Global Transcriptional Responses of the Toxic Cyanobacterium, Microcystis aeruginosa, to Nitrogen Stress, Phosphorus Stress, and Growth on Organic Matter

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Harke, Matthew J ^a   Gobler, Christopher J ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; BACTERIAL ENZYME; INORGANIC COMPOUND; MICROCYSTIN; MICROCYSTIN SYNTHETASE; NITROGEN; ORGANIC MATTER; PHOSPHORUS; TRANSCRIPTOME; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL METABOLISM; CELLULAR STRESS RESPONSE; CONCENTRATION (PARAMETERS); CYTOTOXICITY; GENE EXPRESSION; GENE INDUCTION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; MICROCYSTIS AERUGINOSA; MOLECULAR WEIGHT; NONHUMAN; OPERON; PHOTOSYNTHESIS; PHOX GENE; PSTABC GENE; REGULON; SPHX GENE; UREA TRANSPORT GENE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BRAIN MAPPING; CASE-CONTROL STUDIES; CELL PHYSIOLOGICAL PHENOMENA; FEMALE; FLUORODEOXYGLUCOSE F18; FOLLOW-UP STUDIES; GLUCOSE; HUMANS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; NEURAL NETWORKS (COMPUTER); NEUROIMAGING; POSITRON-EMISSION TOMOGRAPHY;

EID: 84880747816     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069834     Document Type: Article

References (112)

1. Chorus I, Bartram J (1999) Toxic Cyanobacteria in Water: A guide to their public health consequences, monitoring and management. London: E & FN Spon.
2. Hudnell HK, Dortch Q, Zenick H (2008) Chapter 1: An overview of the interagency, international symposium on cyanobacterial harmful algal blooms (ISOC-HAB): Advancing the scientific understanding of freshwater harmful algal blooms. In: Hudnell HK, editor. Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs. Berlin: Springer-Verlag Berlin. 1-16.
3. Reynolds CS, Jaworski GHM, Cmiech HA, Leedale GF, (1981) On the Annual Cycle of the Blue-Green Alga Microcystis aeruginosa Kütz. Emend. Elenkin. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 239: 419-477.
4. Okino T, (1974) Studies on the Blooming of Microcystis aeruginosa. II: Rapid Accumulation of Phosphate by Microcystis aeruginosa. Journal of the Faculty of Science, Shinshu University 8: 135-145.
5. Jacoby JM, Collier DC, Welch EB, Hardy FJ, Crayton M, (2000) Environmental factors associated with a toxic bloom of Microcystis aeruginosa. Canadian Journal of Fisheries and Aquatic Sciences 57: 231-240.
6. Perovich G, Dortch Q, Goodrich J, Berger PS, Brooks J, et al. (2008) Chapter 9: Causes, prevention, and mitigation workgroup report. In: Hudnell HK, editor. Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs. Berlin: Springer-Verlag Berlin. 185-215.
7. Dolman AM, Rucker J, Pick FR, Fastner J, Rohrlack T, et al. (2012) Cyanobacteria and Cyanotoxins: The Influence of Nitrogen versus Phosphorus. PLoS ONE 7: e38757.
8. Schindler DE, Carpenter SR, Cole JJ, Kitchell JF, Pace ML, (1997) Influence of food web structure on carbon exchange between lakes and the atmosphere. Science 277: 248-251.
9. Hecky RE, Kilham P, (1988) Nutrient limitation of phytoplankton in fresh-water and marine environments- A review of recent evidence on the effects of enrichment. Limnology and Oceanography 33: 796-822.
10. Likens GE, Bartsch AF, Lauff GH, Hobble JE, (1971) Nutrients and Eutrophication. Science 172: 873-874.
11. Smith VH, (1983) Low Nitrogen to Phosphorus Ratios Favor Dominance by Blue-green Algae in Lake Phytoplankton. Science 221: 669-671.
12. Kotak BG, Lam AKY, Prepas EE, Kenefick SL, Hrudey SE, (1995) Variability of the hepatotoxin microcystin-LR in hypereutrophic drinking water lakes. Journal of Phycology 31: 248-263.
13. 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.
14. Davis TW, Harke MJ, Marcoval MA, Goleski J, Orano-Dawson C, et al. (2010) Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms. Aquatic Microbial Ecology 61: 149-162.
15. Orr PT, Jones GJ, (1998) Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnology and Oceanography 43: 1604-1614.
16. Watanabe MF, Oishi S, (1985) Effects of Environmental Factors on Toxicity of a Cyanobacterium (Microcystis aeruginosa) under Culture Conditions. Applied and Environmental Microbiology 49: 1342-1344.
17. Codd GA, Poon GK (1988) Biochemistry of the Algae and Cyanobacteria; Rogers LJ, Gallon JR, editors. Oxford Clarendon Press.
18. Gobler CJ, Davis TW, Coyne KJ, Boyer GL, (2007) Interactive influences of nutrient loading, zooplankton grazing, and microcystin synthetase gene expression on cyanobacterial bloom dynamics in a eutrophic New York lake. Harmful Algae 6: 119-133.
19. Moisander PH, Ochiai M, Lincoff A, (2009) Nutrient limitation of Microcystis aeruginosa in northern California Klamath River reservoirs. Harmful Algae 8: 889-897.
20. Utkilen H, Gjølme N, (1995) Iron-stimulated toxin production in Microcystis aeruginosa. Applied and Environmental Microbiology 61: 797-800.
21. Paerl HW, Fulton III RS, Moisander PH, Dyble J, (2001) Harmful Freshwater Algal Blooms, With an Emphasis on Cyanobacteria. The Scientific World 1: 76-116.
22. Paerl HW, (1988) Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnololgy and Oceanography 33: 823-847.
23. Paerl HW (2008) Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum. In: Hudnell HK, editor. Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs: Springer. 217-237.
24. Bertram PE, (1993) Total phosphorus and dissolved oxygen trends in the central basin of Lake Erie, 1970-1991. Journal of Great Lakes Research 19: 224-236.
25. Wilhelm SW, DeBruyn JM, Gillor O, Twiss MR, Livingston K, et al. (2003) Effect of phosphorus amendments on present day plankton communities in pelagic Lake Erie. Aquatic Microbial Ecology 32: 275-285.
26. Stumpf RP, Wynne TT, Baker DB, Fahnenstiel GL, (2012) Interannual Variability of Cyanobacterial Blooms in Lake Erie. PLoS ONE 7: e42444.
27. Berman T, Bronk DA, (2003) Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems. Aquatic Microbial Ecology 31: 279-305.
28. Dai R, Liu H, Qu J, Zhao X, Hou Y, (2009) Effects of amino acids on microcystin production of the Microcystis aeruginosa. Journal of Hazardous Materials 161: 730-736.
29. Berman T, Chava S, (1999) Algal growth on organic compounds as nitrogen sources. Journal of Plankton Research 21: 1423-1437.
30. Gilbert 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. Marine Ecology Progress Series 280: 73-83.
31. Whitton BA, Grainger SLJ, Hawley GRW, Simon JW, (1991) Cell-Bound and Extracellular Phosphatase Activities of Cyanobacterial Isolates. Microbial Ecology 21: 85-98.
32. Dyhrman S, Chappell P, Haley S, Moffett J, Orchard E, et al. (2006) Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439: 68-71.
33. Vahtera E, Laamanen M, Rintala JM, (2007) Use of different phosphorus sources by the bloom-forming cyanobacteria Aphanizomenon flos-aquae and Nodularia spumigena. Aquatic Microbial Ecology 46: 225-237.
34. Harke MJ, Berry DL, Ammerman JW, Gobler CJ, (2012) Molecular Response of the Bloom-Forming Cyanobacterium, Microcystis aeruginosa, to Phosphorus Limitation. Microbial Ecology 63: 188-198.
35. Kaneko T, Nakajima N, Okamoto S, Suzuki I, Tanabe Y, et al. (2007) Complete genomic structure of the bloom-forming toxic cyanobacterium Microcystis aeruginosa NIES-843. DNA Research 14: 247-256.
36. Frangeul L, Quillardet P, Castets A-M, Humbert J-F, Matthijs HC, et al. (2008) Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium. BMC Genomics 9: 274.
37. Ludwig M, Bryant DA, (2011) Acclimation of the global transcriptome of the cyanobacterium Synechococcus sp. strain PCC7002 to nutrient limitations and different nitrogen sources. Frontiers in Microbiology 3: 1-15.
38. Zinser ER, Lindell D, Johnson ZI, Futschik ME, Steglich C, et al. (2009) Choreography of the Transcriptome, Photophysiology, and Cell Cycle of a Minimal Photoautotroph, Prochlorococcus. PLoS ONE 4: e5135.
39. Thompson AW, Huang K, Saito MA, Chisholm SW, (2011) Trasncriptome response of high- and low-light-adapted Prochlorococcus strains to changing iron availability. The ISME Journal 10: 1580-1594.
40. Flaherty BL, Nieuwerburgh FV, Head SR, Golden JW (2011) Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp. strain PCC 7120 to combinded-nitrogen deprivation. BMC Genomics 12.
41. Wurch LL, Haley ST, Orchard ED, Gobler CJ, Dyhrman ST, (2011) Nutrient-regulated transcriptional responses in the brown tide-forming alga Aureococcus anophagefferens. Environmental Microbiology 13: 468-481.
42. Moustafa A, Evans AN, Kulis DM, Hackett JD, Erdner DL, et al. (2011) Transcriptome Profiling of a Toxic Dinoflagellate Reveals a Gene-Rich Protist and a Potential Impact on Gene Expression Due to Bacterial Presence. PLoS ONE 5: 1-10.
43. Erdner DL, Anderson DM, (2006) Global transcriptional profiling of the toxic dinoflagellate Alexandrium fundyense using Massively Parallel Signature Sequencing. BMC Genomics 7: 1471-2164.
44. Straub C, Quillardet P, Vergalli J, de Marsac NT, Humbert J-F, (2011) A Day in the Life of Microcystis aeruginosa Strain PCC 7806 as Revealed by a Transcriptomic Analysis. PLoS ONE 6: e16208.
45. Brittain SM, Wang J, Babcock-Jackson L, Carmichael WW, Rinehart KL, et al. (2000) Isolation and characterization of microcystins, cyclic heptapeptide hepatotoxins from a Lake Erie strain of Microcystis aeruginosa. Journal of Great Lakes Research 26: 241-249.
46. Gobler CJ, Sañudo-Wilhelmy SA, (2003) Cycling of colloidal organic carbon and nitrogen during an estuarine phytoplankton bloom. Limnology and Oceanography 48: 2314-2320.
47. Dempster EL, Pryor KV, Francis D, Young JE, Rogers HJ, (1999) Rapid DNA extraction from ferns for PCR-based analyses. Biotechniques 27: 66-68.
48. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
49. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quanitification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28: 511-515.
50. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, et al. (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotech 31: 46-53.
51. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7: 567-578.
52. Bullard JH, Purdom E, Hansen KD, Dudoit S (2010) Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 11.
53. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology 11.
54. Guillard RRL (1973) Division Rates. In: Stein, editor. Handbook of Phycological Methods. Cambridge: Cambridge University Press. 289-312.
55. Jones MN, (1984) Nitrate reduction by shaking with cadmium: Alternative to cadmium columns. Water Research 18: 643-646.
56. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Oxford: Pergamon Press.
57. Valderrama JC, (1981) The simultaneous analysis of total nitrogen and phosphorus in natural waters. Marine Chemistry 10: 109-122.
58. Price NM, Harrison PJ, (1987) Comparison of methods for the analysis of dissolved urea in seawater. Marine Biology 94: 307-317.
59. Fischer WJ, Garthwaite I, Miles CO, Ross KM, Aggen JB, et al. (2001) Congener-independent immunoassay for microcystins and nodularins. Environmental Science & Technology 35: 4849-4856.
60. Hoppe HG, (1983) Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Marine Ecology-Progress Series 11: 299-308.
61. Simis SGH, Huot Y, Babin M, Seppälä J, Metsamaa L, (2012) Optimization of variable fluorescence measurements of phytoplankton communities with cyanobacteria. Photosynthesis Research 112: 13-30.
62. Montané M-H, Dreyer S, Triantaphylides C, Kloppstech K, (1997) Early light-inducible proteins during long-term acclimation of barley to photooxidative stress caused by light and cold: high level of accumulation by posttranscriptional regulation. PLanta 202: 293-302.
63. Montané M-H, Petzold B, Kloppstech K, (1999) Formation of early-light-inducible-protein complexes and status of xanthophyll levels under high light and cold stress in barley (Hordeum vulgare L.). Planta 208: 519-527.
64. Ouellette AJA, Handy SM, Wilhelm SW, (2006) Toxic Microcystis is widespread in Lake Erie: PCR detection of toxin genes and molecular characterization of associated cyanobacterial communities. Microbial Ecology 51: 154-165.
65. Isvánovics V, Shafik HM, Présing M, Juhos S, (2000) Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshwater Biology 43: 257-275.
66. Horst GP, Sarnelle O (2009) Phosphorus uptake physiology of Microcystis and competing taxa along a nutrient gradient in western Lake Erie. 52nd Annual Conference on Great Lakes Research International Association for Great Lakes Research. Toledo, Ohio, USA. 95.
67. Rinta-Kanto JM, Ouellette AJA, Boyer GL, Twiss MR, Bridgeman TB, et al. (2005) Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-time PCR. Environmental Science & Technology 39: 4198-4205.
68. Vézie C, Rapala J, Vaitomaa J, Seitsonen J, Sivonen K, (2002) Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microbial Ecology 43: 443-454.
69. Rapala J, Sivonen K, Lyra C, Niemela SI, (1997) Variation of microcystin, cyanobacterial hepatotoxins, in Anabaena spp as a function of growth stimulation. Applied and Environmental Microbiology 63: 2206-2212.
70. Herrero A, Muro-Pastor AM, Flores E, (2001) Nitrogen Control in Cyanobacteria. Journal of Bacteriology 183: 411-425.
71. Ohashi Y, Shi W, Takatini N, Aichi M, Maeda S-i, et al. (2011) Regulation of nitrate assimilation in cyanobacteria. Journal of experimental Botany 62: 1411-1424.
72. Frias JE, Flores E, Herrero A, (1997) Nitrate Assimilation Gene Cluster from the Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120. Journal of Bacteriology 179: 477-486.
73. Kikuchi H, Aichi M, Suzuki I, Omata T, (1996) Positive Regulation by Nitrite of the Nitrate Assimilation Operon in the Cyanobacteria Synechococcus sp. Strain PCC 7942 and Plectonema boryanum. Journal of Bacteriology 178: 5822-5825.
74. Suzuki I, Sugiyama T, Omata T, (1993) Primary Structure and Transcriptional Regulation of the Gene for Nitrite Reductase from the Cyanobacterium Synechococcus PCC 7942. Plant and Cell Physiology 34: 1311-1320.
75. Debussche L, Thibaut D, Cameron B, Crouzet J, Blanche F, (1993) Biosynthesis of the Corrin Macrocycle of Coenzyme B12 in Pseudomonas denitrificans. Journal of Bacteriology 175: 7430-7440.
76. Antia NJ, Harrison PJ, Oliveira L, (1991) The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology. Phycologia 30: 1-89.
77. Cho BC, Park MG, Shim JH, Azam F, (1996) Significance of bacteria in urea dynamics in coastal surface waters. Marine Ecology Progress Series 142: 19-26.
78. Xu X, Elhai J, Wolk CP (2008) Transcriptional and Developmental Responses by Anabaena to Deprivation of Fixed Nitrogen. In: Herrero A, Flores E, editors. The Cyanobacteria: Molecular Biology, Genomics and Evolution. Norfolk, UK: Caister Academic Press.
79. Mobley HLT, Island MD, Hausinger RP, (1995) Molecular Biology of Microbial Ureases. Microbiological Reviews 59: 451-480.
80. Kamel M, Ragaa R, (1973) Constitutive synthesis of urease in Aerobacter aerogenese PRL-R3. The effect of different nitrogenous compounds on its inhibition and formation. Acta biologica et medica Germanica 30: 457.
81. Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, et al. (2009) Ecological Genomics of Marine Picocyanobacteria. Microbiol Mol Biol Rev 73: 249-299.
82. Pitt FD, Mazard S, Humphreys L, Scanlan DJ, (2010) Functional Characterization of Synechocystis sp Strain PCC 6803 pst1 and pst2 Gene Clusters Reveals a Novel Strategy for Phosphate Uptake in a Freshwater Cyanobacterium. Journal of Bacteriology 192: 3512-3523.
83. Van Mooy BAS, Rocap G, Fredricks HF, Evans CT, Devol AH, (2006) Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marne environments. Proceedings of the National Academy of Sciences 103: 8607-8612.
84. Benning C, (1998) Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu Rev Plant Physiol Plant Mol Biol 49: 53-75.
85. Collier JL, Grossman AR, (1992) Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. Journal of Bacteriology 174: 4718-4726.
86. Allen MM, Smith AJ, (1969) Nitrogen Chlorosis in Blue-Green Algae. Arch Mikrobiol 69: 114-120.
87. Collier JL, Grossman AR, (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. The EMBO Journal 13: 1039-1047.
88. Geider RJ, MacIntyre HL, Kana TM, (1998) A Dynamic Regulatory Model of Phytoplanktonic Acclimation to Light, Nutrients, and Temperature. Limnology and Oceanography 43: 679-694.
89. Turpin DH, (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. Journal of Phycology 27: 14-20.
90. Collier JL, Brahamsha B, Palenik B, (1999) The marine cyanobacterium Synechococcus sp. WH7805 requires urease (urea amidohydrolase, EC 3.5.1.5) to utilize urea as a nitrogen source: molecular-genetic and biochemmical analysis of the enzyme. Microbiology 145: 447-459.
91. Ge X, Cain K, Hirschberg R, (1990) Urea metabolism and urease regulation n the cyanobacterium Anabaena variabilis. Canadian Journal of Microbiology 36: 218-222.
92. Herrero A, Flores E, (1990) Transport of Basic Amino Acids by the Dinitrogen-fixing Cyanobacterium Anabaena PCC 7120. The Journal of Biological Chemistry 265: 3931-3935.
93. Pernil R, Picossi S, Mariscal V, Herrero A, Flores E, (2008) ABC-type amino acid uptake transporters Bgt and N-II of Anabaena sp strain PCC 7120 share an ATPase subunit and are expressed in vegetative cells and heterocysts. Molecular Microbiology 67: 1067-1080.
94. Quintero MJ, Montesinos ML, Herrero A, Flores E, (2001) Identification of genes encoding amino acid permeases by inactivation of selected ORFs from the Synechocystis genomic sequence. Genome Research 11: 2034-2040.
95. Berg GM, Repeta DJ, LaRoche J, (2003) The role of the picoeukaryote Aureococcus anophagefferens in cycling of marine high-molecular weight dissolved organic nitrogen. Limnology and Oceanography 48: 1825-1830.
96. Stolte W, Panosso R, Gisselson L-Å, Granéli E, (2002) Utilization efficiency of nitrogen associated with riverine dissolve dorganic carbon (>1 kDa) by two toxin-producing phytoplankton species. Aquatic Microbial Ecology 29: 97-105.
97. Stolte W, Balode M, Carlsson P, Grzebyk D, Janson S, et al. (2006) Stimulation of nitrogen-fixing cyanobacteria in a Baltic Sea plankton community by land-derived organic matter or iron addition. Marine Ecology Progress Series 327: 71-82.
98. Aravind L, Koonin EV, (2002) Classification of the caspase-hemoglobinase fold: detection of new families and implications for the origin of the eukaryotic separins. Proteins 46: 355-367.
99. Lawrence SA (2004) Amines: synthesis, properties and applications.: Cambridge University Press.
100. Dirix G, Monsieurs P, Dombrecht B, Daniels R, Marchal K, et al. (2004) Peptide signal molecules and bacteriocins in Gram-negative bacteria: a genome-wide in silico screening for peptides containing a double-glycine leader sequence and their cognate transporters. Peptides 25: 1425-1440.
101. Sperandeo P, Cescutti R, Villa R, Di Benedetto C, Candia D, et al. (2007) Characterization of lptA and lptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. Journal of Bacteriology 189: 244-253.
102. Goldman JC, McCarthy JJ, Peavey DG, (1979) Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279: 210-215.
103. Haugen SP, Ross W, Gourse RL, (2008) Advances in bacterial promoter recognition and its control by factors that do not bind DNA. Nature Reviews Microbiology 6: 507-519.
104. Klumpp S, Zhang Z, Hwa T, (2009) Growth Rate-Dependent Global Effects on Gene Expression in Bacteria. Cell 139: 1366-1375.
105. Brunberg A-K, (1999) Contribution of bacteria in the mucilage of Microcystis spp. (Cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiology Ecology 29: 13-22.
106. Kirchman DL, (1994) The Uptake of Inorganic Nutrients by Heterotrophic Bacteria. Microbial Ecology 28: 255-271.
107. Azam F, Smith DC, Steward GF, Hagström Å, (1994) Bacteria-Organic Matter Coupling and Its Significance for Oceanic Carbon Cycling. Microbial Ecology 28: 167-179.
108. Nagata S, Tsutsumi T, Hasegawa A, Yoshida F, Ueno Y, et al. (1997) Enzyme immunoassay for direct determination of microcystins in environmental water. Journal of AOAC International 80: 408-417.
109. Tillett D, Dittmann E, Erhard M, Döhren Hv, Börner T, et al. (2000) Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chemistry and Biology 7: 753-764.
110. Hesse K, Dittmann E, Börner T, (2001) Consequences of impaired microcystin production for light-dependent growth and pigmentation of Microcystis aeruginosa PCC 7806. FEMS Microbiology Ecology 37: 39-43.
111. Van de Waal DB, Verspagen JMH, Lürling M, Donk EV, Visser PM, et al. (2009) The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis. Ecology Letters 12: 1326-1335.
112. Yoshida M, Yoshida T, Takashima Y, Hosoda N, Hiroishi S, (2007) Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiology Letters 266: 49-53.