Abstract
Associated heterotrophic bacteria alter the microenvironment of cyanobacteria and potentially influence cyanobacterial development. Therefore, we studied interactions of the unicellular freshwater cyanobacterium Microcystis aeruginosa with heterotrophic bacteria. The associated bacterial community was greatly driven by temperature as seen by DNA fingerprinting. However, the associated microbes also closely interacted with the cyanobacteria indicating changing ecological consequence of the associated bacterial community with temperature. Whereas concentration of dissolved organic carbon in cyanobacterial cultures changed in a temperature-dependent manner, its quality greatly varied under the same environmental conditions, but with different associated bacterial communities. Furthermore, temperature affected quantity and quality of cell-bound microcystins, whereby interactions between M. aeruginosa and their associated community often masked this temperature effect. Both macro- and microenvironment of active cyanobacterial strains were characterized by high pH and oxygen values creating a unique habitat that potentially affects microbial diversity and function. For example, archaea including ‘anaerobic’ methanogens contributed to the associated microbial community. This implies so far uncharacterized interactions between Microcystis aeruginosa and its associated prokaryotic community, which has unknown ecological consequences in a climatically changing world.
Similar content being viewed by others
References
Blom JF, Jüttner F (2005) High crustacean toxicity of microcystin congeners does not correlate with high protein phosphatase inhibitory activity. Toxicon 46:465–470
Casamatta DA, Wickstrom CE (2000) Sensitivity of two disjunct bacterioplankton communities to exudates from the cyanobacterium Microcystis aeruginosa Kützing. Microb Ecol 41:64–73
Cole JJ (1982) Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst 13:291–314
Czarnecki O, Lippert I, Henning M, Welker M (2006) Identification of peptide metabolites of Microcystis (Cyanobacteria) that inhibit trypsin-like activity in planktonic herbivorous Daphnia (Cladocera). Environ Microbiol 8:77–87
De Stasio jun BT, Hill DK, Kleinhans JM, Nibbelink NP, Magnuson JJ (1996) Potential effects of global climate change on small north-temperate lakes: physics, fish, and plankton. Limnol Oceanogr 41:1136–1149
DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689
Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438:1–12
Dziallas C, Grossart H-P (2011a) Temperature and biotic factors influence bacterial communities associated with Microcystis sp. (cyanobacteria). Environ Microbiol 13:1632–1641
Dziallas C, Grossart H-P (2011b) Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS ONE 6(9):e25569. doi:10.1371/journal.pone.0025569
Fastner J, Flieger I, Neumann U (1998) Optimised extraction of microcystins from field samples—a comparison of different solvents and procedures. Wat Res 32:3177–3181
Futuyama DJ (1983). Evolutionary interactions among herbivorous insects and plants. In: Futuyama DJ, Slatkin M (eds) Coevolution. Sinauer Associates Inc., Sunderland, pp 207–231
Ghadouani A, Pinel-Alloul B, Plath K, Codd GA, Lampert W (2004) Effects of Microcystis aeruginosa and purified microcystin-LR on the feeding behavior of Daphnia pulicaria. Limnol Oceanogr 49:666–679
Grossart H-P, Frindte K, Dziallas C, Eckert W, Tang KW (2011) Microbial methane production in oxygenated water column of an oligotrophic lake. Proc Natl Acad Sci USA 108:19657–19661
Gupta N, Pant SC, Vijayaraghavan R, Lakshmana Rao PV (2003) Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice. Toxicology 188:285–296
Ho L, Gaudieux A-L, Fannok S, Newcombe G, Humpage AR (2007) Bacterial degradation of microcystin toxins in drinking water eliminates their toxicity. Toxicon 50:438–441
Holliday IE (2011) Two-Way ANOVA (v1.0.3) in free statistics software (v1.1.23-r7), office for research development and education. http://www.wessa.net/Ian.Holliday/rwasp_Two%20Factor%20ANOVA.wasp/
Hudnell HK, Dortch Q (2008) A synopsis of research needs identified at the interagency, international symposium on cyanobacterial harmful algal blooms (ISOC-HAB). In: Hudnell HK (ed) Cyanobacterial harmful algal blooms—state of the science and research needs. Springer, New York
Ibelings BW, Mur LR (1992) Microprofiles of photosynthesis and oxygen concentration in Microcystis sp. Scums. FEMS Microbiol Ecol 86:195–203
Jähnichen S, Petzoldt T, Benndorf J (2001) Evidence for control of microcystin dynamics in Bautzen Reservoir (Germany) by cyanobacterial population growth rates and dissolved inorganic carbon. Arch Hydrobiol 150:177–196
Jähnichen S, Long BM, Petzoldt T (2011) Microcystin production by Microcystis aeruginosa: direct regulation by multiple environmental factors. Harmful Algae. doi:10.1016/j.hal.2011.09.002
Kirkwood AE, Nalewajko C, Fulthorpe RR (2006) The effects of cyanobacterial exudates on bacterial growth and biodegradation of organic contaminants. Microb Ecol 51:4–12
Kühl M, Glud RN, Ploug H, Ramsing NB (1996) Microenvironmental control of photosynthesis and photosynthesis-coupled respiration in an epilithic cyanobacterial biofilm. J Phycol 32:799–812
Lawton L, Edwards C, Codd G (1994) Extraction and High-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst 119:1525–1530
Logan BE, Grossart H-P, Simon M (1994) Direct observation of phytoplankton, TEP and aggregates on polycarbonate filters using brightfield microscopy. J Plankton Res 16:1811–1815
Manz W, Amann R, Ludwig W, Wagner M, Schleifer K-H (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. System Appl Microbiol 15:593–600
Maruyama T, Kato K, Yokoyama A, Tanaka T, Hiraishi A, Park H-D (2003) Dynamics of microcystin-degrading bacteria in mucilage of Microcystis. Microb Ecol 46:279–288
Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S ribosomal-RNA. Appl Environ Microbiol 59:695–700
Nicolaus B, Panico A, Lama L, Romano I, Manca MC, De Guilio A, Gambacorta A (1999) Chemical composition and production of exopolysaccharides from representative members of heterocystous and nonheterocystous cyanobacteria. Phytochemistry 52:639–647
O′Brien HE, Miadlikowska J, Lutzoni F (2005) Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungus Peltigera. Eur J Phycol 40:363–378
Paerl HW (1996) Microscale physiological and ecological studies of aquatic cyanobacteria: macroscale implications. Microsc Res Techniq 33:47–72
Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58
Paerl HW, Millie DF (1996) Physiological ecology of toxic aquatic cyanobacteria. Phycologia 35:160–167
Paerl HW, Pinckney JL (1996) A mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling. Microb Ecol 31:225–247
Ploug H (2008) Cyanobacterial surface blooms formed by Aphanizomenon sp. and Nodularia spumigena in the Baltic Sea: small-scale fluxes, pH, and oxygen microenvironments. Limnol Oceanogr 53:914–921
Rantala A, Fewer DP, Hisbergues M, Rouhiainen L, Vaitomaa J, Börner T, Sivonen K (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci USA 101:568–573
Rouco M, Lopez-Rodas V, Flores-Moya A, Costas E (2011) Evolutionary changes in growth rate and toxin production in the cyanobacterium Microcystis aeruginosa under a scenario of eutrophication and temperature increase. Environ Microbiol 62:265–273
Salomon PS, Janson S, Graneli E (2003) Molecular identification of bacteria associated with filaments of Nodularia spumigena and their effect on the cyanobacterial growth. Harmful Algae 2:261–272
Sekar R, Pernthaler A, Pernthaler J, Warnecke F, Posch T, Amann R (2003) An improved protocol for quantification of freshwater Actinobacteria by flourescence in situ hybridization. Appl Environ Microbiol 69(5):2928–2935
Shapiro J (1990) Current Beliefs Regarding Dominance by Blue-Greens: The Case for the Importance of CO2 and pH. Verhandlungen IVTLAP 24:38–54
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
Surono I, Collado M, Salminen S, Meriluoto J (2008) Effect of glucose and incubation temperature on metabolically active Lactobacillus plantarum from dadih in removing microcystin-LR. Food ChemToxicol 46:502–507
Teske A, Wawer C, Muyzer G, Ramsing NB (1996) Distribution of sulfate-reducing bacteria in a stratied fjord (Mariager Fjord, Denmark) as evaluated by most-probable-number counts and DGGE of PCR amplified ribosomal DNA fragments. Appl Environ Microbiol 62:1405–1415
Welker M, Sejnohova L, Nemethova D, von Döhren H, Jarkovsky J, Marsalek B (2007) Seasonal Shifts in Chemotype Composition of Microcystis sp. Communities in the Pelagial and the Sediment of a Shallow Reservoir. Limnol Oceanogr 52:609–619
Wiedner C, Visser PM, Fastner J, Metcalf JS, Codd GA, Mur LR (2003) Effects of light on the Microcystin content of Microcystis strain PCC 7806. Appl Environ 69:1475–1481
Worm J, Sondergaard M (1998) Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquat Microb Ecol 14:19–28
Zehnder A, Gorham P (1960) Factors influencing the growth of Microcystis aeruginosa Kütz. Emend. Elenkin. Can J Microbiol 6:645–660
Zhou J, Bruns M, Tiedje J (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:695–724
Zilliges I, Kehr JC, Meissner S, Ishida K, Mikkat S, Hagemann M, Kaplan A, Börner T, Dittmann E (2011) The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness under oxidative stress conditions. PLoS One. doi:10.1371/journal.pone.0017615
Acknowledgments
We thank Solvig Pinnow for technical assistance and Andreas Ballot and Manfred Henning for providing us a variety of M. aeruginosa strains. We further acknowledge Helle Ploug for scientific input and technical help with the microelectrode measurements. We thank three anonymous reviewers for their very helpful suggestions and comments. This study was funded by the German Science Foundation (DFG, GR 1540/11-1,2).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by U. Sommer.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Dziallas, C., Grossart, HP. Microbial interactions with the cyanobacterium Microcystis aeruginosa and their dependence on temperature. Mar Biol 159, 2389–2398 (2012). https://doi.org/10.1007/s00227-012-1927-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-012-1927-4