Cyanobacteria and Cyanotoxins: The Influence of Nitrogen versus Phosphorus

The importance of nitrogen (N) versus phosphorus (P) in explaining total cyanobacterial biovolume, the biovolume of specific cyanobacterial taxa, and the incidence of cyanotoxins was determined for 102 north German lakes, using methods to separate the effects of joint variation in N and P concentration from those of differential variation in N versus P. While the positive relationship between total cyanobacteria biovolume and P concentration disappeared at high P concentrations, cyanobacteria biovolume increased continually with N concentration, indicating potential N limitation in highly P enriched lakes. The biovolumes of all cyanobacterial taxa were higher in lakes with above average joint NP concentrations, although the relative biovolumes of some Nostocales were higher in less enriched lakes. Taxa were found to have diverse responses to differential N versus P concentration, and the differences between taxa were not consistent with the hypothesis that potentially N2-fixing Nostocales taxa would be favoured in low N relative to P conditions. In particular Aphanizomenon gracile and the subtropical invasive species Cylindrospermopsis raciborskii often reached their highest biovolumes in lakes with high nitrogen relative to phosphorus concentration. Concentrations of all cyanotoxin groups increased with increasing TP and TN, congruent with the biovolumes of their likely producers. Microcystin concentration was strongly correlated with the biovolume of Planktothrix agardhii but concentrations of anatoxin, cylindrospermopsin and paralytic shellfish poison were not strongly related to any individual taxa. Cyanobacteria should not be treated as a single group when considering the potential effects of changes in nutrient loading on phytoplankton community structure and neither should the N2-fixing Nostocales. This is of particular importance when considering the occurrence of cyanotoxins, as the two most abundant potentially toxin producing Nostocales in our study were found in lakes with high N relative to P enrichment.

[1]  Lars Håkanson,et al.  On the issue of limiting nutrient and predictions of cyanobacteria in aquatic systems. , 2007, The Science of the total environment.

[2]  V. Smith.  Eutrophication of freshwater and coastal marine ecosystems a global problem , 2003, Environmental science and pollution research international.

[3]  Jamie Bartram,et al.  Toxic Cyanobacteria in Water: a Guide to Their Public Health Consequences, Monitoring and Management Chapter 2. Cyanobacteria in the Environment 2.1 Nature and Diversity 2.1.1 Systematics , 2022 .

[4]  Helmut Hillebrand,et al.  Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. , 2007, Ecology letters.

[5]  R. Ptáčník,et al.  Oligopeptide chemotypes of the toxic freshwater cyanobacterium Planktothrix can form sub‐populations with dissimilar ecological traits , 2008 .

[6]  P. Nõges,et al.  Analysis of changes over 44 years in the phytoplankton of Lake Võrtsjärv (Estonia): the effect of nutrients, climate and the investigator on phytoplankton-based water quality indices , 2010, Hydrobiologia.

[7]  Anne Lohrli.  Chapman and Hall , 1985 .

[8]  Hans W Paerl,et al.  Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. , 2011, The Science of the total environment.

[9]  G. Eaglesham,et al.  Analysis of cyanobacterial toxins by hydrophilic interaction liquid chromatography-mass spectrometry. , 2004, Journal of chromatography. A.

[10]  A. Ballantyne,et al.  Effects of N : P loading ratios on phytoplankton community composition, primary production and N fixation in a eutrophic lake , 2009 .

[11]  D. B. Nedwell,et al.  Environmental costs of freshwater eutrophication in England and Wales. , 2003, Environmental science & technology.

[12]  V. Smith.  Predictive models for the biomass of blue-green algae in lakes , 1985 .

[13]  D. Schindler,et al.  Eutrophication and Recovery in Experimental Lakes: Implications for Lake Management , 1974, Science.

[14]  H. Panzel.  Deutsche Einheitsverfahren zur Wasser‐, Abwasser‐ und Schlammuntersuchung. 9. Lieferung. Herausgeg. von der Fachgruppe Wasserchemie in der Gesellschaft Deutscher Chemiker. Verlag Chemie, Weinheim – Deerfield Beach – Basel 1981. 3. neubearb. Aufl., IV, 158 S., Loseblattwerk, DM 49,–. , 1982 .

[15]  Moselio Schaechter,et al.  Encyclopedia of microbiology , 2009 .

[16]  Edward McCauley,et al.  Sigmoid relationships between nutrients and chlorophyll among lakes , 1989 .

[17]  Edward McCauley,et al.  Sigmoid Relationships between Phosphorus, Algal Biomass, and Algal Community Structure , 1992 .

[18]  E. Rott,et al.  Some results from phytoplankton counting intercalibrations , 1981, Schweizerische Zeitschrift für Hydrologie.

[19]  H. Oh,et al.  Microcystin Production by Microcystis aeruginosa in a Phosphorus-Limited Chemostat , 2000, Applied and Environmental Microbiology.

[20]  I. Chorus,et al.  Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes. , 2007, Toxicon : official journal of the International Society on Toxinology.

[21]  David Tilman,et al.  Phytoplankton Community Ecology: The Role of Limiting Nutrients , 1982 .

[22]  I. Chorus,et al.  First report on cylindrospermopsin producing Aphanizomenon flos-aquae (Cyanobacteria) isolated from two German lakes. , 2006, Toxicon : official journal of the International Society on Toxinology.

[23]  J. Shapiro,et al.  Current beliefs regarding dominance by blue-greens: The case for the importance of CO2 and pH , 1990 .

[24]  K. Sivonen.  Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains , 1990, Applied and environmental microbiology.

[25]  R. Howarth,et al.  � 2006, by the American Society of Limnology and Oceanography, Inc. Eutrophication of freshwater and marine ecosystems , 2022 .

[26]  W. Wurtsbaugh.  Iron, Molybdenum and Phosphorus Limitation of N2 Fixation Maintains Nitrogen Deficiency of Plankton in the Great Salt Lake Drainage (Utah, USA) , 1988 .

[27]  H. Utermöhl.  Zur Vervollkommnung der quantitativen Phytoplankton-Methodik , 1958 .

[28]  W. Lewis,et al.  Control of Lacustrine Phytoplankton by Nutrients: Erosion of the Phosphorus Paradigm , 2008 .

[29]  V. Smith,et al.  Low Nitrogen to Phosphorus Ratios Favor Dominance by Blue-Green Algae in Lake Phytoplankton , 1983, Science.

[30]  M. Westoby,et al.  Bivariate line‐fitting methods for allometry , 2006, Biological reviews of the Cambridge Philosophical Society.

[31]  G. Cronberg.  Changes in the phytoplankton of Lake Trummen induced by restoration , 2004, Hydrobiologia.

[32]  David W. Schindler,et al.  Eutrophication of lakes cannot be controlled by reducing nitrogen input: Results of a 37-year whole-ecosystem experiment , 2008, Proceedings of the National Academy of Sciences.

[33]  J. Downing,et al.  The nitrogen : phosphorus relationship in lakes , 1992 .

[34]  D. Schindler.  Evolution of phosphorus limitation in lakes. , 1977, Science.

[35]  B. Neilan,et al.  Ecological and molecular investigations of cyanotoxin production. , 2001, FEMS microbiology ecology.

[36]  M. Salkinoja-Salonen,et al.  Variation of Microcystin Content of Cyanobacterial Blooms and Isolated Strains in Lake Grand-Lieu (France) , 1998, Microbial Ecology.

[37]  W. Pearsall.  Phytoplankton in the English Lakes: II. The Composition of the Phytoplankton in Relation to Dissolved Substances , 1932 .

[38]  Thomas Rohrlack,et al.  Genetic characterisation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) isolates from Africa and Europe , 2008 .

[39]  A. Ballot,et al.  Paralytic Shellfish Poisoning Toxin-Producing Cyanobacterium Aphanizomenon gracile in Northeast Germany , 2010, Applied and Environmental Microbiology.

[40]  S. Mbedi,et al.  Variability of the microcystin synthetase gene cluster in the genus Planktothrix (Oscillatoriales, Cyanobacteria). , 2005, FEMS microbiology letters.

[41]  J. Downing,et al.  Predicting cyanobacteria dominance in lakes , 2001 .

[42]  B. Cade,et al.  A gentle introduction to quantile regression for ecologists , 2003 .

[43]  A. Ballot,et al.  First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatschenkoi in northeastern Germany. , 2010, Toxicon : official journal of the International Society on Toxinology.

[44]  J. Weckesser,et al.  Microcystins (hepatotoxic heptapeptides) in german fresh water bodies , 1999 .

[45]  J. Graham,et al.  Environmental factors influencing microcystin distribution and concentration in the Midwestern United States. , 2004, Water research.

[46]  Vitor Vasconcelos,et al.  Toxicology and detection methods of the alkaloid neurotoxin produced by cyanobacteria, anatoxin-a. , 2007, Environment international.

[47]  G. Codd,et al.  Cyanobacterial toxins: risk management for health protection. , 2005, Toxicology and applied pharmacology.

[48]  O. Pietiläinen,et al.  Chlorophyll–nutrient relationships of different lake types using a large European dataset , 2008, Aquatic Ecology.

[49]  M. Dokulil,et al.  Cyanobacterial dominance in lakes , 2000, Hydrobiologia.

[50]  Rainer Kurmayer,et al.  Diversity of microcystin genotypes among populations of the filamentous cyanobacteria Planktothrix rubescens and Planktothrix agardhii , 2006, Molecular ecology.

[51]  Charles R. Goldman,et al.  Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America : a review and critique of experimental enrichments , 1990 .

[52]  Marten Scheffer,et al.  On the Dominance of filamentous cyanobacteria in shallow, turbid lakes , 1997 .

[53]  W. Dodds,et al.  Eutrophication of U.S. freshwaters: analysis of potential economic damages. , 2009, Environmental science & technology.

[54]  Edward McCauley,et al.  Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status , 1997 .

[55]  I. Chorus,et al.  Anatoxin‐a and neurotoxic cyanobacteria in German lakes and reservoirs , 1999 .

[56]  John T. Lehman,et al.  The effect of changes in the nutrient income on the condition of Lake Washington1 , 1981 .

[57]  J. Weckesser,et al.  Regulation of cyanobacteria and microcystin dynamics in polymictic shallow lakes , 2002 .

[58]  D. Findlay,et al.  Relationship between N2-fixation and heterocyst abundance and its relevance to the nitrogen budget of Lake 227 , 1994 .

[59]  C. Berger.  Consistent blooming of Oscillatoria agardhii Gom. in shallow hypertrophic lakes: With 1 figure and 5 tables in the text , 1984 .

[60]  H. Paerl,et al.  OXYGEN‐INDUCED CHANGES IN MORPHOLOGY OF AGGREGATES OF APHANIZOMENON FLOS‐AQUAE (CYANOPHYCEAE): IMPLICATIONS FOR NITROGEN FIXATION POTENTIALS 1 , 1989 .

[61]  H. Matthijs,et al.  Comparison of the light‐limited growth of the nitrogen‐fixing cyanobacteria Anabaena and Aphanizomenon , 1998 .

[62]  L. R. Mur,et al.  Effects of light on nitrate-limited Oscillatoria agardhii in chemostat cultures , 1980, Archives of Microbiology.

[63]  C. Wiedner,et al.  Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekei in eutrophic shallow lakes , 2004, Hydrobiologia.

[64]  E. Rydin,et al.  Nutrient limitation of cyanobacterial blooms: an enclosure experiment from the coastal zone of the NW Baltic proper , 2002 .

[65]  R. Sterner.  On the Phosphorus Limitation Paradigm for Lakes , 2008 .

[66]  A. C. Ziegler,et al.  Cyanotoxin mixtures and taste-and-odor compounds in cyanobacterial blooms from the Midwestern United States. , 2010, Environmental science & technology.

[67]  J. Fastner,et al.  Optimised extraction of microcystins from field samples — a comparison of different solvents and procedures , 1998 .

[68]  L. Carvalho,et al.  Quantitative responses of lake phytoplankton to eutrophication in Northern Europe , 2008, Aquatic Ecology.

[69]  G. Harris.  Phytoplankton Ecology: Structure, Function and Fluctuation , 1986 .

[70]  L. Lawton,et al.  Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. , 1994, The Analyst.

[71]  J. Lund,et al.  Some relationships between algal standing crop, water chemistry, and sediment chemistry in the English Lakes1 , 1974 .

[72]  L. R. Mur,et al.  Effects of Light on the Microcystin Content of Microcystis Strain PCC 7806 , 2003, Applied and Environmental Microbiology.