Nitrogen forms influence microcystin concentration and composition via changes in cyanobacterial community structure

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Monchamp, Marie Eve ^a,d   Pick, Frances R ^b   Beisner, Beatrix E ^c   Maranger, Roxane ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^d SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; DISSOLVED ORGANIC MATTER; MICROCYSTIN; MICROCYSTIN LA; MICROCYSTIN RR; MICROCYSTIN YR; NITROGEN; UNCLASSIFIED DRUG;

APHANIZOMENON; APHANIZOMENON FLOS AQUAE; ARTICLE; BIOMASS; CHEMICAL COMPOSITION; COMMUNITY STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYANOBACTERIUM; ENVIRONMENTAL FACTOR; EUTROPHICATION; LAKE; MICROCYSTIS; MICROCYSTIS AERUGINOSA; NONHUMAN; PREDICTION; REDUNDANCY ANALYSIS; TOXICITY; WATER TEMPERATURE;

BIOMASS; CYANOBACTERIA; EUTROPHICATION; FRESH WATER; LAKES; MICROCYSTINS; NITROGEN; PHYTOPLANKTON; QUEBEC; SEASONS;

EID: 84897484673     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085573     Document Type: Article

References (70)

1. Smith VH, Joye SB, Howarth RW (2006) Eutrophication of freshwater and marine ecosystems. Limnol Oceanogr 51: 351-355. (Pubitemid 43259725)
2. Dodds WK, Bouska WW, Eitzmann JL, Pilger TJ, Pitts KL, et al. (2009) Eutrophication of US freshwaters: Analysis of potential economic damages. Environ Sci Technol 43: 12-19.
3. O'Neil JM, Davis TW, Burford MA, Gobler CJ (2012) The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change. Harmful Algae 14: 313-334.
4. Watson S, McCauley E, Downing J (1997) Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status. Limnol Oceanogr 42: 487-495. (Pubitemid 27422592)
5. Paerl HW, Huisman J (2009) Climate change: A catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1: 27-37.
6. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21: 541-554. (Pubitemid 38339670)
7. Howarth RW, Marino R, Lane J, Cole JJ (1988) Nitrogen-fixation in freshwater, estuarine, and marine ecosystems. 1.Rates and importance. Limnol Oceanogr 33: 669-687.
8. Carmichael WW (1994) Toxins of cyanobacteria. Sci Am 270: 78-86.
9. Falconer IR (1999) An overview of problems caused by toxic blue-green algae (cyanobacteria) in drinking and recreational water. Environ Toxicol 14: 5-12.
10. Smith VH (1983) Low nitrogen to phosphorus ratios favor dominance by blue-green-algae in lake phytoplankton. Science 221: 669-671.
11. Downing JA, McCauley E (1992) The nitrogen - phosphorus relationship in lakes. Limnol Oceanogr 37: 936-945.
12. Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195: 260-262.
13. Pick FR, Lean DRS (1987) The role of macronutrients (C, N, P) in controlling cyanobacterial dominance in temperate lakes. N Z J Mar Freshwat Res 21: 425-434.
14. Downing JA, Watson SB, McCauley E (2001) Predicting cyanobacteria dominance in lakes. Can J Fish Aquat Sci 58: 1905-1908. (Pubitemid 33023417)
15. Paerl HW, Scott JT (2010) Throwing fuel on the fire: Synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environ Sci Technol 44: 7756-7758.
16. Lewis WM Jr, Wurtsbaugh WA, Paerl HW (2011) Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environ Sci Technol 45: 10300-10305.
17. Chorus I, Bartram J (1999) Toxic cyanobacteria in water: A guide to their public health consequences, monitoring and management. London: Spon. 416 p.
18. Sivonen K, Jones GJ (1999) Cyanobacteria toxins. In: Chorus I, Bartram J, editors. Toxic Cyanobacteria in Water: A Guide to Public Health, Significance, Monitoring and Management. London: Spon. pp. 44-111.
19. Welker M, von Döhren H (2006) Cyanobacterial peptides - Nature's own combinatorial biosynthesis. FEMS Microbiol Rev 30: 530-563. (Pubitemid 43855766)
20. Cerasino L, Salmaso N (2012) Diversity and distribution of cyanobacterial toxins in the Italian subalpine lacustrine district. Oceanol Hydrobiol Stud 41: 54-63.
21. Cronberg G, Annadotter H (2006) Manual on aquatic cyanobacteria: A photo guide and a synopsis of their toxicology. Copenhagen: International Society for the Study of Harmful Algae and the United Nations Educational, Scientific, and Cultural Organization. 106 p.
22. Rolland A, Bird DF, Giani A (2005) Seasonal changes in composition of the cyanobacterial community and the occurrence of hepatotoxic blooms in the eastern townships, Quebec, Canada. J Plankton Res 27: 683-694. (Pubitemid 41261348)
23. van de Waal DB, Verspagen JMH, Lurling M, van Donk E, Visser PM, et al. (2009) The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis. Ecol Lett 12: 1326-1335.
24. Dolman AM, Rücker J, Pick FR, Fastner J, Rohrlack T, et al. (2012) Cyanobacteria and cyanotoxins: The influence of nitrogen versus phosphorus. PLoS ONE 7: e38757.
25. Giani A, Bird D, Prairie Y, Lawrence J (2005) Empirical study of cyanobacterial toxicity along a trophic gradient of lakes. Can J Fish Aquat Sci 2109: 2100-2109. (Pubitemid 41810287)
26. Graham JL, Jones JR, Jones SB, Downing JA, Clevenger TE (2004) Environmental factors influencing microcystin distribution and concentration in the Midwestern United States. Water Res 38: 4395-4404. (Pubitemid 39534940)
27. Blomqvist P, Pettersson 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.
28. Berman T, Chava S (1999) Algal growth on organic compounds as nitrogen sources. J Plankton Res 21: 1423-1437. (Pubitemid 29390671)
29. Ferber LR, Levine SN, Lini A, Livingston GP (2004) Do cyanobacteria dominate in eutrophic lakes because they fix atmospheric nitrogen? Freshwat Biol 49: 690-708. (Pubitemid 38693274)
30. McCarthy MJ, James RT, Chen Y, East TL, Gardner WS (2009) Nutrient ratios and phytoplankton community structure in the large, shallow, eutrophic, subtropical Lakes Okeechobee (Florida, USA) and Taihu (China). Limnology 10: 215-227.
31. Orr P, Jones G (1998) Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnol Oceanogr 43: 1604-1614. (Pubitemid 28552075)
32. Downing TG, Meyer C, Gehringer MM, van de Venter M (2005) Microcystin content of Microcystis aeruginosa is modulated by nitrogen uptake rate relative to specific growth rate or carbon fixation rate. Environ Toxicol 20: 257-262. (Pubitemid 40827443)
33. Donald DB, Bogard MJ, Finlay K, Bunting L, Leavitt PR (2013) Phytoplankton-specific response to enrichment of phosphorus-rich surface waters with ammonium, nitrate, and urea. PLoS ONE 8: e53277-e53277.
34. 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.
35. Tonk L, van de Waal DB, Slot P, Huisman J, Matthijs HCP, et al. (2008) Amino acid availability determines the ratio of microcystin variants in the cyanobacterium Planktothrix agardhii. FEMS Microbiol Ecol 65: 383-390.
36. OECD (1982) Eutrophication of waters. Monitoring, assessment and control. Final report, OECD cooperative programme on monitoring of inland waters (eutrophication control). Paris: Environment Directorate, OECD. 154 p.
37. Wetzel R (1975) Limnology. W. B. Saunders, Philadelphia, Pa., 743 p.
38. Aranda-Rodriguez R, Tillmanns A, Benoit FM, Pick FR, Harvie J, et al. (2005) Pressurized liquid extraction of toxins from cyanobacterial cells. Environ Toxicol 20: 390-396. (Pubitemid 40827460)
39. Lund J, Kipling C, Cren E (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia: 143-170.
40. Gosselain V, Hamilton P (2000) Algamica: revisions to a key-based computerized counting program for free-living, attached, and benthic algae. Hydrobiologia: 139-142. (Pubitemid 32106270)
41. American Public Health Association (2005) Standard methods for the examination of water and wastewater. Washington, DC: American Public Health Association. 1200 p.
42. Wetzel RG, Likens GE (2000) Limnological analysis. New York, NY, USA: Springer. 429 p.
43. Bronk DA, Lomas MW, Glibert PM, Schukert KJ, Sanderson MP (2000) Total dissolved nitrogen analysis: comparisons between the persulfate, UV and high temperature oxidation methods. Mar Chem 69: 163-178. (Pubitemid 30168033)
44. R Development Core Team (2011) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
45. Legendre P, Gallagher E (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271-280. (Pubitemid 32996572)
46. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: Estimation and comparison of fractions. Ecology 87: 2614-2625. (Pubitemid 44885972)
47. Shapiro J (1973) Blue-green algae: Why they become dominant. Science 179: 382-384.
48. Reynolds C, Petersen A (2000) The distribution of planktonic cyanobacteria in Irish lakes in relation to their trophic states. Hydrobiologia: 91-99. (Pubitemid 30466587)
49. Lewis WMJ, Wurtsbaugh WA (2008) Control of lacustrine phytoplankton by nutrients: Erosion of the phosphorus paradigm. Int Rev Hydrobiol 93: 446-465.
50. Scott JT, McCarthy MJ (2010) Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnol Oceanogr 55: 1265-1270.
51. Berman T, Bronk DA (2003) Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems. Aquat Microb Ecol 31: 279-305. (Pubitemid 36524263)
52. Glibert PM, Heil CA, Hollander D, Revilla M, Hoare A, et al. (2004) Evidence for dissolved organic nitrogen and phosphorus uptake during a cyanobacterial bloom in Florida Bay. Mar Ecol Prog Ser 280: 73-83. (Pubitemid 39484109)
53. 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.
54. Bronk D, See J, Bradley P, Killberg L (2007) DON as a source of bioavailable nitrogen for phytoplankton. Biogeosciences 3: 1247-1277.
55. Flores E, Herrero A (2005) Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans 33: 164-167. (Pubitemid 40313790)
56. McCarthy MJ, Lavrentyev PJ, Yang L, Zhang L, Chen Y, et al. (2007) Nitrogen dynamics and microbial food web structure during a summer cyanobacterial bloom in a subtropical, shallow, well-mixed, eutrophic lake (Lake Taihu, China). Hydrobiologia 581: 195-207.
57. Watanabe M, Kaya K, Takamura N (1992) Fate of the toxic cyclic heptapeptides, the microcystins, from blooms of Microcystis (cyanobacteria) in a hypertrophic lake. J Phycol 28: 761-767.
58. Kotak B, Lam A (1995) Variability if the hepatotoxin microcystin-LR in hypereutrophic drinking water lakes. J Phycol 31: 248-263.
59. Fastner J, Neumann U, Wirsing B, Weckesser J, Wiedner C, et al. (1999) Microcystins (hepatotoxic heptapeptides) in German fresh water bodies. Environ Toxicol 14: 13-22.
60. Robarts RD, Zohary T (1987) Temperature effects on photosynthetic capacity, respiration, and growth-rates of bloom-forming cyanobacteria N Z J Mar Freshwat Res 21: 391-399.
61. Rantala A, Fewer DP, Hisbergues M, Rouhiainen L, Vaitomaa J, et al. (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci USA 101: 568-573. (Pubitemid 38084677)
62. Xu Y, Wu Z, Yu B, Peng X, Yu G, et al. (2008) Non-microcystin producing Microcystis wesenbergii (Komárek) Komárek (Cyanobacteria) representing a main waterbloom-forming species in Chinese waters. Environ. Pollut. (Barking, Essex : 1987) 156: 162-167.
63. Via-Ordorika L, Fastner J, Kurmayer R, Hisbergues M, Dittmann E, et al. (2004) Distribution of microcystin-producing and non-microcystin-producing Microcystis sp. in European freshwater bodies: detection of microcystins and microcystin genes in individual colonies. Syst Appl Microbiol 27: 592-602. (Pubitemid 39263658)
64. Otsuka S, Suda S, Li R, Watanabe M, Oyaizu H, et al. (1999) Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiol Lett 172: 15-21. (Pubitemid 29090284)
65. Beversdorf LJ, Miller TR, McMahon KD (2013) The role of nitrogen fixation in cyanobacterial bloom toxicity in a temperate, eutrophic lake. PLoS ONE 8: e56103.
66. Kosten S, Huszar VLM, Bécares E, Costa LS, Donk E, et al. (2012) Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biol 18: 118-126.
67. Lee SJ, Jang MH, Kim HS, Yoon BD, Oh HM (2000) Variation of microcystin content of Microcystis aeruginosa relative to medium N:P ratio and growth stage. J Appl Microbiol 89: 323-329.
68. Davis TW, Berry DL, Boyer GL, Gobler CJ (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8: 715-725.
69. Tillmanns AR, Pick FR (2011) The effect of sampling scales on the interpretation of environmental drivers of the cyanotoxin microcystin. Lake Reserv Manage 27: 183-193.
70. Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, et al. (2009) Controlling eutrophication: Nitrogen and phosphorus. Science 323: 1014-1015.