Advertisement

Chinese Journal of Oceanology and Limnology

, Volume 34, Issue 6, pp 1173–1182 | Cite as

The combined effects of Dolichospermum flos-aquae, light, and temperature on microcystin production by Microcystis aeruginosa

  • Ruoqi Chen (陈若旗)
  • Fangfang Li (李方方)
  • Jiadong Liu (刘佳栋)
  • Hongye Zheng (郑红叶)
  • Fei Shen (沈飞)
  • Yarong Xue (薛雅蓉)Email author
  • Changhong Liu (刘常宏)Email author
Biology

Abstract

The effects of light, temperature, and coculture on the intracellular microcystin-LR (MC-LR) quota of Microcystis aeruginosa were evaluated based on coculture experiments with nontoxic Dolichospermum (Anabaena) flos-aquae. The MC-LR quota and transcription of mcyB and mcyD genes encoding MC synthetases in M. aeruginosa were evaluated on the basis of cell counts, high-performance liquid chromatography, and reverse-transcription quantitative real-time PCR. The MC-LR quotas of M. aeruginosa in coculture with a 1/1 ratio of inoculum of the two species were significantly lower relative to monocultures 6-d after inoculation. Decreased MC-LR quotas under coculture conditions were enhanced by increasing the D. flos-aquae to M. aeruginosa ratio in the inoculum and by environmental factors, such as temperature and light intensity. Moreover, the transcriptional concentrations of mcyB and mcyD genes in M. aeruginosa were significantly inhibited by D. flos-aquae competition in coculture (P <0.01), lowered to 20% of initial concentrations within 8 days. These data suggested that coculture eff ects by D. flos-aquae not only reduced M. aeruginosa’s intracellular MC-LR quota via inhibition of genes encoding MC synthetases, but also that this eff ect was regulated by environmental factors, including temperature and light intensities.

Keywords

coculture effects microcystin M. aeruginosa D. flos-aquae biosynthesis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bittencourt-Oliveira M do C, Kujbida P, Cardozo K H M, Carvalho V M, Moura A do N, Colepicolo P, Pinto E. 2005. A novel rhythm of microcystin biosynthesis is described in the cyanobacterium Microcystis panniformis Komárek et al. Biochem. Biophys. Res. Commun., 326(3): 687–694.CrossRefGoogle Scholar
  2. Briand E, Bormans M, Quiblier C, Salencon M J, Humbert J F. 2012. Evidence of the cost of the production of microcystins by Microcystis aeruginosa under differing light and nitrate environmental conditions. PLoS One. 7 (1): e29981.CrossRefGoogle Scholar
  3. Briand E, Yéprémian C, Humbert J F, Quiblier C. 2008. Competition between microcystin-and non-microcystinproducing Planktothrix agardhii (cyanobacteria) strains under different environmental conditions. Environ. Microbiol., 10(12): 3337–3348.CrossRefGoogle Scholar
  4. Bustin S A. 2000. Absolute quantification of mRNA using realtime reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol., 25(2): 169–193.CrossRefGoogle Scholar
  5. Butler N, Carlisle J C, Linville R, Washburn B. 2009. Microcystins: a Brief Overview of Their Toxicity and Effects, with Special Reference to Fish, Wildlife, and Livestock. Ecotoxicology Program Integrated Risk Assessment Branch Office of Environmental Health Hazard Assessment California Environmental Protection Agency, Sacramento, CA, USA, p.1–17.Google Scholar
  6. Carmichael W W. 1994. The toxins of cyanobacteria. Sci. Am., 2 70(1): 78–86.CrossRefGoogle Scholar
  7. Chen J, Hu L B, Zhou W, Yan S H, Yang J D, Xue Y F, Shi Z Q. 2010. Degradation of microcystin-LR and RR by a Stenotrophomonas sp. strain EMS isolated from Lake Taihu, China. Int. J. Mol. Sci., 11(3): 896–911.Google Scholar
  8. Chen Y W, Qin B Q, Teubner K, Dokulil M T. 2003. Long-term dynamics of phytoplankton assemblages: microcystis -domination in Lake Taihu, a large shallow lake in China. J. Plankton Res., 25(4): 445–453.CrossRefGoogle Scholar
  9. Dawson R M. 1998. The toxicology of microcystins. Toxicon. 36(7): 953–962.CrossRefGoogle Scholar
  10. Fahnenstiel G L, Millie D F, Dyble J, Litaker R W, Tester P A, McCormick M J, Rediske R, Klarer D. 2008. Microcystin concentrations and cell quotas in Saginaw Bay, Lake Huron. Aquatic Ecosystem Health & Management. 11(2): 190–195.CrossRefGoogle Scholar
  11. Gan N Q, Xiao Y, Zhu L, Wu Z X, Liu J, Hu C L, Song L R. 2012. The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environ. Microbiol., 14(3): 730–742.CrossRefGoogle Scholar
  12. Ginn H P, Pearson L A, Neilan B A. 2010. NtcA from Microcystis aeruginosa PCC 7806 is autoregulatory and binds to the microcystin promoter. Appl. Environ. Microbiol., 76(13): 4362–4368.CrossRefGoogle Scholar
  13. Grosse Y, Baan R, Straif K, Secretan B, EI Ghissassi F, Cogliano V. 2006. Carcinogenicity of nitrate, nitrite, and cyanobacterial peptide toxins. Lancet Oncol., 7(8): 628–629.CrossRefGoogle Scholar
  14. Health Canada. 2002. Guidelines for Canadian drinking water quality: supporting documentation. Cyanobacterial Toxins-Microcystin-LR.Google Scholar
  15. Horst G P, Sarnelle O, White J D, Hamilton S K, Kaul R B, Bressie J D. 2014. Nitrogen availability increases the toxin quota of a harmful cyanobacterium, Microcystis aeruginosa. Water Res., 54: 188–198.CrossRefGoogle Scholar
  16. Hu X, Liu Y G, Zeng G M, Hu X J, Wang Y Q, Zeng X X. 2014. Effects of limonene stress on the growth of and microcystin release by the fresh water cyanobacterium Microcystis aeruginosa FACHB-905. Ecotoxicol. Environ. Saf., 105: 121–127.CrossRefGoogle Scholar
  17. Jang M H, Ha K, Joo G J, Takamura N. 2003. Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshwater Biology. 48(9): 1540–1550.CrossRefGoogle Scholar
  18. Kaebernick M, Neilan B A, Börner T, Dittmann E. 2000. Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl. Environ. Microbiol., 66(8): 3387–3392.CrossRefGoogle Scholar
  19. Karadžic V, Subakov-Simic G, Krizmanic J, Natic D. 2010. Phytoplankton and eutrophication development in the water supply reservoirs Garaši and Bukulja (Serbia). Desalination. 255(1-3): 91–96.CrossRefGoogle Scholar
  20. Krishnamurthy T, Carmichael W W, Sarver E W. 1986. Toxic peptides from freshwater cyanobacteria (blue-green algae). I. Isolation, purification and characterization of peptides from Microcystis aeruginosa and Anabaena flos-aquae. Toxicon. 24(9): 865–873.Google Scholar
  21. Kuniyoshi T M, Sevilla E, Bes M T, Fillat M F, Peleato M L. 2013. Phosphate deficiency (N/P 40: 1) induces mcyD transcription and microcystin synthesis in Microcystis aeruginosa PCC7806. Plant Physiol. Biochem., 65: 120–124.CrossRefGoogle Scholar
  22. Kurmayer R. 2011. The toxic cyanobacterium Nostoc sp. strain 152 produces highest amounts of microcystin and nostophycin under stress conditions. J. Phycol., 47(1): 200–207.Google Scholar
  23. Laub J, Henriksen P, Brittain S M et al. 2002. [ADMAdda 5 ]-microcystins in Planktothrix agardhi i strain PH-123 (cyanobacteria)-importance for monitoring of microcystins in the environment. Environ. Toxicol., 17(4): 351–357.CrossRefGoogle Scholar
  24. LeBlanc S, Pick F R, Aranda-Rondriguze R. 2005. Allelopathic effects of the toxic cyanobacterium Microcystis aeruginosa on duckweed, Lemma gibba L. Environ. Toxicol., 20(1): 67–73.CrossRefGoogle Scholar
  25. Lehman P W, Boyer G, Satchwell M, 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(1): 187–204.CrossRefGoogle Scholar
  26. Li Y X, Li D H. 2012. Competition between toxic Microcystics aeruginosa and nontoxic Microcystis wesenbergii with Anabaena PCC7120. J. Appl. Phycol., 24(1): 69–78.CrossRefGoogle Scholar
  27. Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-C T method. Methods. 25(4): 402–408.CrossRefGoogle Scholar
  28. Oh H M, Lee S J, Jang M H, Yoon B D. 2000. Microcystin production by Microcystis aeruginosa in a phosphorouslimited chemostat. Appl. Environ. Microbiol., 66(1): 176–179.CrossRefGoogle Scholar
  29. Orr P Y, Jones G J. 1998. Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Lancet Oceanogr., 43(7): 1604–1614.Google Scholar
  30. Papadimitriou T, Armeni E, Stalikas C D, Kagalou I, Leonardos I D. 2012. Detection of microcystins in Pamvotis lake water and assessment of cyanobacterial bloom toxicity. Environ mental Monit oring A nd Assess ment. 184(5): 3043–3052.CrossRefGoogle Scholar
  31. Pineda-Mendoza R M, Zúñiga G, Martínez-Jerónimo F. 2014. Infochemicals released by Daphnia magna fed on Microcystis aeruginosa affect mcyA gene expression. Toxicon. 80: 78–86.CrossRefGoogle Scholar
  32. Rantala A, Rajaniemi-Wacklin P, Lyra C, Lepistö L, Rintala J, Mankiewicz-Boczek J, Sivonen K. 2006. Detection of microcystin-producing cyanobacteria in Finnish Lakes with genus-specific microcystin synthetase gene E (mcyE) PCR and associations with environmental factors. Appl. Environ. Microbiol., 72(9): 6101–6110.CrossRefGoogle Scholar
  33. Rinta-Kanto J M, Konopko E A, De Bruyn J M, Bourbonniere R A, Boyer G L, Wilhelm S W. 2009. Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae. 8(5): 665–673.CrossRefGoogle Scholar
  34. Ríos V, Moreno I, Prieto A I, Soria-Díaz M E, Frías J E, Cameán A M. 2014. Comparison of Microcystis aeruginosa (PCC7820 and PCC7806) growth and intracellular microcystins content determined by liquid chromatography-mass spectrometry, enzyme-linked immunosorbent assay anti-Adda and phosphatase bioassay. J. Water Health. 12(1): 69–80.CrossRefGoogle Scholar
  35. Rouhiainen L, Vakkilainen T, Siemer B L, Buikema W, Haselkorn R, Sivonen K. 2004. Genes coding for hepatotoxic heptapeptides (microcystins) in the cyanobacterium Anabaena strain 90. Appl. Environ. Microbiol., 70(2): 686–692.CrossRefGoogle Scholar
  36. Rzymski P, Poniedzialek B, Kokocinski M, Jurczak T, Lipski D, Wiktorowicz K. 2014. Interspecific allelopathy in cyanobacteria: Cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa. Harmful Algae. 35: 1–8.CrossRefGoogle Scholar
  37. Saker M L, Welker M, Vasconcelos V M. 2007. Multiplex PCR for the detection of toxigenic cyanobacteria in dietary supplements produced for human consumption. Appl. Microbiol. Biot echnol., 73(5): 1136–1142.CrossRefGoogle Scholar
  38. Schatz D, Keren Y, Hadas O, Carmeli S, Sukenik A, Kaplan A. 2005. Ecological implications of the emergence of nontoxic subcultures from toxic Microcystis strains. Environ. Microbiol., 7(6): 798–805.CrossRefGoogle Scholar
  39. Schatz D, Keren Y, Vardi A, Sukenik A, Carmeli S, Berner T, Dittmann E, Kaplan A. 2007. Towards clarification of the biological role of microcystins, a family of cyanobacterial toxins. Environ. Microbiol., 9(4): 965–970.CrossRefGoogle Scholar
  40. Schmidt J R, Wilhelm S W, Boyer G L. 2014. The fate of Microcystins in the environment and challenges for monitoring. Toxins. 6(12): 3354–3387.CrossRefGoogle Scholar
  41. Scott L L, Downing S, Phelan R R, Downing T G. 2014. Environmental modulation of microcystin and ß-N-methylamino-L-alanine as a function of nitrogen availability. Toxicon. 87: 1–5.CrossRefGoogle Scholar
  42. Sevilla E, Martin-Luna B, Vela L, Bes M T, Fillat M F, Peleato M L. 2008. Iron availability affects mcyD expression and microcystin-LR synthesis in Microcystis aeruginosa PCC7806. Environ. Microbiol., 10(10): 2476–2483.CrossRefGoogle Scholar
  43. Sevilla E, Martin-Luna B, Vela L, Bes M T, Peleato M L, Fillat M F. 2010. Microcystin-LR synthesis as response to nitrogen: transcriptional analysis of the mcyD gene in Microcystis aeruginosa PCC7806. Ecotoxicology. 19(7): 1167–1173.CrossRefGoogle Scholar
  44. Song R F, Wang G X, Xu Y, Shao J H, Wang Z J, Liu Y, Li R H. 2011. Transcriptional response of microcystin biosynthesis gene cluster of Microcystis aeruginosa PCC7806 under Daphnia stress using real-time RT-PCR technique. J. Lake Sci., 23(1): 150–154.CrossRefGoogle Scholar
  45. Te S H, Gin K Y H. 2011. The dynamics of cyanobacteria and microcystin production in a tropical reservoir of Singapore. Harmful Alage. 10(3): 319–329.CrossRefGoogle Scholar
  46. Tillett D, Dittmann E, Erhard M, von Döhren H, Börner T, Neilan B A. 2000. Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem. Biol., 7(10): 753–764.CrossRefGoogle Scholar
  47. Wan L, Zhu W, Zhao L F. 2007. Effect of nitrogen and phosphorus on growth and competition of M. aeruginosa and S. quadricauda. Environ. Sci., 28(6): 1230–1235. (in Chinese with English abstract)Google Scholar
  48. Wang J, Zhao F, Chen B H, Li Y N, Na P, Zhuo J. 2013. Small water clusters stimulate microcystin biosynthesis in cyanobacterial Microcystis aeruginosa. J. Appl. Phycol., 25(1): 329–336.CrossRefGoogle Scholar
  49. WHO. 2003. Cyanobacterial Toxins: Microcystin-LR in Drinking-Water. In: Background Document for Preparation of WHO Guidelines for Drinking-water Quality. World Health Organization (WHO/SDS/WSH/03. 04/57), Geneva.Google Scholar
  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 PC. 7806. Appl. Environ. Microbiol., 69(3): 1475–1481.CrossRefGoogle Scholar
  51. Wood S A, Rueckert A, Hamilton D P, Cary S C, Dietrich D R. 2011. Swiching toxin production on and off: intermittent microcystin synthesis in a Microcystis bloom. Environ. Microbiol. Rep., 3(1): 118–124.CrossRefGoogle Scholar
  52. Wu X D, Kong F X. 2008. The determination of in situ growth rates of the bloomed Microcystis in Meiliang Bay, Lake Taihu. China Environ. Sci., 28(6): 552–555. (in Chinese with English abstract)Google Scholar
  53. Yen H K, Lin T F, Tseng I C. 2012. Detection and quantification of major toxigenic Microcystis genotypes in Moo-Tan reservoir and associated water treatment plant. J. Environ. Monitor., 14(2): 687–696.CrossRefGoogle Scholar
  54. Zhai C M, Song S, Zou S H, Liu C H, Xue Y R. 2013. The mechanism of competition between two bloom-forming Microcystis species. Freshwater Biology. 58(9): 1831–1839.CrossRefGoogle Scholar
  55. Zhang P, Zhai C M, Chen R Q, Liu C H, Xue Y R, Jiang J H. 2012. The dynamics of the water bloom-forming Microcystis aeruginosa and its relationship with biotic and abiotic factors in Lake Taihu, China. Ecol. Eng., 47: 274–277.CrossRefGoogle Scholar
  56. Zhang P, Zhai C M, Wang X X, Liu C H, Jiang J H, Xue Y R. 2013. Growth competition between Microcystis aeruginosa and Quadrigula chodatii under controlled conditions. J. Appl. Phycol., 25(2): 555–565.CrossRefGoogle Scholar
  57. Zhang T, Song L R. 2006. Allelopathic effect between Microcystis aeruginosa and three filamentous cyanobacteria. J. Lake Sci., 18(2): 150–156. (in Chinese with English abstract)CrossRefGoogle Scholar
  58. Zhang X W, Fu J, Song S, Zhang P, Yang X H, Zhang L R, Luo Y, Liu C H, Zhu H L. 2014. Interspecific competition between Microcystis aeruginosa and Anabaena flos -aquae from Taihu Lake, China. Zeitschrift für Naturforschung C. 69(1-2): 53–60.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ruoqi Chen (陈若旗)
    • 1
  • Fangfang Li (李方方)
    • 1
  • Jiadong Liu (刘佳栋)
    • 1
  • Hongye Zheng (郑红叶)
    • 1
  • Fei Shen (沈飞)
    • 1
  • Yarong Xue (薛雅蓉)
    • 1
    Email author
  • Changhong Liu (刘常宏)
    • 1
    Email author
  1. 1.State Key Laboratory of Pharmaceutical Biotechnology, School of Life ScienceNanjing UniversityNanjingChina

Personalised recommendations