Modeling continuous cultures of microalgae colimited by nitrogen and phosphorus

Journal of Theoretical Biology

Volumn 265, Issue 3, 2010, Pages 443-454

  Bougaran, Gaël ^a   Bernard, Olivier ^b   Sciandra, Antoine ^c,d  

^a IFREMER   (France)

^b INRIA   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d CNRS   (France)

Author keywords

Colimitation; Mathematical model; Phytoplankton; Quota

Indexed keywords

NITROGEN; PHOSPHORUS;

BIOCHEMISTRY; GROWTH RATE; MICROALGA; NITROGEN; NUMERICAL MODEL; NUTRIENT UPTAKE; PHOSPHORUS; PHYTOPLANKTON;

ARTICLE; BIOCHEMISTRY; CONTINUOUS CULTURE; CONTROLLED STUDY; DOWN REGULATION; MATHEMATICAL ANALYSIS; MICROALGA; NITROGEN UPTAKE; NONHUMAN; NUTRIENT UPTAKE; PHYTOPLANKTON; PLANT GROWTH; PRIORITY JOURNAL; PROCESS MODEL; BIOLOGICAL MODEL; EUKARYOTE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SPECIES DIFFERENCE;

ALGAE; MODELS, BIOLOGICAL; NITROGEN; PHOSPHORUS; PHYTOPLANKTON; SPECIES SPECIFICITY; EUKARYOTA;

ISOCHRYSIS; SELENASTRUM MINUTUM;

EID: 77954621332     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2010.04.018     Document Type: Article

References (69)

1. Afghan B.K. Nutrients. Chemical Analysis of Inorganic Constituents of Water 1982, 170-178. CRC Press, West Palm Beach, FL. J.C. Van Loon (Ed.).
2. Agren G.I. The c:n:p stoichiometry of autotrophs-theory and observations. Ecology Letters 2004, 7:185-191.
3. Ahlgren G. Growth of Oscillatoria agardhii in chemostat culture: 1. Nitrogen and phosphorus requirements. Oikos 1977, 29(2):209-224.
4. Aksnes D., Egge J. A theoretical model for nutrient uptake in phytoplankton. Marine Ecology Progress Series 1991, 70:65-72.
5. Arrigo K.R. Marine microorganisms and global nutrient cycles. Nature 2005, 437:349-355.
6. Beardall, J., Berman, T., Heraud, P., Kadiri, M.O., Light, B.R., Patterson, G.W., Roberts, S., Sulzberger, B., Sahan, E., Uehlinger, U., Wood, B., 2001. A comparison of methods for detection of phosphate limitation in microalgae. Aquatic Sciences 63, 107-121.
7. Berdalet E., Latasa M., Estrada M. Effects of nitrogen and phosphorus starvation on nucleic acid and protein content of Heterocapsa sp. Journal of Plankton Research 1994, 16:303-316.
8. Bergstrom A.K., Jonsson A., Jansson M. Phytoplankton responses to nitrogen and phosphorus enrichment in unproductive Swedish lakes along a gradient of atmospheric nitrogen deposition. Aquatic Biology 2008, 4(1):55-64.
9. 2 under nitrate limitation. Ecological Modelling 2008, 211:324-338.
10. Bernard O., Gouzé J.L. Transient behavior of biological loop models, with application to the Droop model. Mathematical Biosciences 1995, 127(1):19-43.
11. Bernard O., Gouzé J.-L. Nonlinear qualitative signal processing for biological systems: application to the algal growth in bioreactors. Mathematical Biosciences 1999, 157:357-372.
12. Bernard O., Sallet G., Sciandra A. Nonlinear observers for a class of biological systems. Application to validation of a phytoplanktonic growth model. IEEE Transactions on Automatic Control 1998, 43:1056-1065.
13. Bougaran, G., Bernard, O., Sciandra, A., 2009. Modelling continuous cultures of microalgae colimited with nitrogen and phosphorus. In: Proceedings of the Mathmod 09 Conference, Vienna, Austria.
14. Bougaran G.L., Le Dean L., Lukomska E., Kaas R., Baron R. Transient initial phase in continuous culture of Isochrysis galbana affinis Tahiti. Aquatic Living Resources 2003, 16(4):389-394.
15. Burmaster D. The unsteady continuous culture of phosphate-limited Monochrisis lutheri Droop: experimental and theoretical analysis. Journal of Experimental Marine Biology and Ecology 1979, 39(2):167-186.
16. Crawford N.M., Glass A.D.M. Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science 1998, 3:389-395.
17. Dai R., Liu H., Qu J., Zhao X., Ru J., Hou Y. Relationship of energy charge and toxin content of Microcystis aeruginosa in nitrogen-limited or phosphorous-limited cultures. Toxicon 2008, 51(4):649-658.
18. Davey M., Tarran G.A., Mills M.M., Ridame C., Geider R.J., LaRoche J. Nutrient limitation of picophytoplankton photosynthesis and growth in the tropical North Atlantic. Limnology and Oceanography 2008, 53(5):1722-1733.
19. Davidson K., Gurney W.S.C. An investigation of non-steady-state algal growth. II. Mathematical modelling of co-nutrient-limited algal growth. Journal of Plankton Research 1999, 21(5):839-858.
20. Davies A.G., Sleep J.A. The photosynthetic response of nutrient-depleted dilute cultures of Skeletonema costatum to pulses of ammonium and nitrate; the importance of phosphate. Journal of Plankton Research 1989, 11:141-164.
21. 12 and marine ecology. IV. The kinetics of uptake, growth and inhibition in Monochrysis lutheri. Journal of Marine Biology 1968, 48:689-733.
22. 12 and marine ecology. IV. The kinetics of uptake growth and inhibition in Monochrysis lutheri. Journal of the Marine Biological Association 1968, 48(3):689-733.
23. Droop M.R. Some thoughts on nutrient limitation in algae. Journal of Phycology 1973, 9:264-272.
24. Droop M.R. The nutrient status of algal cells in continuous culture. Journal of the Marine Biological Association of the United Kingdom 1974, 54:825-855.
25. Droop M.R. 25 years of algal growth kinetics. A personal view. Botanica Marina 1983, 26:99-112.
26. Dugdale R.C. Nutrient limitation in the sea: dynamics, identification and significance. Limnology and Oceanography 1967, 12:685-695.
27. Elrifi I.R., Turpin D.H. Steady-state luxury consumption and the concept of optimum nutrient ratios: a study with phosphate and nitrate limited Selenastrum minutum (chlorophyta). Journal of Phycology 1985, 21:592-602.
28. Elser J., Marzolf E., Goldman C. Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: a review and critique of experimental enrichments. Canadian Journal of Fisheries and Aquatic Sciences 1990, 47(7):1468-1477.
29. Falkowski P.G., Stone D.P. Nitrate uptake in marine phytoplankton: energy sources and the interaction with carbon fixation. Marine Biology 1975, 32(1):77-84.
30. Flynn J.K. The importance of the form of the quota curve and control of non-limiting nutrient transport in phytoplankton models. Journal of Plankton Research 2008, 30:423-438.
31. Forde B.G. Nitrate transporters in plants: structure, function and regulation. Biochimica et Biophysica Acta 2000, 1465:219-235.
32. Geider R.J., LaRoche J. Redfield revisited: variability of c:n:p in marine microalgae and its biochemical basis. European Journal of Phycology 2002, 37:1-17.
33. Glover H.E., Garside C., Trees C.C. Physiological responses of Sargasso Sea picoplankton to nanomolar nitrate perturbations. Journal of Plankton Research 2007, 29(3):263-274.
34. Goldman J.C., Peavey D.G. Steady-state growth and chemical composition of the marine chlorophyte Dunaliella tertiolecta in nitrogen-limited continuous cultures. Applied and Environmental Microbiology 1979, 38:894-901.
35. Gotham I.J., Rhee G.-Y. Comparative kinetic studies of phosphate-limited growth and phosphate uptake in phytoplankton in continuous culture. Journal of Phycology 1981, 17:257-265.
36. Healey F.P. Interacting effects of light and nutrient limitation on the growth rate of Synechococcus linearis (cyanophyceae). Journal of Phycology 1985, 21(1):134-146.
37. Healey F.P., Hendzel L.L. Effect of phosphorus deficiency on 2 algae growing in chemostats. Journal of Phycology 1975, 11:303-309.
38. Hunter B.L., Laws E.A. Atp and chlorophyll a as estimators of phytoplankton carbon biomass. Limnology and Oceanography 1981, 26(5):944-956.
39. Karl D.M., Craven D.B. Effects of alkaline phosphatase activity on nucleotide measurements in aquatic microbial communities. Applied and Environmental Microbiology 1980, 40(3):549-561.
40. Ketchum B.H. The absorption of phosphate and nitrate by illuminated cultures of Nitzschia closterium. American Journal of Botany 1939, 26(6):399-407.
41. Klausmeier C.A., Litchman E., Daufresne T., Levin S.A. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 2004, 429:171-174.
42. Klausmeier C.A., Litchman E., Levin S.A. Phytoplankton growth and stoichiometry under multiple nutrient limitation. Limnology and Oceanography 2004, 49:1463-1470.
43. Klausmeier C.A., Litchman E., Levin S.A. A model of flexible uptake of two essential resources. Journal of Theoretical Biology 2007, 246:278-289.
44. Lange K., Oyarzun F.J. The attractiveness of the Droop equations. Mathematical Biosciences 1992, 111:261-278.
45. Laws E.A., Bannister T.T. Nutrient- and light-limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean. Limnology and Oceanography 1980, 25(3):457-473.
46. Laws E.A., Karl D.M., Redalje D.G., Jurick R.S., Winn C.D. Variability in ratios of phytoplankton carbon and rna to atp and chlorophyll a in batch and continuous cultures. Journal of Phycology 1983, 19(4):439-445.
47. Legovic T., Cruzado A. A model of phytoplankton growth on multiple nutrients based on the Michaelis-Menten-Monod uptake, Droop's growth and Liebig's law. Ecological Modelling 1997, 99(1):19-31.
48. Lehman J., Botkin D., Likens G. The assumptions and rationales of a computer model of phytoplankton population dynamics. Limnology and Oceanography 1975, 20(3):343-364.
49. Leonardos N., Geider R.J. Elemental and biochemical composition of Rhodomonas reticulata (cryptophyta) in relation to light and nitrate-to-phosphate supply ratios. Journal of Phycology 2005, 41:567-576.
50. Maberly S.C., King L., Dent M.M., Jones R.I., Gibson C.E. Nutrient limitation of phytoplankton and periphyton growth in upland lakes. Freshwater Biology 2002, 47:2136-2152.
51. Morel F.M.M. Kinetics of nutrient uptake and growth in phytoplankton. Journal of Phycology 1987, 23:137-150.
52. Nielsen E.S. Growth of plankton algae as a function of n-concentration, measured by means of batch technique. Marine Biology 1978, 46(3):185-189.
53. Pahlow M. Linking chlorophyll-nutrient dynamics to the redfield n:c ratio with a model of optimal phytoplankton growth. Marine Ecology Progress Series 2005, 287:33-43.
54. Pahlow M., Oschlies A. Chain model of phytoplankton p, n and light colimitation. Marine Ecology Progress Series 2009, 376:69-83.
55. Perry M.J. Phosphate utilization by an oceanic diatom in phosphorus-limited chemostat culture and in oligotrophic waters of central North-Pacific. Limnology and Oceanography 1976, 21(1):88-107.
56. Persic V., Horvatic J., Has-Schon E., Bogut I. Changes in n and p limitation induced by water level fluctuations in Nature Park Kopacki Rit (croatia): nutrient enrichment bioassay. Aquatic Ecology 2009, 43(1):27-36.
57. Ren L., Rabalais N.N., Turner R.E., Morrison W., Mendenhall W. Nutrient limitation on phytoplankton growth in the upper Barataria Basin, Louisiana: microcosm bioassays. Estuaries and Coasts 2009, 32(5):958-974.
58. Rhee G.Y. Phosphate uptake under nitrate limitation by Scenedesmus sp. and its ecological implications. Journal of Phycology 1974, 10:470-475.
59. Rhee G.Y. Effects of n:p atomic ratios and nitrate limitation on algal growth, cell composition, and nitrate uptake. Limnology and Oceanography 1978, 23:10-24.
60. Saito M.A., Goepfert T.J., Ritt J.T. Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability. Limnology and Oceanography 2008, 53:276-290.
61. Sciandra A., Ramani P. The limitations of continuous cultures with low rates of medium renewal per cell. Journal of Experimental Marine Biology and Ecology 1994, 178:1-15.
62. Seppala J., Tamminen T., Kaitala S. Experimental evaluation of nutrient limitation of phytoplankton communities in the Gulf of Riga. Journal of Marine Systems 1999, 23:107-126.
63. Smalley G.W., Coats D.W., Stoecker D.K. Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Marine Ecology Progress Series 2003, 262:137-151.
64. Smith S.L., Yamanaka Y. Optimization-based model of multinutrient uptake kinetics. Limnology and Oceanography 2007, 54(4):1545-1558.
65. Suttle C., Harrison P. Ammonium and phosphate uptake rates, n:p supply ratios, and evidence for n and p limitation in some oligotrophic lakes. Limnology and Oceanography 1988, 33(2):186-202.
66. Terry K.L. Nitrogen and phosphorus requirements of Pavlova lutheri in continuous culture. Botanica Marina 1980, 23:757-764.
67. Terry K.L. Nitrate and phosphate uptake interactions in a marine prymnesiophyte. Journal of Phycology 1982, 18:79-86.
68. Vatcheva I., de Jong H., Bernard O., Mars N. Experiment selection for the discrimination of semi-quantitative models of dynamical systems. Artificial Intelligence 2006, 170:472-506.
69. Zohary T., Herut B., Krom M.D., Mantoura R.F.C., Pitta P., Psarra F.R.S., Stambler N., Tanaka T., Thingstad T.F., Woodward E.M.S. P-limited bacteria but n and p co-limited phytoplankton in the Eastern Mediterranean-a microcosm experiment. Deep Sea Research Part II: Topical Studies in Oceanography on the Nature of Phosphorus Cycling and Limitation in the Eastern Mediterranean 2005, 52:3011-3023.