Journal of Korean Society on Water Environment (한국물환경학회지)

Korean Society on Water Environment (한국물환경학회)
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Response of Growth and Toxigenicity to Varying Temperature and Nutrient Conditions in Aphanizomenon flos-aquae (Cyanophyceae)

환경조건에 따른 Aphanizomenon flos-aquae (Cyanophyceae) 균주의 성장 반응 및 독소 생성

  • Ryu, Hui-Seong (Yeongsan River Environment Research Center, National Institute of Environmental Research) ;
  • Shin, Ra-Young (Department of Biology Education, Daegu University) ;
  • Lee, Jung-Ho (Department of Biology Education, Daegu University)
  • 류희성 (국립환경과학원 영산강물환경연구소) ;
  • 신라영 (대구대학교 생물교육전공) ;
  • 이정호 (대구대학교 생물교육전공)
  • Received : 2017.04.05
  • Accepted : 2017.07.28
  • Published : 2017.09.30
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Abstract

The purpose of this study is to investigate growth response and toxigenicity under various temperature and nutritional conditions, in order to understand the physioecological characteristics of Aphanizomenon flos-aquae, which is a bloom-forming cyanobacterium in the Nakdong River. The strain was inoculated into media under combinations of four temperatures (4, 12, 21, $30^{\circ}C$) and three nutrients (modified CB medium, P-depleted CB medium, N-depleted CB medium) for 28 days. The algae-inhibition tests were performed to assess the potential allelopathic effects of the strains' filtrates on the growth of four algae strains (Microcystis aeruginosa, Aulacoseria ambigua f. spiralis, Aphanizomenon flos-aquae, Scenedesmus obliquus). Toxin production of a strain was measured by Enzyme-Linked ImmunoSolbent Assay (ELISA). The optimal growth temperature (Topt) of strains was $19.9^{\circ}C$ ($18.3-21.2^{\circ}C$), and the temperature range for growth was from $-0.3^{\circ}C$ to $34.3^{\circ}C$. Specific growth rate (${\mu}$) in modified CB medium varied from 0.10 to $0.16day^{-1}$, and the maximum growth rate (${\mu}_{max}$) was $0.17day^{-1}$. Although growth curves under N-existed and N-depleted conditions were almost the same, growth under N-depleted condition was relatively slowed (${\mu}=0.09$ to $0.14day^{-1}$), with a decreased maximum cell density. However, growth under the P-depleted condition was restricted for all temperatures, Two stains of Aphanizomenon flos-aquae were confirmed as not producing toxins, because saxitoxin and cylindrospermopsin were not detected by ELISA. The exudates or filtrates from the Aphanizomenon flos-aquae (DGUC003) resulted in significant inhibition of algal growth on the Aulacoseira ambigua f. spiralis (DGUD001) and Aphanizomenon flos-aquae (DGUC001) (p < 0.01).

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References

  1. Ballot, A., Fastner, J., Lentz, M., and Wiedner, C. (2010). First Report of Anatoxin-a-Producing Canobacterium Aphanizomenon issatschenkoi in Northeastern German, Toxicon, 56(6), 964-971. https://doi.org/10.1016/j.toxicon.2010.06.021
  2. Ballot, A., Fastner, J., and Wiedner, C. (2010). Paralytic Shellfish Poisoning Toxin-Producing Cyanobacterium Aphanizomenon gracile in Northest Germany, Applied and Environmental Microbiology, 76(4), 1173-1180. https://doi.org/10.1128/AEM.02285-09
  3. Beakes, G., Canter, H. M., and Jaworski, G. H. M. (1988). Zoospores. Ultrastructure of Zygorhizidium affluens Canter and Z. planktonicum Canter, Two Chytrids Parasitizing the Diatom Asterionella formosa Hassall, Canadian Journal of Botany, 66, 1054-1067. https://doi.org/10.1139/b88-151
  4. Berry, J. P., Gantar, M., Perez, M. H., Berry, G., and Noriega, F. G. 2008). Cyanobacterial Toxins as Allelochemicals with Potential Applications as Algaecides, Herbicides and Insecticides, Marine Drugs, 6, 117-146. https://doi.org/10.3390/md6020117
  5. Blahova, L., Oravec, M., Marsalek, B., Sejnohova, L., Simek, Z., and Blaha, L. (2009). The First Occurrence of the Cyanobacterial Alkaloid Toxin Cylindrospermopsin in the Czech Republic as Determined by Immunochemical and LC/MS methods, Toxicon, 53, 519-524. https://doi.org/10.1016/j.toxicon.2009.01.014
  6. Casero, M. C., Ballot, A., Agha, R., Quesada, A., and Cires, S. (2014). Characterization of Saxitoxin Production and Release and Phylogeny of sxt Genes in Paralytic Shellfish Poidoning Toxin-Producion Aphanizomenon gracile, Harmful Algae, 37, 28-37. https://doi.org/10.1016/j.hal.2014.05.006
  7. Chonudomkul, D., Yongmanitchai, W., Theeragool, G., Kawachi, M., Kasai, F., Kaya, K., and Watanabe, M. M. (2004). Morphology, Genetic Diversity, Temperature Tolerance and Toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) Strains from Thailand and Japan, FEMS Microbiology Ecology, 48, 345-355. https://doi.org/10.1016/j.femsec.2004.02.014
  8. Cires, S. and Ballot, A. (2016). A Review of the Phylogeny, Ecology and Toxin Production of Bloom-Forming Aphanizomenon spp. and Related Species within the Nostocales (Cyanobacteria), Harmful Algae, 52, 21-43.
  9. Cires, S., Wormer, L., Ballot, A., Agha, R., Wiedner, C., Velazquez, D., Casero, M. C., and Quesada, A. (2014). Phylogeography of Cylindrospermopsin and Paralytic Shellfish Toxin-Producing Nostocales Cyanobacteria from Mediterranean Europe (Spain), Applied and Environmental Microbiology, 80, 1359-1370. https://doi.org/10.1128/AEM.03002-13
  10. de Figueiredo, D. R., Azeiteiro, U. M., Gonçalves, F., and Pereira, M. J. (2004) Aphanizomenon flos-aquae Grown under Different Nutrient Concentrations and the Effects of its Exudates on Growth of Two Green Algae, Fresenius Environmental Bulletin, 13, 657-66.
  11. de Figueiredo, D. R., Goncalves, A. M. M., Castro, B. B., Gonçalves, F., Pereira, M., and Correia, A. (2011). Differential Inter- and Intra-specific Responses of Aphanizomenon Strains to Nutrient Limitation and Algal Growth Inhibition, Journal of Plankton Research, 33, 1606-1616. https://doi.org/10.1093/plankt/fbr058
  12. Dias, E., Pereira, P., and Franca, S. (2002). Production of Paralytic Shellfish Toxins by Aphanizomenon sp. LMECYA 31 (Cyanobacteria). Journal of Phycology, 38(4), 705-712. https://doi.org/10.1046/j.1529-8817.2002.01146.x
  13. Goncavalves, A. M., de Figueirede, D. R., and Pereira, M. J. (2005). A Low-cost Methology for Algal Growth Inhibition Tests using Three Freshwater Green Algae, Fresenius Environmental Bulletin, 14, 1192-1195.
  14. Holland, A. and Kinnear, S. (2013). Interpreting the Possible Ecological Role(s) of Cyanotoxins: Compounds for Competitive Advantage and/or Physiological Aide?, Marine Drugs, 11, 2239-2258. https://doi.org/10.3390/md11072239
  15. Johnk, K. D., Huisman, J., Sharples, J., Sommeijer, B., Visser P. M., and Stroom, J. M. (2008). Summer Heatwaves Promote Blooms of Harmful Cyanobacteria, Global Change Biology, 14, 495-512. https://doi.org/10.1111/j.1365-2486.2007.01510.x
  16. Leao, P. N., Pereira, A. R., Liu, W. T., Ng, J., Pevzner P. A., Dorrestein, P. C., Konig, G. M., Vasconcelos, V. M. and Gerwick, W. H. (2010). Synergistic Allelochemicals from a Freshwater Cyanobacterium, Proceedings of the National Academy of Sciences, 107, 11183-11188.
  17. Leao, P. N., Vasconcelos, M. T., and Vasconcelos, V. M. (2009). Allelopathy in Freshwater Cyanobacteria, Critical Reviews in Microbiology, 35, 271-282. https://doi.org/10.3109/10408410902823705
  18. Ma, H., Wu, Y., Gan, N., Zheng, L., Li, T., and Song, L. (2015). Growth Inhibitory Effect of Microcystis on Aphanizomenon flos-aquae Isolated from Cyanobacteria Bloom in Lake Dianchi, China, Hamful Algae, 42, 43-51. https://doi.org/10.1016/j.hal.2014.12.009
  19. Mehnert, G., Leunert, F., Cires, S., Jöhnk, K. D., Rucker, J., Nixdorf, B., and Wiedner, C. (2010). Competitiveness of Invasive and Native Cyanobacteria from Temperate Freshwaters under Varios Light and Temperature Conditions, Journal of Plankton Research, 32, 1009-1021. https://doi.org/10.1093/plankt/fbq033
  20. Moustafa, A., Loram, J. E., Hackett, J. D., Anderson, D. M., Plumley, F. G., and Bhattacharya, D. (2009). Origin of Saxitoxin Biosynthetic Genes in Cyanobacteria, PLoS ONE 4, e5758. https://doi.org/10.1371/journal.pone.0005758
  21. Murakami, N., Yamada, N., and Sakakibara, J. (1990). An Autolytic Substance in a Freshwater Cyanobacterium Phormidium tenue, Chemical and Pharmaceutical Bulletin, 38, 812-814. https://doi.org/10.1248/cpb.38.812
  22. Murphy, T., Lean, D., and Nalewajko, C. (1976). Blue-green Algae: Their Excretion of Iron-selective Chelators Enables Them to Dominate Other Algae, Science, 192, 900-902. https://doi.org/10.1126/science.818707
  23. Nelson, N. P. B. (1903). Observations upon Some Algae which Cause "Water bloom.", Minnesota Botanical Studies, 3, 51-56.
  24. Nakdong River Environment Research Center (NRERC). (2015). Aquatic Ecosystem Monitoring in Weir of the Nakdong River, Nakdong River Environment Research Center, 378.
  25. Orr, P. T. and Jones, G. J. (1998). Relationship between Microcystin Production and Cell Division Rates in Nitrogen-limited Microcystis aeruginosa cultures, Limnology and Oceanography, 43, 1604-1614. https://doi.org/10.4319/lo.1998.43.7.1604
  26. Park, H. K., Shin, R. Y., Lee, H. J., Lee, K. L., and Cheon, S. U. (2015). Spatio-temporal Characteristics of Cyanobacterial Communities in the Middle-downstream of Nakdong River and Lake Dukdong, Journal of korean Society on Water Environment, 31(3), 286-294. [Korean Leterature] https://doi.org/10.15681/KSWE.2015.31.3.286
  27. Pierangelini, M., Sinha, R., Willis, A., Burford, M. A., Orr, P. T., Beardall, J., and Neilan, B. A. (2015). Constitutive Cylindrospermopsin Pool Size in Cylindrospermopsis raciborskii under Different light and $CO_2$ Partial Pressure Conditions, Applied and Environmental Microbiology, 81, 3069-3076. https://doi.org/10.1128/AEM.03556-14
  28. Pollingher, U., Hadas, O., Yacobi, Y., Zohary, T., and Berman, T. (1998). Aphanizomenon ovalisporum (Forti) in Lake Kinneret, Israel, Journal of Plankton Research, 20, 1321-1339. https://doi.org/10.1093/plankt/20.7.1321
  29. PreBel, K., Wessel, G., Fastner, J., and Chorus, I. (2009). Response of Cylindrospermopsin Production and Release in Aphanizomenon flos-aquae(Cyanobacteria) to Varying Light and Temperature Conditions, Harmful Algae, 8, 645-650. https://doi.org/10.1016/j.hal.2008.10.009
  30. Preussel, K., Chorus, I., and Fastner, J. (2014). Nitrogen Limitation Promotes Accumulation and Suppresses Release of Cylindrospermopsins in Cells of Aphanizomenon sp., Toxins, 6 (10), 2932-2947. https://doi.org/10.3390/toxins6102932
  31. Rapala, J. and Sivonen, K. (1998). Assessment of Environmental Conditions that Favor Fepatotoxic and Neurotoxin Anabaena spp. Stains Cultured under Light Limitation at Different Temperatures, Microbial Ecology, 36, 181-192. https://doi.org/10.1007/s002489900105
  32. Rucker, J., Stuken, A., Nixdorf, B., Fastner, J., Chorus, I., and Wiedner, C. (2007). Concentrations of Particulate and Dissolved Cylindrospermopsin in 21 Aphanizomenon-dominated Temperate Lakes, Toxicon, 50, 800-809. https://doi.org/10.1016/j.toxicon.2007.06.019
  33. Ryu, H. S., Park, H. K., Lee, H. J., Shin, R. Y., and Cheon, S. U. (2016). Occurrence and Succession Pattern of Cyanobacteria in the Upper Region of the Nakdong River : Factors Influencing Aphanizomenon Bloom, Journal of Korean Society on Water Environment, 32(1), 52-59. [Korean Literature] https://doi.org/10.15681/KSWE.2016.32.1.52
  34. Ryu, H. S., An, S. M., Lim, C. K., Shin, R. Y., Park, J. G., and Lee, J. H. (2017). Analysis of Potential Toxigenicity and Phylogeny using Target Genes in Aphanizomenon flos-aquae (Cyanophyceae) Strains Isolated from the Nakdong River. Korean Journal of Ecology and Environment, 50(1), 137-147. [Korean Leterature] https://doi.org/10.11614/KSL.2017.50.1.137
  35. Shirai, M., Matumaru, K., Ohotake, A., Takamura, Y., Aida, T., and Nakano, M. (1989). Development of a Solid Medium for Growth and Isolation of Axenic Microcystis Strains (Cyanobacteria), Applied and Envieonmental Microbiology, 55(10), 2569-2571.
  36. Stanier, R.Y., Kunisawa, R., Mandel, M., and Cohen-Bazire, G. (1971). Purification and Properties of Unicellular Blue-green Algae (Order Chroococcales), Bacteriological Reviews, 35, 171-205.
  37. Stuken, A. and Jakobsen, K. S. (2010). The Cylindrospermopsin Gene Cluster of Aphanizomenon sp. strain 10E6: Organization and Recombination, Microbiology, 156, 2438-2451. https://doi.org/10.1099/mic.0.036988-0
  38. Suikkanen, S., Fistarol, G. O., and Granéli, E. (2005). Effects of Cyanobacterial Allelochemicals on a Natural Plankton Community, Marine Ecology Progress Series, 287, 1-9. https://doi.org/10.3354/meps287001
  39. Uveges, V., Tapolczai, K., Krienitz, L., and Padisak, J. (2012). Photosynthetic Characteristics and Physiological Plasticity of an Aphanizomenon flos-aquae (Cyanobacteria, Nostocaceae) Winter Bloom in a Deep Oligo-mesotrophic Lake (Lake Stechlin, Germany), Hydrobiologia, 698, 263-272. https://doi.org/10.1007/s10750-012-1103-3
  40. Yamamoto, T. (2009). Environmental Factors that Determine the Occurrence and Seasonal Dynamics of Aphanizomenon flos-aquae, Journal of Limnology, 68(1), 122-132. https://doi.org/10.4081/jlimnol.2009.122
  41. Yang, Z., Geng, L., Wang, W., and Zhang, J. (2012). Combined Effects of Temperature, Light Intensity and Nitrogen Concentration on the Growth and Polysaccaharide Content of Microcystis aeruginosa in Batch Culture, Biochemical Systematics and Ecology, 41, 130-135. https://doi.org/10.1016/j.bse.2011.12.015
  42. Yu, J. J., Lee, H. J., Lee, K. L., Lyu, H. S., Hwang, J. W., Shin, L. Y., and Cheon, S. U. (2014). Relations between Distribution of the Dominant Phytoplankton Species and Water Temperature in the Nakdong River, Korea. Korean Journal of Ecology and Environment, 47(4), 247-257. [Korean Leterature] https://doi.org/10.11614/KSL.2014.47.4.247