Stoichiometric regulation of phytoplankton toxins

Ecology Letters

Volumn 17, Issue 6, 2014, Pages 736-742

  Van de Waal, Dedmer B ^a   Smith, Val H ^b   Declerck, Steven A J ^a   Stam, Eva C M ^a   Elser, James J ^c  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b UNIVERSITY OF KANSAS   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Ecological stoichiometry; Harmful algal blooms; Harmful cyanobacteria; Natural toxins; Nutrient limitation; Secondary metabolites

Indexed keywords

ALGAE; BACTERIA (MICROORGANISMS); CYANOBACTERIA; FUNGI;

CARBON; NITROGEN; PHOSPHORUS; TOXIN;

CHEMISTRY; ECOLOGICAL STOICHIOMETRY; HARMFUL ALGAL BLOOMS; HARMFUL CYANOBACTERIA; LETTER; METABOLISM; NATURAL TOXINS; NUTRIENT LIMITATION; PHYSIOLOGY; PHYTOPLANKTON; SECONDARY METABOLITES;

ECOLOGICAL STOICHIOMETRY; HARMFUL ALGAL BLOOMS; HARMFUL CYANOBACTERIA; NATURAL TOXINS; NUTRIENT LIMITATION; SECONDARY METABOLITES;

CARBON; NITROGEN; PHOSPHORUS; PHYTOPLANKTON; TOXINS, BIOLOGICAL;

EID: 84899954192     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12280     Document Type: Article

References (50)

1. Allen, M.M. (1984). Cyanobacterial cell inclusions. Annu. Rev. Microbiol., 38, 1-25.
2. Anderson, D.M., Glibert, P.M. & Burkholder, J.M. (2002). Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries, 25, 704-726.
3. Auro, M.E. & Cochlan, W.P. (2013). Nitrogen utilization and toxin production by two diatoms of the Pseudo-nitzschia pseudodelicatissima Complex: P. cuspidata and P. fryxelliana. J. Phycol., 49, 156-169.
4. Baker, J.W., Grover, J.P., Brooks, B.W., Urena-Boeck, F., Roelke, D.L., Errera, R. et al. (2007). Growth and toxicity of Prymnesium parvum (Haptophyta) as a function of salinity, light, and temperature. J. Phycol., 43, 219-227.
5. Bates, S.S. (1998). Ecophysiology and Metabolism of ASP Toxin Production. In: Physiological ecology of harmful algal blooms. (eds Anderson, D.M., Cembella, A.D., Hallegraeff, G.M.). Springer-Verlag, Berlin Heidelberg, Heidelberg, Germany, pp. 405-426.
6. Borenstein, M., Hedges, L.V., Higgins, J.P.T. & Rothstein, H.R. (2009). Introduction to Meta-Analysis. John Wiley & Sons, Chichester, UK.
7. Carpenter, S.R., Caraco, N.F., Correll, D.L., Howarth, R.W., Sharpley, A.N. & Smith, V.H. (1998). Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol. Appl., 8, 559-568.
8. Cembella, A.D. (1998). Ecophysiology and Metabolism of Paralytic Shellfixh Toxins in Marine Microalgae. In: Physiological Ecology of Harmful Algal Blooms. (eds Anderson, D.M., Cembella, A.D., Hallegraeff, G.M.). Springer-Verlag, Berlin Heidelberg Heidelberg, Germany, pp. 281-403.
9. Cornforth, D.M. & Foster, K.R. (2013). Competition sensing: the social side of bacterial stress responses. Nat. Rev. Microbiol., 11, 285-293.
10. Cusack, C.K., Bates, S.S., Quilliam, M.A., Patching, J.W. & Raine, R. (2002). Confirmation of domoic acid production by Pseudo-nitzschia australis (Bacillariophyceae) isolated from Irish waters. J. Phycol., 38, 1106-1112.
11. Dolman, A.M., Rucker, J., Pick, F.R., Fastner, J., Rohrlack, T., Mischke, U. et al. (2012). Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus. PLoS ONE, 7, e38757.
12. Edvardsen, B. & Imai, I. (2006). The Ecology of Harmful Flagellates within Prymnesiophyceae and Raphidophyceae. In: Ecology of Harmful Algae. (eds Granéli, E., Turner, J.T.). Springer-Verlag, Berlin Heidelberg, Heidelberg, Germany, pp. 67-79.
13. Elser, J.J., Bracken, M.E.S., Cleland, E.E., Gruner, D.S., Harpole, W.S., Hillebrand, H. et al. (2007). Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett., 10, 1135-1142.
14. Elser, J.J., Andersen, T., Baron, J.S., Bergstrom, A.K., Jansson, M., Kyle, M. et al. (2009). Shifts in lake N: P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition. Science, 326, 835-837.
15. Etheridge, S.M. & Roesler, C.S. (2005). Effects of temperature, irradiance, and salinity on photosynthesis, growth rates, total toxicity, and toxin composition for Alexandrium fundyense isolates from the Gulf of Maine and Bay of Fundy. Deep Sea Res. (II Top. Stud. Oceanogr.), 52, 2491-2500.
16. Fu, F.X., Place, A.R., Garcia, N.S. & Hutchins, D.A. (2010). CO2 and phosphate availability control the toxicity of the harmful bloom dinoflagellate Karlodinium veneficum. Aquat. Microb. Ecol., 59, 55-65.
17. Glibert, P.M. & Burkholder, J.M. (2011). Harmful algal blooms and eutrophication: 'Strategies' for nutrient uptake and growth outside the Redfield comfort zone. Chin. J. Oceanol. Limnol., 29, 724-738.
18. Granéli, E. & Flynn, K. (2006). Chemical and Physical Factors Influencing Toxin Content. In: Ecology of Harmful Algae. (eds Granéli, E., Turner, J.T.). Springer-Verlag, Berlin Heidelberg, Heidelberg, Germany, pp. 229-241.
19. Granéli, E. & Turner, J.T. (2006). Ecology of Harmful Algae. Springer-Verlag, Berlin Heidelberg, Heidelberg, Germany.
20. Granéli, E., Johansson, N. & Panosso, R. (1998). Cellular Toxin Contents in Relation to Nutrient Conditions for Different Groups of Phytotoxins. In: Harmful Algae (edsReguera, B., Blanco, J., Fernández, M.L., Wyatt, T.). Xunta de Galicia and IOC-UNESCO, Santiago de Compostella, pp. 321-324.
21. Granéli, E., Edvardsen, B., Roelke, D.L. & Hagstrom, J.A. (2012). The ecophysiology and bloom dynamics of Prymnesium spp. Harmful Algae, 14, 260-270.
22. Hackett, J.D., Wisecaver, J.H., Brosnahan, M.L., Kulis, D.M., Anderson, D.M., Bhattacharya, D. et al. (2013). Evolution of Saxitoxin Synthesis in Cyanobacteria and Dinoflagellates. Mol. Biol. Evol., 30, 70-78.
23. Heisler, J., Glibert, P.M., Burkholder, J.M., Anderson, D.M., Cochlan, W., Dennison, W.C. et al. (2008). Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae, 8, 3-13.
24. Hillebrand, H., Steinert, G., Boersma, M., Malzahn, A., Meunier, C.L., Plum, C. et al. (2013). Golman revisited: faster-growing phytoplankton has lower N: P and lower stoichiometric flexibility. Limnol. Oceanogr., 58, 2076-2088.
25. Iason, G.R., Dicke, M. & Hartley, S.E. (2013). The Ecology of Plant Secondary Metabolites: From Genes to Global Processes. Cambridge University Press, New York.
26. Kardinaal, W.E.A., Janse, I., Kamst-van Agterveld, M., Meima, M., Snoek, J., Mur, L.R. et al. (2007). Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquat. Microb. Ecol., 48, 1-12.
27. Keller, L. & Surette, M.G. (2006). Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol., 4, 249-258.
28. Klausmeier, C.A., Litchman, E., Daufresne, T. & Levin, S.A. (2004). Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature, 429, 171-174.
29. Koricheva, J., Larsson, S., Haukioja, E. & Keinanen, M. (1998). Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos, 83, 212-226.
30. Legrand, C., Johansson, N., Johnsen, G., Borsheim, K.Y. & Graneli, E. (2001). Phagotrophy and toxicity variation in the mixotrophic Prymnesium patelliferum (Haptophyceae). Limnol. Oceanogr., 46, 1208-1214.
31. Moustafa, A., Loram, J.E., Hackett, J.D., Anderson, D.M., Plumley, F.G. & Bhattacharya, D. (2009). Origin of saxitoxin biosynthetic genes in cyanobacteria. PLoS ONE, 4, e5758.
32. Nielsen, L.T., Krock, B. & Hansen, P.J. (2013). Production and excretion of okadaic acid, pectenotoxin-2 and a novel dinophysistoxin from the DSP-causing marine dinoflagellate Dinophysis acuta: effects of light, food availability and growth phase. Harmful Algae, 23, 34-45.
33. Orihel, D.M., Bird, D.F., Brylinsky, M., Chen, H.R., Donald, D.B., Huang, D.Y. et al. (2012). High microcystin concentrations occur only at low nitrogen-to-phosphorus ratios in nutrient-rich Canadian lakes. Can. J. Fish. Aquat. Sci., 69, 1457-1462.
34. Parkhill, J.P. & Cembella, A.D. (1999). Effects of salinity, light and inorganic nitrogen on growth and toxigenicity of the marine dinoflagellate Alexandrium tamarense from northeastern Canada. J. Plankton Res., 21, 939-955.
35. Quigg, A., Finkel, Z.V., Irwin, A.J., Rosenthal, Y., Ho, T.Y., Reinfelder, J.R. et al. (2003). The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature, 425, 291-294.
36. Sanchez, S. & Demain, A.L. (2002). Metabolic regulation of fermentation processes. Enzyme Microb. Technol., 31, 895-906.
37. Scott, J.T., McCarthy, M.J., Otten, T.G., Steffen, M.M., Baker, B.C., Grantz, E.M. et al. (2013). Comment: an alternative interpretation of the relationship between TN:TP and microcystins in Canadian lakes. Can. J. Fish. Aquat. Sci., 70, 1265-1268.
38. Sivonen, K. & Jones, G. (1999). Cyanobacterial Toxins. In: Toxic Cyanobacteria in Water: A Guide to their Public Health Consequences, Monitoring and Management (eds Chorus, I., Bartram, J.). E & FN Spon, WHO London, pp. 41-112.
39. Skovgaard, A., Legrand, C., Hansen, P.J. & Graneli, E. (2003). Effects of nutrient limitation on food uptake in the toxic haptophyte Prymnesium parvum. Aquat. Microb. Ecol., 31, 259-265.
40. Smalley, G.W., Coats, D.W. & Stoecker, D.K. (2003). Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Mar. Ecol. Prog. Ser., 262, 137-151.
41. Smith, V.H. (2003). Eutrophication of freshwater and coastal marine ecosystems: a global problem. Environ. Sci. Pollut. Res., 10, 126-139.
42. Staunton, J. & Weissman, K.J. (2001). Polyketide biosynthesis: a millennium review. Natural Product Reports, 18, 380-416.
43. Sterner, R.W. & Elser, J.J. (2002). Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton.
44. Stoecker, D.K., Tillmann, U. & Granéli, E. (2006). Phagotrophy in Harmful Algae. In Ecology of Harmful Algae. (eds Granéli, E., Turner, J.T.). Springer-Verlag, Berlin Heidelberg, Heidelberg, Germany, pp. 177-187.
45. Sun, J., Hutchins, D.A., Feng, Y.Y., Seubert, E.L., Caron, D.A. & Fu, F.X. (2011). Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo-nitzschia multiseries. Limnol. Oceanogr., 56, 829-840.
46. Tillmann, U. (2003). Kill and eat your predator: a winning strategy of the planktonic flagellate Prymnesium parvum. Aquat. Microb. Ecol., 32, 73-84.
47. Tonk, L., Visser, P.M., Christiansen, G., Dittmann, E., Snelder, E., Wiedner, C. et al. (2005). The microcystin composition of the cyanobacterium Planktothrix agardhii changes toward a more toxic variant with increasing light intensity. Appl. Environ. Microbiol., 71, 5177-5181.
48. Touzet, N., Franco, J.M. & Raine, R. (2007). Characterization of nontoxic and toxin-producing strains of Alexandrium minutum (Dinophyceae) in Irish coastal waters. Appl. Environ. Microbiol., 73, 3333-3342.
49. Van de Waal, D.B., Verspagen, J.M.H., Lurling, M., Van Donk, E., Visser, P.M. & Huisman, J. (2009). The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis. Ecol. Lett., 12, 1326-1335.
50. Wiedner, C., Visser, P.M., Fastner, J., Metcalf, J.S., Codd, G.A. & Mur, L.R. (2003). Effects of light on the microcystin content of Microcystis strain PCC 7806. Appl. Environ. Microbiol., 69, 1475-1481.