Abstract
Cyanobacterial blooms have become a serious global environmental issue due to their potential risk for releasing detrimental secondary metabolites into aquatic ecosystems, posing a great threat to water quality management for public health authorities. Aphanizomenon, a common filamentous cyanobacterial genus belonging to Nostocales, is under particular concern because its several members are able to form harmful blooms. Furthermore, succession of bloom between A. flos-aquae and Microcystis occurs in many natural lakes. To evaluate the competitiveness of A. flos-aquae vs. M. aeruginosa, two sets of experiments at different ratios of biomass at 15 °C and 25 °C were conducted. Results show that at 15 °C, the two species were able to coexist, and A. flos-aquae showed a specific higher growth rate, and its growth was promoted by the presence of M. aeruginosa. At 25 °C, the growth of A. flos-aquae was inhibited by the biomass of M. aeruginosa, and M. aeruginosa suppressed A. flos-aquae in competition. Additionally, the vegetative cell size of A. flos-aquae was significantly influenced by the co-culture with M. aeruginosa, whereas the filament length of A. flos-aquae was not significantly affected. This study confirms that temperature is the dominating factor on the succession of A. flos-aquae and M. aeruginosa of a different biomass.
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Data Availability Statement
All data generated and/or analyzed during this study are available from the corresponding author on reasonable request.
References
Baker K K. 1981. Ecology and taxonomy of five natural populations of the genus Aphanizomenon Morren (Cyanophyceae). Archiv fur Hydrobiologie, 92: 222–251, https://doi.org/10.1046/j.1529-8817.2000.99146.x.
Best J. 2019. Anthropogenic stresses on the world’s big rivers. Nature Geoscience, 12(1): 7–21, https://doi.org/10.1038/s41561-018-0262-x.
Bohannan, B. J. M., B. Kerr, C. M. Jessup, J. B. Hughes & G. Sandvik, 2002. Trade-offs and coexistence in microbial microcosms. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 81: 107–115, https://doi.org/10.1023/a:1020585711378.
Bormans M, Ford P W, Fabbro L. 2005. Spatial and temporal variability in cyanobacterial populations controlled by physical processes. Journal of Plankton Research, 27(1): 61–70, https://doi.org/10.1093/plankt/fbh150.
Brookes J D, Ganf G G. 2001. Variations in the buoyancy response of Microcystis aeruginosa to nitrogen, phosphorus and light. Journal of Plankton Research, 23(12): 1399–1411, https://doi.org/10.1093/plankt/23.12.1399.
Carey C C, Ibelings B W, Hoffmann E P et al. 2012. Ecophysiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Research, 46(5): 1394–1407, https://doi.org/10.1016/j.watres.2011.12.016.
Cirés S, 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, 54: 21–43, https://doi.org/10.1016/j.hal.2015.09.007.
Codd G, Bell S, Kaya K et al. 1999. Cyanobacterial toxins, exposure routes and human health. European Journal of Phycology, 34(4): 405–415, https://doi.org/10.1017/s0967026299002255
Finkel, Z. V., J. Beardall, K. J. Flynn, A. Quigg, T. A. V. Rees & J. A. Raven, 2010. Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research, 32(1):119–137, https://doi.org/10.1093/plankt/fbp098.
Gehringer M M, Wannicke N. 2014. Climate change and regulation of hepatotoxin production in Cyanobacteria. FEMS Microbiology Ecology, 88(1): 1–25, https://doi.org/10.1111/1574-6941.12291
Glibert P M, Anderson D M, Gentien P et al. 2005. The global, complex phenomena of harmful algal blooms. Oceanography, 18(2): 136–147, https://doi.org/10.5670/oceanog.2005.49.
Grover J P. 1989. Influence of cell shape and size on algal competitive ability. Journal of Phycology, 25(2): 402–405, https://doi.org/10.1111/j.1529-8817.1989.tb00138.x.
Guan Y, Zhang M, Yang Z, Shi X, Zhao X. 2020. Intraannual variation and correlations of functional traits in Microcystis and Dolichospermum in Lake Chaohu. Ecological Indicators, 111: 106052, https://doi.org/10.1016/j.ecolind.2019.106052.
Jia N N, Yang Y M, Yu G L et al. 2020. Interspecific competition reveals Raphidiopsis raciborskii as a more successful invader than Microcystis aeruginosa. Harmful Algae, 97: 101858, https://doi.org/10.1016/j.hal.2020.101858.
Jones R I. 1979. Notes on the growth and sporulation of a natural population of Aphanizomenon flos-aquae. Hydrobiologia, 62(1): 55–58, https://doi.org/10.1007/bf00012562.
Khan Z, Wan Omar W M, Merican F M M S, Azizan A A, Foong C P, Convey P, Najimudin N, Smykla J, Alias S A. 2017. Identification and phenotypic plasticity of Pseudanabaena catenata from the Svalbard archipelago. Polish Polar Research, 38(4): 445–458, https://doi.org/10.1515/popore-2017-0022.
Konopka A, Brock T D. 1978. Effect of temperature on blue-green algae (Cyanobacteria) in lake Mendota. Applied and Environmental Microbiology, 36(4): 572–576, https://doi.org/10.1128/aem.36.4.572-576.1978.
Litchman E, Klausmeier C A, Schofield O M, Falkowski P G. 2007. The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecology Letters, 10(12): 1170–1181, https://doi.org/10.1111/j.1461-0248.2007.01117.x.
Litchman, E., 2003. Competition and coexistence of phytoplankton under fluctuating light: experiments with two cyanobacteria. Aquatic Microbial Ecology, 31(3):241–248, https://doi.org/10.3354/ame031241.
Liu X Y, Shi M, Liao Y H et al. 2006a. Feeding characteristics of an amoeba (Lobosea: Naegleria) grazing upon cyanobacteria: food selection, ingestion and digestion progress. Microbial Ecology, 51(3): 315–325, https://doi.org/10.1007/s00248-006-9031-2.
Liu Y M, Chen W, Li D H et al. 2006b. First report of aphantoxins in China—waterblooms of toxigenic Aphanizomenon flos-aquae in Lake Dianchi. Ecotoxicology and Environmental Safety, 65(1): 84–92, https://doi.org/10.1016/j.ecoenv.2005.06.012.
Ma H Y, Wu Y L, Gan N Q et al. 2015. Growth inhibitory effect of Microcystis on Aphanizomenon flos-aquae isolated from cyanobacteria bloom in Lake Dianchi, China. Harmful Algae, 42: 43–51, https://doi.org/10.1016/j.hal.2014.12.009.
McDonald K E, Lehman J T. 2013. Dynamics of Aphanizomenon and Microcystis (cyanobacteria) during experimental manipulation of an urban impoundment. Lake and Reservoir Management, 29(2): 103–115, https://doi.org/10.1080/10402381.2013.800172.
Messineo V, Melchiorre S, Di Corcia A et al. 2010. Seasonal succession of Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum blooms with cylindrospermopsin occurrence in the volcanic Lake Albano, central Italy. Environmental Toxicology, 25(1): 18–27, https://doi.org/10.1002/tox.20469.
Moustaka-Gouni M, Vardaka E, Tryfon E. 2007. Phytoplankton species succession in a shallow Mediterranean lake (L. Kastoria, Greece): steady-state dominance of Limnothrix redekei, Microcystis aeruginosa and Cylindrospermopsis raciborskii. Hydrobiologia, 575(1): 129–140, https://doi.org/10.1007/s10750-006-0360-4.
Mushtaq N, Singh D V, Bhat R A et al. 2020. Freshwater contamination: sources and hazards to aquatic biota. In: Qadri H, Bhat R A, Mehmood M A et al. eds. Fresh Water Pollution Dynamics and Remediation. Springer, Singapore. p.27–50, https://doi.org/10.1007/978-981-13-8277-2_3.
Paerl H W, Otten T G. 2013. Harmful cyanobacterial blooms: causes, consequences, and controls. Microbial Ecology, 65(4): 995–1010, https://doi.org/10.1007/s00248-012-0159-y.
Paerl H W, Otten T G. 2016. Duelling ‘CyanoHABs’: unravelling the environmental drivers controlling dominance and succession among diazotrophic and non-N2-fixing harmful cyanobacteria. Environmental Microbiology, 18(2): 316–324, https://doi.org/10.1111/1462-2920.13035.
Paerl H W, Paul V J. 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Research, 46(5): 1349–1363, https://doi.org/10.1016/j.watres.2011.08.002.
Pearson L, Mihali T, Moffitt M et al. 2010. On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Marine Drugs, 8(5): 1650–1680, https://doi.org/10.3390/md8051650.
Rapala J, Sivonen K, Luukkainen R et al. 1993. Anatoxin-a concentration in Anabaena and Aphanizomenon under different environmental conditions and comparison of growth by toxic and non-toxic Anabaena-strains — a laboratory study. Journal of Applied Phycology, 5(6): 581–591, https://doi.org/10.1007/bf02184637.
Robarts R D, Zohary T. 1987. Temperature effects on photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. New Zealand Journal of Marine and Freshwater Research, 21(3): 391–399, https://doi.org/10.1080/00288330.1987.9516235.
Rzymski P, Poniedzialek B, Karczewski J. 2011. Gastroenteritis and liver carcinogenesis induced by cyanobacterial toxins. Gastroenterologia Polska, 18(4): 159–162.
Sabour B, Loudiki M, Oudra B et al. 2005. Dynamics and toxicity of Anabaena aphanizomenoides (Cyanobacteria) waterblooms in the shallow brackish Oued Mellah Lake (Morocco). Aquatic Ecosystem Health & Management, 8(1): 95–104, https://doi.org/10.1080/14634980590914944.
Shan K, Song L R, Chen W et al. 2019. Analysis of environmental drivers influencing interspecific variations and associations among bloom-forming cyanobacteria in large, shallow eutrophic lakes. Harmful Algae, 84: 84–94, https://doi.org/10.1016/j.hal.2019.02.002.
Shen H, Song L R. 2007. Comparative studies on physiological responses to phosphorus in two phenotypes of bloom-forming Microcystis. Hydrobiologia, 592(1): 475–486, https://doi.org/10.1007/s10750-007-0794-3.
Smayda T J. 2008. Complexity in the eutrophication-harmful algal bloom relationship, with comment on the importance of grazing. Harmful Algae, 8(1): 140–151, https://doi.org/10.1016/j.hal.2008.08.018.
Soares M C S, Luerling M, Huszar V L M. 2013. Growth and temperature-related phenotypic plasticity in the cyanobacterium Cylindrospermopsis raciborskii. Phycological Research, 61(1): 61–67, https://doi.org/10.1111/pre.12001.
Suurnäkki S, Gomez-Saez G V, Rantala-Ylinen A et al. 2015. Identification of geosmin and 2-methylisoborneol in cyanobacteria and molecular detection methods for the producers of these compounds. Water Research, 68: 56–66, https://doi.org/10.1016/j.watres.2014.09.037.
Takamura N, Iwakuma T, Yasuno M. 1987. Uptake of 13C and 15N (ammonium, nitrate and urea) by Microcystis in Lake Kasumigaura. Journal of Plankton Research, 9(1): 151–165, https://doi.org/10.1093/plankt/9.1.151.
Tan X, Gu H H, Ruan Y L et al. 2019. Effects of nitrogen on interspecific competition between two cell-size cyanobacteria: Microcystisaeruginosa and Synechococcus sp. Harmful Algae, 89: 101661, https://doi.org/10.1016/j.hal.2019.101661.
Thomas W H, Gibson C H. 1990. Effects of small-scale turbulence on microalgae. Journal of Applied Phycology, 2(1): 71–77, https://doi.org/10.1007/bf02179771.
Tsujimura S, Ishikawa K, Tsukada H. 2001. Effect of temperature on growth of the cyanobacterium Aphanizomenon flos-aquae in Lake Biwa and Lake Yogo. Phycological Research, 49(4): 275–280, https://doi.org/10.1046/j.1440-1835.2001.00255.x.
Tsukada H, Tsujimura S, Nakahara H. 2006. Seasonal succession of phytoplankton in Lake Yogo over 2 years: effect of artificial manipulation. Limnology, 7(1): 3–14, https://doi.org/10.1007/s10201-005-0159-4.
Üveges V, Tapolczai K, Krienitz L et al. 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(1): 263–272, https://doi.org/10.1007/s10750-012-1103-3.
Violle C, Enquist B J, McGill B J, Jiang L, Albert C H, Hulshof C, Jung V, Messier J. 2012. The return of the variance: intraspecific variability in community ecology. Trends in Ecology & Evolution, 27(4): 244–252, https://doi.org/10.1016/j.tree.2011.11.014.
Wang Z H, Akbar S, Sun Y F et al. 2021. Cyanobacterial dominance and succession: factors, mechanisms, predictions, and managements. Journal of Environmental Management, 297: 113281, https://doi.org/10.1016/j.jenvman.2021.113281.
Wu W J, Li G B, Li D H et al. 2010. Temperature may be the dominating factor on the alternant succession of Aphanizomenon flos-aquae and Microcystis aeruginosa in Dianchi Lake. Fresenius Environmental Bulletin, 19(5): 846–853.
Wu YL, Li L, Zheng L L et al. 2016. Patterns of succession between bloom-forming cyanobacteria Aphanizomenon flos-aquae and Microcystis and related environmental factors in large, shallow Dianchi Lake, China. Hydrobiologia, 765(1): 1–13, https://doi.org/10.1007/s10750-015-2392-0.
Xiao Y, Li Z, Li C et al. 2016. Effect of small-scale turbulence on the physiology and morphology of two bloom-forming cyanobacteria. PLoS One, 11(12): e0168925, https://doi.org/10.1371/journal.pone.0168925.
Yang Z, Kong F X, Shi X L et al. 2006. Morphological response of Microcystis aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia, 563(1): 225–230, https://doi.org/10.1007/s10750-005-0008-9.
Zhu X, Wang J, Lu Y, Chen Q, Yang Z. 2015. Grazer-induced morphological defense in Scenedesmus obliquus is affected by competition against Microcystis aeruginosa. Scientific Reports, 5: 12743, https://doi.org/10.1038/srep12743.
Acknowledgment
We thank the Wuhan Branch, Supercomputing Center, Chinese Academy of Sciences, for providing computing facilities, and all staff from the Analysis and Testing Center at Institute of Hydrobiology, CAS, for technical supports.
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Supported by the National Key Research and Development Program of China (No. 2017YFA0605201), the Major Project of Natural Science Foundation of Zhejiang Province (No. LD21C030001), the National Natural Science Foundation of China (No. 51779247), the Controlling Technology of Cyanobacterial Bloom in the Major Lakes of Wuhan city (No. HBT-16200117-201482), and the Featured Institute Service Project from Institute of Hydrobiology, Chinese Academy of Sciences (No. Y85Z061601)
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Wen, Q., Xiao, P., Li, H. et al. Succession of Aphanizomenon flos-aquae and Microcystis aeruginosa in direct co-culture experiments at different temperatures and biomasses. J. Ocean. Limnol. 40, 1819–1828 (2022). https://doi.org/10.1007/s00343-022-2041-1
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DOI: https://doi.org/10.1007/s00343-022-2041-1