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Microcystin production in Microcystis aeruginosa: effect of type of strain, environmental factors, nutrient concentrations, and N:P ratio on mcyA gene expression

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Abstract

Blooms affect water quality mainly due to the release of microcystins (MCs) by cyanobacteria. The synthesis of MCs is influenced by factors such as nutrient concentration, temperature, pH, light intensity, salinity, turbidity, and the presence of xenobiotics. In this study, we evaluated the effect of environmental factors (temperature and light intensity), the concentration of three nutrients (NaNO3, K2HPO4, and FeCl3), and the N:P ratio on the growth of two Microcystis aeruginosa strains (Ch10 and UTEX LB2385), as well as on mcyA gene expression and intracellular MC concentration. Under similar conditions, the population growth and chlorophyll a concentration per cell of both strains were different. The mcyA gene was significantly up-regulated from the early growth phase (5 days) to the stationary phase (15 days) in most cases, whereas intracellular MC concentrations varied depending on the assessed factor. The N:P ratio affected the development of both strains and MCs production differently. High concentration of intracellular MCs was recorded at low nitrogen and iron concentrations, low temperature, and high light intensity. The response in mcyA gene expression, related to the incubation time, of both strains was different, because strain Ch10 responded in most cases starting at 5 days of growth, whereas UTEX LB2385 responded until 10 and 15 days. This difference reflects physiological plasticity that could help to understand the permanence and dominance of Microcystis genus blooms in eutrophic freshwaters. The variability in response to the tested environmental factors confirms that population growth, genetic expression, and microcystin production are not related to a single factor but to an array of conditions that, when combined, stimulate MCs production. These conditions can be both stress-causing and favorable; hence, monitoring of environmental factors aimed at alerting against health risks provoked by cyanotoxins is a very complex task.

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References

  • Alexova R, Fujii M, Birch D, Cheng J, Waite TD, Ferrari BC, Neilan BA (2011a) Iron uptake and toxin synthesis in the bloom-forming Microcystis aeruginosa under iron limitation. Environ Microbiol 13:1064–1077

    Article  CAS  PubMed  Google Scholar 

  • Alexova R, Haynes PA, Ferrari BC, Neilan BA (2011b) Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa. Mol Cell Proteomics 10:1–16

    Article  Google Scholar 

  • Amé MV, Wunderlin DA (2005) Effects of iron, ammonium and temperature on microcystin content by a natural concentrated Microcystis aeruginosa population. Water Air Soil Pollut 168:235–248

    Article  Google Scholar 

  • Amé MV, Díaz MP, Wunderlin DA (2003) Occurrence of toxic cyanobacterial blooms in San Roque Dam (Córdoba—Argentina): a field and chemometric study. Environ Toxicol 18:192–201

    Article  PubMed  Google Scholar 

  • Arzate-Cárdenas M, Olvera-Ramírez R, Martínez-Jerónimo F (2010) Microcystis toxigenic strains in urban lakes: a case of study in Mexico City. Ecotoxicology 19:1157–1165

    Article  PubMed  Google Scholar 

  • Bernard C, Monis P, Baker P (2004) Disaggregation of colonies of Microcystis (Cyanobacteria): efficiency of two techniques assessed using an image analysis system. J Appl Phycol 16:117–125

    Article  Google Scholar 

  • Bickel H, Lyck S (2001) Importance of energy charge for microcystin production. In: Chorus I (ed) Cyanotoxins—occurrence, causes, consequences. Springer, Berlin, pp 133–141

    Google Scholar 

  • Bittencourt-Oliviera MC, Oliviera MC, Pinto E (2011) Diversity of microcystin-producing genotypes in Brazilian strains of Microcystis (Cyanobacteria). Braz J Biol 71:209–216

    Article  Google Scholar 

  • Blackburn SI, McCausland MA, Bolch CJS, Newman SJ, Jones GJ (1996) Effect of salinity on growth and toxin production in cultures of the bloom-forming cyanobacteria Nodularia spumigena from Australian waters. Phycologia 35:511–522

    Article  Google Scholar 

  • Boopathi T, Ki JS (2014) Impact of environmental factors on the regulation of cyanotoxin production. Toxins 6:1951–1978

    Article  PubMed Central  PubMed  Google Scholar 

  • Briand E, Gugger M, François JC, Bernard C, Humbert JF, Quiblier C (2008) Temporal variations in the dynamics of potentially microcystin-producing strains in a bloom-forming Planktothrix agardhii (Cyanobacterium) population. Appl Environ Microbiol 74:3839–3848

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bulgakov NG, Levich AP (1999) Ammonium-nitrogen: a key regulatory factor causing dominance of non-nitrogen fixing cyanobacteria in aquatic systems. Arch Hidrobiol 132:141–164

    Google Scholar 

  • Carmichael WW (1992) Cyanobacteria secondary metabolites—the cyanotoxins. J Appl Bacteriol 72:445–459

    Article  CAS  PubMed  Google Scholar 

  • Carmichael WW (1997) The cyanotoxins. Adv Bot Res 27:211–240

    Article  CAS  Google Scholar 

  • Carmichael WW, Azevedo SM, An SI, Molica RJ, Jochimsen EM, Lau S, Rinehart KL, Shaw GR, Eaglesham GK (2001) Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environ Health Perspect 109:663–668

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chorus I (2001) Cyanotoxin occurrence in freshwaters—a summary of survey results from different countries. In: Chorus I (ed) Cyanotoxins. Springer, Berlin, pp 75–82

    Chapter  Google Scholar 

  • Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. WHO, London

    Book  Google Scholar 

  • Codd GA, Bell SG, Kaya K, Ward CJ, Beattie KA, Metcalf JS (1999) Cyanobacterial toxins, exposure routes and human health. Eur J Phycol 34:405–415

    Article  Google Scholar 

  • Dai GZ, Deblois CP, Liu SW, Juneau P, Qiu BS (2008) Differential sensitivity of five cyanobacterial strains to ammonium toxicity and its inhibitory mechanism on the photosynthesis of rice-field cyanobacterium Ge-**an Mi (Nostoc). Aquat Toxicol 89:113–121

    Article  CAS  PubMed  Google Scholar 

  • Dittmann E, Wiegand C (2006) Cyanobacterial toxins—occurrence, biosynthesis and impact on human affairs. Mol Nutr Food Res 50:7–17

    Article  CAS  PubMed  Google Scholar 

  • Downing JA, McCauley E (1992) The nitrogen:phosphorus relationship in lakes. Limnol Oceanogr 37:936–945

    Article  CAS  Google Scholar 

  • Downing TG, Sember CS, Gehringer MM, Leukes W (2005) Medium N:P ratios and specific growth rate comodulate microcystin and protein content in Microcystis aeruginosa PCC7806 and M. aeruginosa UV027. Microb Ecol 49:468–473

    Article  CAS  PubMed  Google Scholar 

  • Dziallas C, Grossart HP (2011) Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS ONE 6:e25569

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Falconer IR, Humpage AR (1996) Tumour promotion by cyanobacteria. Phycologia 35:74–79

    Article  Google Scholar 

  • Fujimoto N, Sudo R, Sugiura N, Inamori Y (1997) Nutrient-limited growth of Microcystis aeruginosa and Phormidium tenue ad competition under various N:P ratios and temperatures. Limnol Oceanogr 42:250–256

    Article  CAS  Google Scholar 

  • Giaramida L, Manage PM, Edwards C, Singh BK, Lawton LA (2013) Bacterial communities’ response to microcystins exposure and nutrient availability: linking degradation capacity to community structure. Int Biodeter Biodegr 84:111–117

    Article  CAS  Google Scholar 

  • Ginn HP, Pearson LA, Neilan BA (2010) NtcA from Microcystis aeruginosa PCC 7806 is autoregulatory and binds to the microcystin promoter. Appl Environ Mibrobiol 76:4362–4368

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Havens K, James RT, East TL, Smith VH (2003) N:P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environ Pollut 122:379–390

    Article  CAS  PubMed  Google Scholar 

  • Jacoby JM, Collier DC, Welch EB, Hardy FJ, Crayton M (2000) Environmental factors associated with a toxic bloom of Microcystis aeruginosa. Can J Fish Aquat Sci 57:231–240

    Article  Google Scholar 

  • Jonasson S, Vintila S, Sivonen K, El-Shehawy R (2008) Expression of the nodularin synthetase genes in the Baltic Sea bloom-former cyanobacterium Nodularia spumigena strain AV1. FEMS Microbiol Ecol 65:31–39

    Article  CAS  PubMed  Google Scholar 

  • Kaebernick M, Neilan BA (2001) Ecological and molecular investigations of cyanotoxin production. FEMS Microbiol Ecol 35:1–9

    Article  CAS  PubMed  Google Scholar 

  • Kaebernick M, Neilan BA, Börner T, Dittmann E (2000) Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl Environ Microbiol 66:3387–3392

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kameyama K, Sugiura N, Isoda H, Inamori Y, Maekawa T (2002) Effect of nitrate and phosphate concentration on production of microcystins by Microcystis viridis NIES 102. Aquat Ecosyst Health Manag 5:443–449

    Article  CAS  Google Scholar 

  • Kosakowska A, Nedzi M, Pempkowiak J (2007) Responses of the toxic cyanobacterium Microcystis aeruginosa to iron and humic substances. Plant Physiol Biochem 45:365–370

    Article  CAS  PubMed  Google Scholar 

  • Kotai J (1972) Instructions for preparation of modified Z8 for algae, B-11/69’. Norwegian Institute for Water Research Publication, Blinderan, Oslo

    Google Scholar 

  • Kotak BG, Lam AK-Y, Prepas EE, Hrudey SE (2000) Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes. Can J Fish Aquat Sci 57:1584–1593

    Article  CAS  Google Scholar 

  • Kurmayer R, Kutzenberger T (2003) Application of real-time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp. Appl Environ Microbiol 69:6723–6730

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lehman P, Boyer GL, Satchwell MF, Waller S (2008) The influence of environmental conditions on the seasonal variation of Microcystis cell density and microcystins concentration in San Francisco Estuary. Hydrobiologia 600:187–204

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Long BM, Jones GJ, Orr PT (2001) Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted from growth rate. Appl Environ Microbiol 67:278–283

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lukaĉ M, Aegerter R (1993) Influence of trace metals on growth and toxin production of Microcystis aeruginosa. Toxicon 31:293–305

    Article  PubMed  Google Scholar 

  • Lyck S, Christoffersen K (2003) Microcystin quota, cell division and microcystin net production of precultured Microcystis aeruginosa CYA288 (Chroococcales: Cyanophyceae) under field conditions. Phycologia 42:667–674

    Article  Google Scholar 

  • Lyck S, Gjølme N, Utkilen H (1996) Iron starvation increases toxicity of Microcystis aeruginosa CYA 228/1 (Chroococcales, Cyanophyceae). Phycologia 35:120–124

    Article  Google Scholar 

  • Marinho MM, Azevedo SMFO (2007) Influence of N/P ratio on competitive abilities for nitrogen and phosphorus by Microcystis aeruginosa and Aulacoseira distans. Aquatic Ecol 41:525–533

    Article  CAS  Google Scholar 

  • Martin-Luna B, Sevilla E, Hernandez JA, Bes MT, Fillat MF, Peleato ML (2006) Fur from Microcystis aeruginosa binds in vitro promoter regions of the microcystin biosynthesis gene cluster. Phytochemistry 67:876–881

    Article  CAS  PubMed  Google Scholar 

  • Martin-Luna B, Sevilla E, Fillat MF, Peleato ML, Gonzalez A, Bes MT (2011) Expression of fur and its antisense α-fur from Microcystis aeruginosa PCC7806 as response to light and oxidative stress. J Plant Physiol 168:2244–2250

    Article  CAS  PubMed  Google Scholar 

  • Moreira C, Vasconcelos V, Antunes A (2013) Phylogeny of microcystins: evidence of a biogeographical trend? Curr Microbiol 66:214–221

    Article  CAS  PubMed  Google Scholar 

  • Msagati TAM, Siame BA, Shushu DD (2006) Evaluation of methods for the isolation, detection and quantification of cyanobacterial hepatotoxins. Aquat Toxicol 78:382–397

    Article  CAS  PubMed  Google Scholar 

  • Neilan BA, Dittmann E, Rouhiainen L, Bass RA, Schaub V, Sivonen K, Börner T (1999) Nonribosomal peptide synthesis and toxigenicity of cyanobacteria. J Bacteriol 181:4089–4097

    PubMed Central  CAS  PubMed  Google Scholar 

  • Oh HM, Lee S, Jang MH, Yoon BD (2000) Microcystin production by Microcystis aeruginosa in a phosphorus-limited chemostat. Appl Environ Microbiol 66:176–179

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Orr PT, Jones GJ (1998) Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnol Oceanogr 43:1604–1614

    Article  CAS  Google Scholar 

  • Pearson L, Mihali T, Moffitt M, Kellmann R, Neilan B (2010) On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Mar Drugs 8:1650–1680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pflugmacher S, Wiegand C (2001) Metabolism of microcystin-LR in aquatic organism. In: Chorus I (ed) Cyanotoxins. Springer, Berlin, pp 257–260

    Google Scholar 

  • Pflugmacher S, Codd GA, Steinberg CEW (1999) Effects of the cyanobacterial toxin microcystin-LR on detoxication enzymes in aquatic plants. Environ Toxicol 14:111–115

    Article  CAS  Google Scholar 

  • Pineda-Mendoza R, Zúñiga G, Martínez Jerónimo F (2014) Infochemicals released by Daphnia magna fed on Microcystis aeruginosa affect mcyA gene expression. Toxicon 80:78–86

    Article  CAS  PubMed  Google Scholar 

  • Rantala A, Fewer P, Hisbergues M, Rouhiainen L, Vaitomaa J, Börner T, Sivonen K (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci USA 101:568–573

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rapala J, Sivonen K (1998) Assessment of environmental conditions that favour hepatotoxic and neurotoxic Anabaena spp. Strains in cultured under light-limitation at different temperatures. Microbial Ecol 36:181–192

    Article  CAS  Google Scholar 

  • Rapala J, Sivonen K, Lyra C, Niemelä SI (1997) Variation of microcystins, cyanobacterial hepatotoxins in Anabaena spp. as a function of growth stimuli. Appl Environ Microbiol 63:2206–2212

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rinta-Kanto JM, Konopko EA, DeBruyn JM, Bourbonniere RA, Boyer GL, Wilhelm SW (2009) Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae 8:665–673

    Article  CAS  Google Scholar 

  • Rueckert A, Cary SC (2009) Use of an armored RNA standard to measure microcystin synthetase E gene expression in toxic Microcystis sp. by reverse transcription QPCR. Limnol Oceanogr Methods 7:509–520

    Article  CAS  Google Scholar 

  • Sevilla E, Martin-Luna B, Vela L, Bes MT, Peleato ML, Fillat MF (2010) Microcystin-LR synthesis as response to nitrogen: transcriptional analysis of the mcyD gene in Microcystis aeruginosa PCC7806. Ecotoxicology 19:1167–1173

    Article  CAS  PubMed  Google Scholar 

  • Sevilla E, Martín-Luna B, González A, Gonzalo-Asensio JA, Peleato ML, Fillat MF (2011) Identification of three novel antisense RNAs in the fur locus from unicellular cyanobacteria. Microbiology 157:3398–3404

    Article  CAS  PubMed  Google Scholar 

  • Sevilla E, Martin-Luna B, Bes MT, Fillat MF, Peleato ML (2012) An active photosynthetic electron transfer chain required for mcyD transcription and microcystin synthesis in Microcystis aeruginosa PCC7806. Ecotoxicology 21:811–819

    Article  CAS  PubMed  Google Scholar 

  • Sivonen K (1990) Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Appl Environ Microbiol 56:2658–2666

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water. WHO, London, pp 41–111

    Google Scholar 

  • Smith V (1983) Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221:669–671

    Article  CAS  PubMed  Google Scholar 

  • Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis, second ed. Fish Res Bd Can Bull 167:1–310

    Google Scholar 

  • Tillett D, Dittmann E, Erhard M, von Döhren H, Börner T, Neilan BA (2000) Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC 7806: an integrated peptide-polyketide synthase system. Chem Biol 7:753–764

    Article  CAS  PubMed  Google Scholar 

  • Tonk L, Visser PM, Christiansen G, Dittmann E, Snelder EOFM, Wiedner C, Mur LR, Huisman J (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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Utkilen H, Gjølme N (1995) Iron-stimulated toxin production in Microcystis aeruginosa. Appl Environ Microbiol 61:797–800

    PubMed Central  CAS  PubMed  Google Scholar 

  • Van der Westhuizen AJ, Eloff JN (1985) Effect of temperature and light on the toxicity and growth of blue–green alga M. aeruginosa (UV-006). Planta 163:55–59

    Article  PubMed  Google Scholar 

  • van Gremberghe I, Vanormelingen P, van der Gucht K, Mancheva A, D’hondt S, De Meester L, Vyverman W (2009) Influence of Daphnia infochemicals on functional traits of Microcystis strains (Cyanobacteria). Hydrobiologia 635:147–155

    Article  CAS  Google Scholar 

  • 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. Microb Ecol 43:443–454

    Article  PubMed  Google Scholar 

  • Walsh K, Jones GJ, Dunstan RH (1997) Effect of irradiance on fatty acid, carotenoid, total protein composition and growth of Microcystis aeruginosa. Phytochemistry 44:817–824

    Article  CAS  Google Scholar 

  • Wang Q, Niu Y, **e P, Chen J, Ma Z, Tao M, Qi M, Wu L, Guo L (2010) Variations of microcystins in Gonghu Bay of Lake Taihu, with potential risk of microcystin contamination to human health. Sci World J 10:1795–1809

    Article  CAS  Google Scholar 

  • Watanabe MF (1996) Production of microcystin. In: Watanabe MF, Harada K, Carmichael WW, Fujiki H (eds) Toxic microcystis. CRC Press Inc., Boca Raton, pp 35–56

    Google Scholar 

  • Welker M, Malek B, Sejnohova L, Dohren H (2006) Detection and identification of oligopeptides in Microcystis (cyanobacteria) colonies: toward an understanding of metabolic diversity. Peptides 27:2090–2103

    Article  CAS  PubMed  Google Scholar 

  • Wicks RJ, Thiel PG (1990) Environmental factors affecting the production of peptide toxins in floating scums of the cyanobacterium Microcystis aeruginosa in a hypertrophic African reservoir. Environ Sci Technol 24:1413–1418

    Article  CAS  Google Scholar 

  • Wood SA, Rueckert A, Hamilton DP, Cary SC, Dietrich DR (2011) Switching toxin production on and off: intermittent microcystin synthesis in a microcystis bloom. Environ Microbiol Rep 3:118–124

    Article  CAS  PubMed  Google Scholar 

  • Wood SA, Dietrich DR, Cary SC, Hamilton DP (2012) Increasing microcystis cell density enhances microcystin synthesis: a mesocosm study. Inland Waters 2:17–22

    Article  CAS  Google Scholar 

  • Zilliges Y, Kehr JC, Meissner S, Ishida K, Mikkat S, Hagemann M, Kaplan A, Börner T, Dittmann E (2011) The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions. PLoS One 6:e17615

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to two anonymous reviewers for their comments and valuable suggestions regarding the manuscript. Pineda-Mendoza was a fellow of Consejo Nacional de Ciencia y Tecnología (CONACYT) (No. 206867) and Programa Institucional de Formación de Investigadores of the IPN (PIFI-IPN). Fernando Martínez-Jerónimo is a fellow of the Sistema de Estímulo al Desempeño de los Investigadores (EDI) and the Comisión de Operación y Fomento de Actividades Académicas (COFAA) of the Instituto Politécnico Nacional.

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  1. Laboratorio de Hidrobiología Experimental, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prol. Carpio esq. Plan de Ayala s/n, Col. Sto. Tomás, Mexico, DF, 11340, Mexico

    Rosa María Pineda-Mendoza & Fernando Martínez-Jerónimo

  2. Laboratorio de Variación Biológica y Evolución, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prol. Carpio esq. Plan de Ayala s/n, Col. Sto. Tomás, Mexico, DF, 11340, Mexico

    Rosa María Pineda-Mendoza & Gerardo Zúñiga

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  1. Rosa María Pineda-Mendoza
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Correspondence to Fernando Martínez-Jerónimo.

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Pineda-Mendoza, R.M., Zúñiga, G. & Martínez-Jerónimo, F. Microcystin production in Microcystis aeruginosa: effect of type of strain, environmental factors, nutrient concentrations, and N:P ratio on mcyA gene expression. Aquat Ecol 50, 103–119 (2016). https://doi.org/10.1007/s10452-015-9559-7

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