Abstract
Most mixed culture studies on the allelopathic interactions between toxic and nontoxic cyanobacteria with phytoplankton species rarely investigate the role of microcystins (MC) production and regulation in the course of the studies. This study investigated the interactions between intact cells of toxic (Microcystis aeruginosa (Kützing) Kützing) and nontoxic (Microcystis panniformis Komárek et al.) cyanobacteria with those of green algae (Monoraphidium convolutum (Corda) Komárková-Legnerová and Scenedesmus acuminatus (Largerheim) Chodat) as well as the effects of their respective crude extracts (5 and 10 μg.L−1) on their growth under controlled conditions. M. aeruginosa and M. panniformis were able to significantly (p < 0.05) inhibit the growth of the green algae with M. convolutum being the most affected. The green alga S. acuminatus in return was able to inhibit the growth of the both cyanobacteria. In response to the presence of a competing species in the growth medium, M. aeruginosa significantly increased its MC production per cell with the progression of the experiment, having the highest concentration at the end of the experiment. On the other hand, the extracts of the cyanobacteria had no significant inhibitory effect on the green algal strains investigated, while those of the green algae also had significant inhibitory effect on the growth of M. aeruginosa. In conclusion, both cyanobacterial and green algal strains investigated were negatively affected by the presence of competing species. M. aeruginosa responded to the presence of green algae by increasing its MC production. The green algal strains significantly inhibited the growth of M. aeruginosa.
Similar content being viewed by others
References
Babica P, Bláha L, Marsalek B (2006) Exploring the natural role of microcystins—a review of effects on photoautotrophic organisms. J Phycol 42:9–20
Bártova K, Hilscherova K, Babica P, Marsálek B, Bláha L (2011) Effects of microcystin and complex cyanobacterial samples on the growth and oxidative stress parameters in green alga Pseudokirchneriella subcapitata and comparison with the model oxidative stressor-herbicide paraquat. Environ Toxicol 26:641–648
Bar-Yosef Y, Sukenik A, Hadas O, Viner-Mozzini Y, Kaplan A (2010) Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons. Curr Biol 20:1557–1561
B-Beres V, Grigorszky I, Vasas G, Borics G, Varbiro G, Nagy SA, Borbely G, Bacsi I (2012) The effects of Microcystis aeruginosa (cyanobacterium) on Cryptomonas ovata (Cryptophyta) in laboratory cultures: why these organisms do not coexist in steady-state assemblages? Hydrobiologia 691:97–107
Bittencourt-Oliveira MC (2003) Detection of potential microcystin-producing cyanobacteria in Brazilian reservoirs with a mcyB molecular marker. Harmful Algae 2:51–60
Bittencourt-Oliveira MC, Oliveira MC, Pinto E (2011) Diversity of microcystin-producing genotypes in Brazilian strains of Microcystis (Cyanobacteria). Braz J Biol 71:209–216
Bittencourt-Oliveira MC, Camargo-Santos D, Moura AN, Francisco IB, Dias CTS, Molica RJR, Cordeiro-Araújo MK (2013) Effect of toxic and non-toxic crude extracts on different Microcystis species (Cyanobacteria). Afr J Microbiol Res 7:2596–2600
Briand E, Gugger M, François JCC, Bernard J, Humbert F, 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
Briand E, Bormans M, Quiblier C, Salençon MJ, Humbert JF (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
Campos L, Araújo P, Pinheiro C, Azevedo J, Osório H, Vasconcelos V (2013) Effects on growth, antioxidant enzyme activity and levels of extracellular proteins in the green alga Chlorella vulgaris exposed to crude cyanobacterial extracts and pure microcystin and cylindrospermopsin. Ecotoxicol Environ Saf 94:45–53
Chen YW, Qin BQ, Teubner K, Dokulil MT (2003) Long-term dynamics of phytoplankton assemblages: Microcystis-domination in Lake Taihu, a large shallow lake in China. J Plankton Res 25:445–453
Dunker S, Jakob T, Wilhelm C (2013) Contrasting effects of the cyanobacterium Microcystis aeruginosa on the growth and physiology of two green algae, Oocystis marsonii and Scenedesmus obliquus, revealed by flow cytometry. Freshw Biol 58:1573–1587
Fogg GE, Thake B (1987) Algae Cultures and Phytoplankton Ecology. 3rd edn London: The University of Wisconsins Press Ltd p 269
Frossard V, Versanne-Janodet S, Aleya L (2014) Factors supporting harmful macroalgal blooms in flowing waters: a 2-year study in the lower Ain River, France. Harmful Algae 33:19–28
Guillard RRL (1973) Division rates. In: Stein J (ed) Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, Cambridge, pp 289–311
Harada KI, Ozaki K, Tsuzuki S, Kato H, Hasegawa M, Kuroda E, Arii S, Tsuji K (2009) Blue color formation of cyanobacteria with b-cyclocitral. J Chem Ecol 35:1295–1301
Harel M, Weiss G, Lieman-Hurwitz J, Gun J, Lev O, Lebendiker M, Temper V, Block C, Sukenik A, Zohary T, Braun S, Carmeli S, Kaplan A (2013) Interactions between Scenedesmus and Microcystis may be used to clarify the role of secondary metabolites. Environ Microbiol Rep 5:97–104
Hu ZQ, Liu YD, Li DH (2004) Physiological and biochemical analyses of microcystin-RR toxicity to the cyanobacterium Synechococcus elongatus. Environ Toxicol 19:571–577
Jochimsen EM, Carmichael WW, An JS, Cardo DM, Cookson ST, Holmes CE, Antunes MB, de Melo Filho DA, Lyra TM, Barreto VS, Azevedo SM, Jarvis WR (1998) Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. New Engl J Med 338:873–878
Jonsson PR, Pavia H, Toth G (2009) Formation of harmful algal blooms cannot be explained by allelopathic interactions. Proc Natl Acad Sci 106:11177–11182
Kaplan A, Harel M, Kaplan-Levy RN, Hadas O, Sukenik A, Dittmann E (2012) The languages spoken in the water body (or the biological role of cyanobacterial toxins). Front Microbiol 3:138
Kemp A, John J (2006) Microcystins associated with Microcystis dominated blooms in the southwest wetlands, Western Australia. Environ Toxicol 21:125–130
Kuwata A, Miyazaki T (2000) Effects of ammonium supply rates on competition between Microcystis novacekii (Cyanobacteria) and Scenedesmus quadricauda (Chlorophyta): simulation study. Ecol Modell 135:81–87
Leao PN, Vasconcelos MTSD, Vasconcelos VM (2009) Allelopathic activity of cyanobacteria on green microalgae at low cell densities. Eur J Phycol 44:347–355
Leflaive J, Ten-Hage L (2007) Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshw Biol 52:199–214
Li Y, Li D (2012) Competition between toxic Microcystis aeruginosa and nontoxic Microcystis wesenbergii with Anabaena PCC7120. J Appl Phycol 24:69–78
Lund JWG, Kipling C, Lecren ED (1958) The invert microscope method of estimating algae numbers and statistical basis of estimations by counting. Hydrobiologia 11:143–170
Magrann T, Dunbar SG, Boskovic DS, Hayes WK (2012) Impacts of Microcystis on algal biodiversity and use of new technology to remove Microcystis and dissolved nutrients. Lakes Reserv Res Manag 17:231–239
Máthé C, M-Hamvas M, Vasas G, Surányi G, Bácsi I, Beyer D, Tóth S, Tímár M, Borbély G (2007) Microcystin-LR, a cyanobacterial toxin, induces growth inhibition and histological alterations in common reed (Phragmites australis) plants regenerated from embryogenic calli. New Phytol 176:824–835
Mello MM, Soares MCS, Roland F, Lurling M (2012) Growth inhibition and colony formation in the cyanobacterium Microcystis aeruginosa induced by the cyanobacterium Cylindrospermopsis raciborskii. J Plankton Res 34:987–994
Papadimitriou T, Katsiapi M, Kormas KA, Moustaka-Gouni M, Kagalou I (2013) Artificially-born “killer” lake: phytoplankton based water quality and microcystin affected fish in a reconstructed lake. Sci Total Environ 452–453:116–124
Pinheiro C, Azevedo J, Campos A, Loureiro S, Vasconcelos V (2013) Absence of negative allelopathic effects of cylindrospermopsin and microcystin-LR on selected marine and freshwater phytoplankton species. Hydrobiologia 705:27–42
Rashidan KK, Bird DF (2001) Role of predatory bacteria in the termination of a cyanobacterial bloom. Microb Ecol 41:97–105
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Ross C, Santiago-Vazquez L, Paul V (2006) Toxin release in response to oxidative stress and programmed cell death in the cyanobacterium Microcystis aeruginosa. Aquat Toxicol 78:66–73
Sedmak B, Carmeli S, Elersek T (2008) “Non-toxic” cyclic peptides induce lysis of cyanobacteria—an effective cell population density control mechanism in cyanobacterial blooms. Microb Ecol 56:201–209
Sevilla E, Martin-Luna B, Vela L, Bes MT, Fillat MF, Peleato ML (2008) Iron availability affects mcyD expression and microcystin-LR synthesis in Microcystis aeruginosa PCC 7806. Environ Microbiol 10:2476–2483
Shen H, Song L (2007) Comparative studies on physiological responses to phosphorus in two phenotypes of bloom-forming Microcystis. Hydrobiologia 592:475–486
Sukenik A, Eshkol R, Livne A, Hadas O, Rom M, Tchernov D, Vardi A, Kaplan A (2002) Inhibition of growth and photosynthesis of the dinoflagellate Peridinium gatunense by Microcystis sp. (cyanobacteria): a novel allelopathic mechanism. Limnol Oceanogr 47:1656–1663
Takeya K, Kuwata A, Yoshida M, Miyazaki T (2004) Effect of dilution rate on competitive interactions between the cyanobacterium Microcystis novacekii and the green alga Scenedesmus quadricauda in mixed chemostat cultures. J Plankton Res 26:29–35
Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicol Appl Pharm 203:201–218
Xu N, Duan S, Li A, Zhang C, Cai Z, Hu Z (2010) Effects of temperature, salinity and irradiance on the growth of the harmful dinoflagellate Prorocentrum donghaienense Lu. Harmful Algae 9:13–17
Yang J, Deng X, Xian Q, Qian X, Li A (2014) Allelopathic effect of Microcystis aeruginosa on Microcystis wesenbergii: microcystin-LR as a potential allelochemical. Hydrobiologia 727:65–73
You XH, Wang ZL, Shi XY et al (2007) Advances in the studies of phytoplankton interspecific competition. Trans Oceanol Limn 4:161–166
Zhang P, Zhai C, Wang X, Liu C, Jiang J, Xue Y (2013) Growth competition between Microcystis aeruginosa and Quadrigula chodatii under controlled conditions. J Appl Phycol 25:555–565
Acknowledgments
This study was supported by grants from São Paulo Research Foundation (FAPESP—2011/50840-0 and 2013/11306-3 to M.A. Chia) and Brazilian National Research Council (CNPq—301739/2011-0).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bittencourt-Oliveira, M.C., Chia, M.A., de Oliveira, H.S.B. et al. Allelopathic interactions between microcystin-producing and non-microcystin-producing cyanobacteria and green microalgae: implications for microcystins production. J Appl Phycol 27, 275–284 (2015). https://doi.org/10.1007/s10811-014-0326-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-014-0326-2