Organic and inorganic nitrogen utilization by nitrogen-stressed cyanobacteria during bloom conditions

Journal of Applied Phycology

Volumn 26, Issue 1, 2014, Pages 299-309

  Chaffin, Justin D ^a,b   Bridgeman, Thomas B ^a  

^a UNIVERSITY OF TOLEDO   (United States)

^b Department of Evolution Ecology and Organismal Biology   (United States)

Author keywords

Cyanobacteria; Eutrophication; Microcystis; Nitrogen; Planktothrix

Indexed keywords

EID: 84893661026     PISSN: 09218971     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10811-013-0118-0     Document Type: Article

References (50)

1. Beaver JR, Scotese KC, Minerovic AD, Buccier KM, Tausz CE, Clapham WB (2012) Ecoregion, land use, and phytoplankton relationships in productive Ohio reservoirs. Inland Waters 2: 101-108.
2. Blomqvist P, Petterson A, Hyenstrand P (1994) Ammonium-nitrogen: a key regulatory factor causing dominance of non-nitrogen-fixing cyanobacteria in aquatic systems. Arch Hydrobiol 132: 141-164.
3. Chaffin JD, Bridgeman TB, Bade DL (2013) Nitrogen constrains the growth of late-summer cyanobacterial blooms in Lake Erie. Adv Microbiol In press.
4. Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323: 1014-1015.
5. Conroy JD, Quinlan EL, Kane DD, Culver DA (2007) Cylindrospermopsis in Lake Erie: testing its association with other cyanobacterial genera and major limnological parameters. J Great Lakes Res 33: 519-535.
6. Dai G, Shang J, Qiu B (2012) Ammonia may play an important role in the succession of cyanobacterial blooms and the distribution of common algal species in shallow freshwater lakes. Global Change Biol 18: 1571-1581.
7. Dai R, Liu H, Qu J, Zhao X, Hou Y (2009) Effects of amino acids on microcystin production of the Microcystis aeruginosa. J Hazard Mater 161: 730-736.
8. Davenport T, Drake W (2011) EPA commentary-Grand Lake St. Marys. Ohio-The case for source water protection: Nutrients and algae blooms. Lakeline Fall 2011: 41-46.
9. Davis TW, Harke MJ, Marcoval MA, Goleski J, Orano-Dawson C, Berry DL, Gobler CJ (2010) Effects of nitrogenous compounds and phosphorus on the growth of toxic and nontoxic strains of Microcystis during cyanobacterial blooms. Aquat Microb Ecol 61: 149-162.
10. Donald DB, Bogard MJ, Finlay K, Leavitt PR (2011) Comparative effects of urea, ammonium, and nitrate on phytoplankton abundance, community composition, and toxicity in hypereutrophic freshwaters. Limnol Oceanogr 56: 2161-2175.
11. Dortch Q (1990) The interaction between ammonium and nitrate uptake in phytoplankton. Mar Ecol Prog Ser 61: 183-201.
12. Downs TM, Schallenberg M, Burns CW (2008) Responses of lake phytoplankton to micronutrient enrichment: a study in two New Zealand lakes and an analysis of published data. Aquat Sci 70: 347-360.
13. Dugdale RC, Goering JJ (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol Oceanogr 12: 196-206.
14. Filbrun JE, Conroy JD, Culver DA (2013) Understanding seasonal phosphorus dynamics to guide effective management of shallow, hypereutrophic Grand Lake St. Marys, Ohio. Lake Reserv Manage 29: 1-14.
15. Finlay K, Patoine A, Donald DB, Bogard MJ, Leavitt PR (2010) Experimental evidence that pollution with urea can degrade water quality in phosphorus-rich lakes of the Northern Great Plains. Limnol Oceanogr 55: 1213-1230.
16. Flores E, Herrero A (2005) Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans 33: 164-167.
17. Frias JE, Flores E, Herrero A (1997) Nitrate assimilation gene cluster from the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 179: 477-486.
18. Frias JE, Mérida A, Herrero A, Martin-Nieto J, Flores E (1993) General distribution of the nitrogen control gene ntcA in cyanobacteria. J Bacteriol 175: 5710-5713.
19. Goeyens L, Kindermans N, Yusuf MA, Elskens M (1998) A room temperature procedure for the manual determination of urea in seawater. Estuar Coast Shelf S 47: 415-418.
20. Guillard RRL, Lorenzen CJ (1972) Yellow-green algae with chlorophyllide c. J Phycol 8: 10-14.
21. Havens SM, Hassler CS, North RL, Guildford SJ, Silsbe G, Wilhelm SW, Twiss MR (2012) Iron plays a role in nitrate drawdown by phytoplankton in Lake Erie surface waters as observed in lake-wide assessments. Can J Fish Aquat Sci 69: 369-381.
22. Herrero A, Muro-Pastor AM, Flores E (2001) Nitrogen control in cyanobacteria. J Bacteriol 183: 411-425.
23. Hoorman J, Hone T, Sudman T, Dirksen T, Iles J, Islam R (2008) Agricultural impacts on lake and stream water quality in Grand Lake St. Marys, western Ohio. Water Air Soil Poll 193: 309-322.
24. Ivanikova NV, McKay RML, Bullerjahn GS, Sterner RW (2007) Nitrate utilization by phytoplankton in Lake Superior is impaired by low nutrient (P, Fe) availability and season light limitation- A cyanobacterial bioreporter study. J Phycol 43: 475-484.
25. Jeppesen E, Sondergaard M, Jensen JP, Havens KE, Anneville O, Carvalho L, Coveney MF, Deneke R, Dokulil MT, Foy B, Gerdeaux D, Hampton SE, Hilt S, Kangur K, Kohler J, Lammens EHHR, Lauridsen TL, Manca M, Miracle MR, Moss B, Noges P, Persson G, Phillips G, Portielje R, Schelske CL, Straile D, Tatrai I, Willen E, Winder M (2005) Lake responses to reduced nutrient loading-an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50: 1747-1771.
26. Ji Y, Sherrell RM (2008) Differential effects of phosphorus limitation on cellular metals in Chlorella and Microcystis. Limnol Oceanogr 53: 1790-1804.
27. Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press.
28. Kudela RM, Lane JQ, Cochlan WP (2008) The potential role of anthropogenically derived nitrogen in the growth of harmful algae in California, USA. Harmful Algae 8: 103-110.
29. 13C: revisiting the usual computation formulae. J Plankton Res 19: 263-271.
30. Lewis WM, Wurtsbaugh WA (2008) Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. Int Rev Hydrobiol 93: 446-465.
31. Lindell D, Post AF (2001) Ecological aspects of ntcA gene expression and its use as an indicator of the nitrogen status of marine Synechococcus spp. Appl Environ Microbiol 67: 3340-3349.
32. Millie DF, Fahnenstiel GL, Dyble Bressie J, Pigg RJ, Rediske RR, Klarer DM, Tester PA, Litaker RW (2009) Late-summer phytoplankton in western Lake Erie (Laurentian Great Lakes): bloom distributions, toxicity, and environmental influences. Aquat Ecol 43: 915-934.
33. Moisander PH, Ochiai M, Lincoff A (2009) Nutrient limitation of Microcystis aeruginosa in northern California Klamath River reservoirs. Harmfull Algae 8: 889-897.
34. Mulvenna PF, Savidge G (1992) A modified manual method for the determination of urea in seawater using diacetylmonoxime reagent. Estuar Coast Shelf S 34: 429-438.
35. North RL, Guildford SJ, Smith REH, Havens SM, Twiss MR (2007) Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnol Oceanogr 52: 315-328.
36. Paerl HW, Xu H, McCarthy MJ, Zhu G, Qin B, Li Y, Gardner WS (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res 45: 1973-1983.
37. Quintero MJ, Muro-Pastor AM, Herrero A, Flores E (2000) Arginine catabolism in the cyanobacterium Synechocystis sp. strain PCC 6803 involves the urea cycle and arginase pathway. J Bacteriol 182: 1008-1015.
38. Richards RP, Baker DB, Crumrine JP, Stearns AM (2010) Unusually large loads in 2007 from the Maumee and Sandusky Rivers, tributaries to Lake Erie. J Soil Water Conserve 65: 450-462.
39. Rücker J, Wiedner C, Zippel P (1997) Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekei in eutrophic shallow lakes. Hydrobiologia 342-343: 107-115.
40. Scheffer M. (1998) Ecology of shallow lakes. Chapman and Hall.
41. Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195: 260-262.
42. Schindler DW, Hecky RE, Findlay DL, Stainton MP, Parker BR, Paterson MJ, Beaty KG, Lyng M, Kasian SEM (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proc Nat Acad of Sci 105: 11254-11258.
43. Smith VH (2003) Eutrophication of freshwater and coastal marine ecosystems: a global problem. Environ Sci Pollut R 10: 126-139.
44. Speziale BJ, Schreiner SP, Giammatteo PA, Schindler JE (1984) Comparison of N, N-dimethylformamide, dimethyl sulfoxide, and acetone for extraction of phytoplankton chlorophyll. Can J Fish Aquat Sci 41: 1519-1522.
45. Teubner K, Feyerabend R, Henning M, Nicklisch A, Woitke P, Kohl JG (1999) Alternative blooming of Aphanizomenon flos-aquae or Planktothrix agardhii induced by the timing of the critical nitrogen: phosphorus ratio in hypertrophic riverine lakes. Ergeb Limnol 54: 325-344.
46. Tonk L, van De Waal DB, Slot P, Huisman J, Matthijs HC, Visser PM (2008) Amino acid availability determines the ratio of microcystin variants in the cyanobacterium Planktothrix agardhii. FEMS Microbiol Ecol 65: 383-390.
47. Vega-Palas A, Flores E, Herrero A (1992) NtcA, a global nitrogen regulator from the cyanobacterium Synechococcus that belongs to the Crp family of bacterial regulators. Mol Microbiol 6: 1853-1859.
48. Walsby AE, Jüttner F (2006) The uptake of amino acids by the cyanobacterium Planktothrix rubescens is stimulated by light at low irradiances. FEMS Microbiol Ecol 58: 14-22.
49. Wetzel RG (2001) Limnology: lake and river ecosystems. Academic, NY.
50. Xu H, Paerl HW, Qin B, Zhu G, Gaoa G (2010) Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnol Oceanogr 55: 420-432.