estuary in the United States. J. Phycol. 36: 645–658.CrossRefGoogle Scholar
  68. Molloy C & Syrett P (1988) Interrelationships between uptake of urea and uptake of ammonium by microalgae. J. Exp. Marine Biol. 118: 85–95.CrossRefGoogle Scholar
  69. Monger BC & Landry MR (1990) Direct-interception feeding by marine zooflagellates: The importance of surface and hydrodynamic forces. Marine Ecol. Progr. Ser. 65: 123–140.Google Scholar
  70. Morse J, Presley B, Taylor R, Benoit G & Santschi P (1993) Trace metal chemistry of Galveston Bay: Water, sediments, and biota. Marine Environ. Res. 36: 1–37.CrossRefGoogle Scholar
  71. Munson MA, Nedwell DB & Embley TM (1997) Phylogenetic diversity of Archaea in sediment samples from a coastal salt marsh. Appl. Environ. Microbiol. 63: 4729–4733.PubMedGoogle Scholar
  72. Murray AE, Hollibaugh JT & Orrego C (1996) Phylogenetic compositions of bacterioplankton from two California estuaries compared by denaturing gradient gel electrophoresis of 16S rDNA fragments. Appl. Environ. Microbiol. 62: 2676–2680.PubMedGoogle Scholar
  73. Niemi A (1979) Blue-green algal blooms and N: P ratio in the Baltic Sea. Acta Botanica Fennica 110: 57–61.Google Scholar
  74. Nixon SW (1986) Nutrient dynamics and the productivity of marine coastal waters. In: Halwagy R, Clayton D & Behbehani M (Eds) (pp 97–115). The Alden Press, Oxford.Google Scholar
  75. Nixon SW (1995) Coastal marine eutrophication: A definition, social causes, and future concerns. Ophelia 41: 199–220.Google Scholar
  76. Olson JB, Litaker RW & Paerl HW (1999) Ubiquity of heterotrophic diazotrophs in marine microbial mats. Aquatic Microbial Ecol. 19: 29–36.Google Scholar
  77. Paerl HW (1982) Interactions with bacteria. In: Carr NG & Whitton BA (Eds) The Biology of Cyanobacteria (pp 441–461). Blackwell Scientific, Oxford.Google Scholar
  78. Paerl HW (1983) Factors regulating nuisance blue-green algal bloom potentials in the lower Neuse River. Report No. 177, UNC Water Resources Research Institute, Raleigh, NC. 139 p.Google Scholar
  79. Paerl HW (1987) Dynamics of blue-green algal (Microcystis aeruginosa) blooms in the lower Neuse River, NC: causative factors and potential controls. Report No. 229. UNC Water Resources Research Institute, Raleigh, NC. 164 p.Google Scholar
  80. Paerl HW (1988a) Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnol. Oceanogr. 33: 823–847.CrossRefGoogle Scholar
  81. Paerl HW (1988b) Growth and reproductive strategies of freshwater blue-green algae (cyanobacteria). In: Sandgren CD (Ed) Growth and Reproductive Strategies of Freshwater Phytoplankton (pp 261–315). Cambridge Univ. Press, Cambridge.Google Scholar
  82. Paerl HW (1990) Physiological ecology and regulation of N2 fixation in natural waters. Adv. Microbial Ecol. 11: 305–344.Google Scholar
  83. Paerl HW (1995) Coastal eutrophication in relation to atmospheric nitrogen deposition: current perspectives. Ophelia 41: 237–259.Google Scholar
  84. Paerl HW (1996) A comparison of cyanobacterial bloom dynamics in freshwater, estuarine and marine environments. Phycologia 35: 25–35.CrossRefGoogle Scholar
  85. Paerl HW (1997) Coastal eutrophication and harmful algal blooms: Importance of atmospheric deposition and groundwater as “new” nitrogen and other nutrient sources. Limnol. Oceanogr. 42: 1154–1165.CrossRefGoogle Scholar
  86. Paerl HW & Bowles ND (1987) Dilution bioassays: Their application to assessments of nutrient limitation in hypereutrophic waters. Hydrobiologia 146: 265–273.CrossRefGoogle Scholar
  87. Paerl HW & Fogel ML (1994) Isotopic characterization of atmospheric nitrogen inputs as sources of enhanced primary production in coastal Atlantic Ocean waters. Marine Biol. 119: 635–645.CrossRefGoogle Scholar
  88. Paerl HW & Pinckney JL (1996) Microbial consortia: Their role in aquatic production and biogeochemical cycling. Microbial Ecol. 31: 225–247.CrossRefGoogle Scholar
  89. Paerl HW, Rudek J & Mallin MA (1990) Stimulation of phytoplankton production in coastal waters by natural rainfall inputs: nutritional and trophic implications. Marine Biol. 107: 247–254.CrossRefGoogle Scholar
  90. Paerl HW, Mallin MA, Donahue CA, Go M & Peierls BL (1995) Nitrogen loading sources and eutrophication of the Neuse River Estuary, NC: Direct and indirect roles of atmospheric deposition. Report. 291, UNC Water Resources Research Institute, Raleigh, NC 119 p.Google Scholar
  91. Paerl HW & Millie DF (1996) Physiological ecology of toxic cyanobacteria. Phycologia 35(6): 160–167.CrossRefGoogle Scholar
  92. Paerl HW & Zehr JP (2000) Nitrogen Fixation. In: Kirchman D (Ed) Microbial Ecology of the Oceans (pp 387–426). Academic Press, New York.Google Scholar
  93. Paerl HW, Bales JD, Ausley LW, Buzzelli CP, Crowder LB, Eby LA, Go M, Peierls BL, Richardson TL & Ramus JS (2000) Hurricanes' hydrological, ecological effects linger in major US estuary. EOS 81(40): 457–462.Google Scholar
  94. Paerl HW, Bales JD, Ausley LW, Buzzelli CP, Crowder LB, Eby LA, Fear JM, Go M, Peierls BL, Richardson TL & Ramus JS (2001) Ecosystem impacts of 3 sequential hurricanes (Dennis, Floyd and Irene) on the US's largest lagoonal estuary, Pamlico Sound, NC. Proc. Natl. Acad. Sci. USA 98: 5655–5660.CrossRefPubMedGoogle Scholar
  95. Paul JH, Kang B & Tabita RF (2000) Diel Patterns of Regulation of rbcL Transcription in a Cyanobacterium and a Prymnesiophyte. Marine Biotechnol. 2: 429–436.Google Scholar
  96. Pearce JB, Berman CR Jr & Rosen MR (1982) Annual NEMP report on the health of the northeast coastal waters. NOAA Technical Memorandum NMFS-F/NEC-35, Northeast Fisheries Center. Woods Hole. MA.Google Scholar
  97. Peierls BL & HW Paerl (1997) The bioavailability of atmospheric organic nitrogen deposition to coastal phytoplankton. Limnol. Oceanogr. 42: 1819–1880.CrossRefGoogle Scholar
  98. Phelps C, Kerkhof L & Young L (1998) Molecular characterization of a sulfate-reducing consortium which mineralizes benzene. FEMS Microbial Ecol. 27: 269–279.CrossRefGoogle Scholar
  99. Pichard SL, Campbell L & Paul JH (1997) Diversity of the ribulose bisphosphate carboxylase/oxygenase form I gene (rbcL) in natural phytoplankton communities. Appl. Environ. Microbiol. 63: 3600–3606.PubMedGoogle Scholar
  100. Pinckney JL, Millie DF, Howe KE, Paerl HW & Hurley J (1996) Flow scintillation counting of 14C-labeled microalgal photosynthetic piments. J. Plankton Res. 18: 1867–1880.Google Scholar
  101. Pinckney JL, Millie DF, Vinyard B & Paerl HW (1997) Environmental controls of phytoplankton bloom dynamics in the Neuse River Estuary (North Carolina, USA). Can. J. Fish. aquat. Sci. 54: 2491–2501.CrossRefGoogle Scholar
  102. Pinckney JL, Paerl HW & Harrington MB (1999) Responses of the phytoplankton community growth rate to nutrient pulses in variable estuarine environments. J. Phycol. 35: 1455–1463.CrossRefGoogle Scholar
  103. Pinckney LJ, Richardson TL, Millie DF & Paerl HW (2001) Application of photopigment biomarkers for quantifying microalgal community composition and in situ growth rates. Organic Geochem. 32: 585–595.CrossRefGoogle Scholar
  104. Porter KG & Orcutt JD (1980) Nutritional adequacy, manageability, and toxicity as factors that determine the food quality of green and blue-green algae as food for Daphnia. In: Kerfoot WC (Ed) Evolution and Ecology of Zooplankton Communities (pp 268–281). Univ. Press of New England, Hannover.Google Scholar
  105. Rappe MS, Suzuki MT, Vergin KL & Giovannoni SJ (1998) Phylogenetic diversity of ultraplankton plastid small-subunit rRNA genes recovered in environmental nucleic acid samples from the Pacific and Atlantic coasts of the United States. Appl. Environ. Microbiol. 64: 294–303.PubMedGoogle Scholar
  106. Redalje D (1993) The labeled chlorophyll a technique for determining photoautotrophic carbon specific growth rates and carbon biomass. In: Kemp P, Sherr B, Sherr E & Cole J (Eds) Handbook of Methods in Aquatic Microbial Ecology (pp 563–572) Lewis Publishing Co., Boca Raton, FL.Google Scholar
  107. Redalje DG & Laws EA (1981) A new method for estimating phytoplankton growth rates and carbon biomass. Marine Biol. 62: 73–79.CrossRefGoogle Scholar
  108. Richardson K (1997) Harmful or exceptional phytoplankton blooms in the marine ecosystem. Adv. Marine Biol. 31: 302–385.Google Scholar
  109. Riegman R (1995) Nutrient-related selection mechanisms in marine phytoplankton communities and the impact of eutrophication on the planktonic food web. IAWQ SIL Conference on Selection Mechanisms Controlling Biomass Distribution. Noordwykerhout, the Netherlands 32: 4.Google Scholar
  110. Riemann B, Lignell R & Laws E (1993) Time-course development of 14C specific activity of chlorophyll a, carbon, and proteins in algal cultures. Limnol. Oceanogr. 38: 96–111.Google Scholar
  111. Rizzo WG, Lackey G & Christian RR (1992) Significance of euphotic, subtidal sediments to oxygen and nutrient cycling in a temperate estuary. Marine Ecol. Progr. Ser. 86: 51–61.Google Scholar
  112. Rowan K (1989) Photosynthetic Pigments of the Algae. Cambridge Univ. Press, N.Y., 334 p.Google Scholar
  113. Rudek J, Paerl HW, Mallin MA & Bates PW (1991). Seasonal and hydrological control of phytoplankton nutrient limitation in the lower Neuse River Estuary, North Carolina. Marine Ecol. Progr. Ser. 75: 133–142.CrossRefGoogle Scholar
  114. Santschi PH (1995) Seasonality of nutrient concentrations in Galveston Bay. Marine Environ. Res. 40: 337–362.CrossRefGoogle Scholar
  115. Scala DJ & Kerkhof LJ (1998) Nitrous oxide reductase (nosZ) genespecific PCR primers for detection of denitrifiers and three nosZ genes from marine sediments. FEMS Microbiol. Lett. 162: 61–68.CrossRefPubMedGoogle Scholar
  116. Scala DJ & Kerkhof LJ (1999) Diversity of nitrous oxide reductase (nosZ) genes in continental shelf sediments. Appl. Environ. Microbiol. 65: 1681–1687.PubMedGoogle Scholar
  117. Sellner KG (1997) Physiology, ecology, and toxic properties of marine cyanobacterial blooms. Limnol. Oceanogr. 42: 1089–1104.CrossRefGoogle Scholar
  118. Sheridan PF, Slack RD, Ray SM, McKinney LW, Klima EF & Calnan TR (1988) Biological components of Galveston Bay. In: Whitledge TE & Ray SM (Eds) Galveston Bay: Issues, Resources, Status and Management (pp 23-51). U.S. Department of Commerce.Google Scholar
  119. Simek K et al. (1995) Ciliate grazing on picoplankton in a eutrophic reservoir during the summer phytoplankton maximum: A study at the species and community level. Limnol. Oceanogr. 40: 1077–1090.CrossRefGoogle Scholar
  120. Sivonen KK, Kononen K, Esala A-L & Niemela SI (1989) Toxicity and isolation of the cyanobacterium Nodularia spumigena from the southern Baltic Sea in 1986. Hydrobiologia 185: 3–8.CrossRefGoogle Scholar
  121. Steppe TF, Olson JB, Paerl HW & Belnap J (1996) Consortial N2fixation: A strategy for meeting nitrogen requirements of marine and terrestrial cyanobacterial mats. FEMS Microbiol. Ecol. 21: 149–156.CrossRefGoogle Scholar
  122. Stolte W, McCollin T, Noodeloos A & Riegman R (1994) Effect of nitrogen source on the size distribution within marine phytoplankton populations. J. Exp. Marine Biol. Ecol. 184: 83–97.CrossRefGoogle Scholar
  123. Suzuki MT, Rappe MS, Haimberger ZW, Winfield H, Adair N, Strobel J & Giovannoni SJ (1997) Bacterial diversity among small-subunit rRNA gene clones and cellular isolates from the same seawater sample. Appl. Environ. Microbiol. 63: 983–989.PubMedGoogle Scholar
  124. Suzuki MT, Taylor LT & DeLong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays. Appl. Environ. Microbiol. 66(11): 4605–4614.CrossRefPubMedGoogle Scholar
  125. Syrett P (1981) Nitrogen metabolism in microalgae. Physiological bases of phytoplankton ecology. Can. Bull. Fish. aquat. Sci. 210: 182–210. bTwilley R, Cowan J, Miller-Way T, Montagna P & Mortazavi B (1999) Benthic nutrient fluxes in selected estuaries in the Gulf of Mexico. In: Bianchi TS, Pennock JR & Twilley R (Eds) Biogeochemistry of Gulf of Mexico Estuaries (pp 163-209). John Wiley & Sons.Google Scholar
  126. Twomey L & Thompson P (2001) Nutrient limitation of phytoplankton in a seasonally open bar-built estuary: Wilson Inlet, Western Australia. J. Phycol. 37: 16–29.CrossRefGoogle Scholar
  127. Valigura RA, Alexander RB, Castro MS, Meyers TP, Paerl HW, Stacey PE & Turner RE (Eds) (2000) Nitrogen Loading in Coastal Water Bodies: An Atmospheric Perspective. Coastal and Estuarine Studies No. 57. American Geophysical Union Press, Washington, DC.Google Scholar
  128. Van Heukelem L, Lewitus A, Kana T & Craft N (1994). Improved separations of phytoplankton pigments using temperaturecontrolled high performance liquid chromatography. Marine Ecol. Progr. Ser. 114: 303–313.Google Scholar
  129. Vetriani C, Reysenbach A-L & Doré J (1998) Recovery and phylogenetic analysis of archaeal rRNA sequences from continental shelf sediments. FEMS Microbiol. Lett. 161: 83–88.CrossRefPubMedGoogle Scholar
  130. Vitousek PM, Mooney HA, Lubchenko J & Mellilo JM (1997) Human domination of Earth's ecosystem. Science 277: 494–499.CrossRefGoogle Scholar
  131. Vollenweider RA (1982) Eutrophication of Waters: Monitoring, Assessment and Control. OECD, Paris.Google Scholar
  132. Voytek MA & Ward BB (1995) Detection of ammonium-oxidizing bacteria in the beta subclass of the class Proteobacteria in aquatic samples with the PCR. Appl. Environ. Microbiol. 61: 1444–1450.PubMedGoogle Scholar
  133. Wagner M, Roger AJ, Flax JL, Brusseau GA & Stahl DA (1998) Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J. Bacteriol. 180: 2975–2982.PubMedGoogle Scholar
  134. Warnken KL (1998) Sediment Water Exchange of Trace Metals and Nutrients in Galveston Bay, Texas. Masters Thesis, Texas A&M University.Google Scholar
  135. Wagner M, Roger AJ, Flax JL, Brusseau GA & Stahl DA (1998) Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J. Bacteriol. 80: 2975–2982.Google Scholar
  136. Weisse T (1993) Dynamics of autotrophic picoplankton in marine and freshwater ecosystems. In: Jones JG (Ed) Advances in Microbial Ecology (pp 327–370). Plenum Press, New York.Google Scholar
  137. Whitall DR & Paerl HW (2001) Spatiotemporal variability of wet atmospheric nitrogen deposition to the Neuse River Estuary, NC. J. Environ. Qual. 30: 1508–1515.PubMedCrossRefGoogle Scholar
  138. Wright S, Jeffrey S, Mantoura R, Llewellyn C, Bjørnland T, Repeta D & Welschmeyer N (1991) An improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Marine Ecol. Prog. Ser. 77: 183–196.Google Scholar
  139. Wyman M, Zehr JP & Capone DG (1996) Temporal variability in nitrogenase gene expression in natural populations of the marine cyanobacterium Trichodesmium thiebautii. Appl. Environ. Microbiol. 62: 1073–1075.PubMedGoogle Scholar
  140. Zehr JP & Paerl HW (1998) Nitrogen fixation in the marine environment: Genetic potential and nitrogenase expression. In: Cooksey KE (Ed) Molecular Approaches to the Study of the Ocean (pp 285–302). Chapman and Hall, London.Google Scholar
  141. Zumft WG (1997) Cell biology and molecular basis of denitrification [Review]. Microbiol. Mol. Biol. Rev. 61: 533–616.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Hans W. Paerl
    • 1
    Email author
  • Julianne Dyble
    • 1
  • Luke Twomey
    • 1
  • James L. Pinckney
    • 2
  • Joshua Nelson
    • 3
  • Lee Kerkhof
    • 3
  1. 1.Institute of Marine SciencesUniversity of North Carolina at Chapel HillMorehead CityUSA
  2. 2.Department of OceanographyTexas A & M UniversityCollege StationUSA
  3. 3.Institute of Marine and Coastal SciencesRutgers UniversityNew BrunswickUSA

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