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Selectivity and detrimental effects of epiphytic Pseudanabaena on Microcystis colonies

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Abstract

The cyanobacterium Microcystis aggregates into colonies with a mucilaginous sheath that constitutes a special microhabitat for many microorganisms that associate to it. Here, we examine the notorious, yet scarcely studied case of epiphytic association by the cyanobacterium Pseudanabaena sp. to colonial Microcystis. Co-cultivation of Pseudanabaena with different Microcystis strains evidenced strong specificity in the interaction, with dramatically different outcomes in each case, including (1) inability of Pseudanabaena to access the slime of Microcystis, (2) neutral co-existence of epiphytic Pseudanabaena and Microcystis, and (3) rapid epiphytic proliferation of Pseudanabaena, followed by lysis and rapid decay of Microcystis cells. Whereas strain-specific oligopeptide production could not explain the observed specificity, differences in slime microstructures among Microcystis strains revealed by low-temperature scanning electron microscopy suggest that slime structural features might initially determine the ability of Pseudanabaena to colonize Microcystis, subsequently driving the outcome of the interaction. Furthermore, even under “neutral” co-existence, Pseudanabaena proliferation results in an increase in density that leads to colony settling, implying potential selective losses under natural conditions. Both the selective and antagonistic characters of the interaction indicate that epiphytic Pseudanabaena have the potential to contribute to the dynamics of strains in natural Microcystis communities.

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References

  • Acinas, S. G., T. H. Haverkamp, J. Huisman & L. J. Stal, 2009. Phenotypic and genetic diversification of Pseudanabaena spp. (cyanobacteria). The ISME journal 3: 31–46.

    Article  CAS  PubMed  Google Scholar 

  • Agha, R., S. Cires, L. Woermer, J. Antonio Dominguez & A. Quesada, 2012. Multi-scale strategies for the monitoring of freshwater cyanobacteria: reducing the sources of uncertainty. Water Research 46: 3043–3053.

    Article  CAS  PubMed  Google Scholar 

  • Agha, R., S. Cires, L. Woermer & A. Quesada, 2013. Limited stability of microcystins in oligopeptide compositions of Microcystis aeruginosa (Cyanobacteria): implications in the definition of chemotypes. Toxins 5: 1089–1104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agha, R., M. Á. Lezcano, M. D. M. Labrador, S. Cires & A. Quesada, 2014. Seasonal dynamics and sedimentation patterns of Microcystis oligopeptide chemotypes reveal subpopulations with different ecological traits. Limnology and Oceanography 59: 861–871.

    Article  Google Scholar 

  • Agha, R. & A. Quesada, 2014. Oligopeptides as biomarkers of cyanobacterial subpopulations. toward an understanding of their biological role. Toxins 6: 1929–1950.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bartram, J. & I. Chorus, 1999. Toxic Cyanobacteria in Water: A Guide to their Public Health Consequences, Monitoring and Management. E & FN Spon, London.

    Google Scholar 

  • Beard, S. J., P. A. Davis, D. Iglesias-Rodriguez, O. M. Skulberg & A. E. Walsby, 2000. Gas vesicle genes in Planktothrix spp. from Nordic lakes: strains with weak gas vesicles possess a longer variant of gvpC. Microbiol.-U. K. 146: 2009–2018.

    Article  CAS  Google Scholar 

  • Bers, A. V. & M. Wahl, 2004. The influence of natural surface microtopographies on fouling. Biofouling 20: 43–51.

    Article  CAS  PubMed  Google Scholar 

  • Bolch, C. J. & S. I. Blackburn, 1996. Isolation and purification of Australian isolates of the toxic cyanobacterium Microcystis aeruginosa Kütz. Journal of Applied Phycology 8: 5–13.

    Article  Google Scholar 

  • Caiola, M. G. & S. Pellegrini, 1984. Lysis of Microcystis aeruginosa (Kütz.) By Bdellovibrio-like bacteria. Journal of phycology 20: 471–475.

    Article  Google Scholar 

  • Caiola, M. G., Pellegrini, S., Gerola, F. M. & Ribaldone, A., 1991. Bdellovibrio-like bacteria in Microcystis aeruginosa. Algological Studies/Archiv für Hydrobiologie, Supplement Volumes, 369-376.

  • Chang, T. P., 1985. Selective inhabitation of parasitic cyanophyte Pseudanabaena in water-bloom Microcystis colonies. Archiv für Hydrobiologie 104: 419–426.

    Google Scholar 

  • Cirés, S., L. Wörmer, R. Agha & A. Quesada, 2013. Overwintering populations of Anabaena, Aphanizomenon and Microcystis as potential inocula for summer blooms. Journal of Plankton Research 35: 1254–1266.

    Article  Google Scholar 

  • Czarnecki, O., M. Henning, I. Lippert & M. Welker, 2006. Identification of peptide metabolites of Microcystis (Cyanobacteria) that inhibit trypsin-like activity in planktonic herbivorous Daphnia (Cladocera). Environmental Microbiology 8: 77–87.

    Article  CAS  PubMed  Google Scholar 

  • De los Ríos, A., C. Ascaso, J. Wierzchos, W. Warwick & A. Quesada, 2015. Microstructure and cyanobacterial composition of microbial mats from the High Arctic. Biodiversity and Conservation 24: 841–863.

    Article  Google Scholar 

  • Donlan, R. M., 2001. Biofilm formation: a clinically relevant microbiological process. Clinical Infectious Diseases 33: 1387–1392.

    Article  CAS  PubMed  Google Scholar 

  • Dziallas, C. & H. P. Grossart, 2011. Temperature and biotic factors influence bacterial communities associated with the cyanobacterium Microcystis sp. Environmental Microbiology 13: 1632–1641.

    Article  PubMed  Google Scholar 

  • Falconer, Ian R. & Andrew R. Humpage, 2005. Health risk assessment of cyanobacterial (blue-green algal) toxins in drinking water. International Journal of Environmental Research and Public Health 2: 43–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forni, C., F. R. Telo & M. G. Caiola, 1997. Comparative analysis of the polysaccharides produced by different species of Microcystis (Chroococcales, Cyanophyta). Phycologia 36: 181–185.

    Article  Google Scholar 

  • Gorham, P., S. McNicholas & E. D. Allen, 1982. Problems encountered in searching for new strains of toxic planktonic cyanobacteria. South African Journal of Science. 78: 357.

    Google Scholar 

  • Gumbo, J. R. & T. E. Cloete, 2013. Light and electron microscope assessment of the lytic activity of Bacillus on Microcystis aeruginosa. African Journal of Biotechnology 10: 8054–8063.

    Google Scholar 

  • Ilhe, T., 2008. The spatiotemporal variation of Microcystis spp. (Cyanophyceae) and microcystins in Quitzdorf reservoir (Sachsen). In German: Die raum-zeitliche Variation von Microcystis spp. (Cyanophyceae) und Microcystinen in der Talsperre Quitzdorf (Sachsen). Doctoral Dissertation. Universität Dresden, Germany.

  • Jiang, L., Yang, L., Xiao, L., Shi, X., Gao, G. & Qin, B., 2007. Quantitative studies on phosphorus transference occuring between Microcystis aeruginosa and its attached bacterium (Pseudomonas sp.). In: Eutrophication of Shallow Lakes with Special Reference to Lake Taihu, China, Springer: 161–165.

  • Johnson, Z. I., E. R. Zinser, A. Coe, N. P. Mcnulty, E. M. S. Woodward & S. W. Chisholm, 2006. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311: 1737–1740.

    Article  CAS  PubMed  Google Scholar 

  • Komárek, J. A. K., 2005. Cyanoprokaryota 2. Teil/2nd part: Oscillatoriales. In Büdel, L., L. Krienitz, G. Gärtner & M. Schargel (eds), Subwasserflora von Mitteleuropa 19/2. Elsevier, Heidelberg.

    Google Scholar 

  • Komárek, J. & J. Kaštovský, 2003. Coincidences of structural and molecular characters in evolutionary lines of cyanobacteria. Algological Studies 109: 305–325.

    Article  Google Scholar 

  • Manage, P. M., Z. I. Kawabata & S. Nakano, 2001. Dynamics of cyanophage-like particles and algicidal bacteria causing Microcystis aeruginosa mortality. Limnology 2: 73–78.

    Article  Google Scholar 

  • Pereira, S., A. Zille, E. Micheletti, P. Moradas-Ferreira, R. De Philippis & P. Tamagnini, 2009. Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiology Reviews 33: 917–941.

    Article  CAS  PubMed  Google Scholar 

  • Plude, J. L., D. L. Parker, O. J. Schommer, R. J. Timmerman, S. A. Hagstrom, J. M. Joers & R. Hnasko, 1991. Chemical characterization of polysaccharide from the slime layer of the cyanobacterium Microcystis flos-aquae C3-40. Applied and environmental Microbiology 57: 1696–1700.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds, C. S., G. H. M. Jaworski, H. A. Cmiech & G. F. Leedale, 1981. On the annual cycle of the blue-green-alga Microcystis-aeruginosa Kutz Emend Elenkin. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 293: 419–477.

    Article  Google Scholar 

  • Sedmak, B. & G. Kosi, 1997. Microcystins in Slovene freshwaters (Central Europe)-first report. Natural Toxins 5: 64–73.

    Article  CAS  PubMed  Google Scholar 

  • Sedmak, B., S. Carmeli & T. Elersek, 2008. “Non-Toxic” cyclic peptides induce lysis of cyanobacteria – an effective cell population density control mechanism in cyanobacterial blooms. Microbial Ecology 56: 201–209.

    Article  CAS  PubMed  Google Scholar 

  • Shen, H., Y. Niu, P. Xie, M. Tao & X. Yang, 2011. Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshwater Biology 56: 1065–1080.

    Article  CAS  Google Scholar 

  • Shia, L., Y. Cai, X. Wang, P. Li, Y. Yu & F. Kong, 2010. Community structure of bacteria associated with Microcystis colonies from cyanobacterial blooms. Journal of Freshwater Ecology 25: 193–203.

    Article  Google Scholar 

  • Sigee, D., A. Selwyn, P. Gallois & A. Dean, 2007. Patterns of cell death in freshwater colonial cyanobacteria during the late summer bloom. Phycologia 46: 284–292.

    Article  Google Scholar 

  • Sivonen, K. & G. Jones, 1999. Cyanobacterial toxins. In Chorus, I. & J. Bartram (eds), Toxic Cyanobacteria in Water A Guide to Their Public Health Consequences, Monitoring and Management. E & FN Spoon, London: 41–111.

    Google Scholar 

  • Sønstebø, J. H. & T. Rohrlack, 2011. Possible implications of chytrid parasitism for population subdivision in freshwater cyanobacteria of the genus Planktothrix. Applied and Environmental Microbiology 77: 1344–1351.

    Article  PubMed  Google Scholar 

  • Vasconcelos, V., J. Morais & M. Vale, 2011. Microcystins and cyanobacteria trends in a 14 year monitoring of a temperate eutrophic reservoir (Aguieira, Portugal). Journal of Environmental Monitoring 13: 668–672.

    Article  CAS  PubMed  Google Scholar 

  • Worm, J. & M. Søndergaard, 1998. Alcian blue-stained particles in a eutrophic lake. Journal of plankton research 20: 179–186.

    Article  Google Scholar 

  • Yarmoshenko, L., A. Kureyshevich & V. Yakushin, 2013. Microcystis botrys and Lemmermanniella flexa – new species of Cyanoprokaryota for the flora of Ukraine in phytoplankton of the Kanev reservoir. Hydrobiological Journal 49: 115–121.

    Google Scholar 

  • Young, F., C. Thomson, J. Metcalf, J. Lucocq & G. Codd, 2005. Immunogold localisation of microcystins in cryosectioned cells of Microcystis. Journal of Structural Biology 151: 208–214.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This article is dedicated to our colleague Fernando Pinto, who sadly passed away during the preparation of this manuscript and whose assistance operating the LT-SEM made this work possible. Prof. Assaf Sukenik is acknowledged for kindly providing bloom samples from Lake Kinneret. RA was supported by a Postdoctoral Fellowship from the Alexander von Humboldt Foundation during the writing process of this manuscript. The authors also acknowledge the European Co-Operation in Science and Technology COST Action ES1105 ‘CYANOCOST’ for networking and knowledge-transfer support. LT-SEM analyses were supported by the grant CTM2012-3822-C02-02.

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Agha, R., del Mar Labrador, M., de los Ríos, A. et al. Selectivity and detrimental effects of epiphytic Pseudanabaena on Microcystis colonies. Hydrobiologia 777, 139–148 (2016). https://doi.org/10.1007/s10750-016-2773-z

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