, Volume 831, Issue 1, pp 163–172 | Cite as

Methanogenic archaea associated to Microcystis sp. in field samples and in culture

  • A. M. M. Batista
  • J. N. Woodhouse
  • H.-P. GrossartEmail author
  • A. GianiEmail author


Cyanobacterial mass developments impact the community composition of heterotrophic microorganisms with far-reaching consequences for biogeochemical and energy cycles of freshwater ecosystems including reservoirs. Here we sought to evaluate the temporal stability of methanogenic archaea in the water column and further scrutinize their associations with cyanobacteria. Monthly samples were collected from October 2009 to December 2010 in hypereutrophic Pampulha reservoir with permanently blooming cyanobacteria, and from January to December 2011 in oligotrophic Volta Grande reservoir with only sporadic cyanobacteria incidence. The presence of archaea in cyanobacterial cultures was investigated by screening numerous strains of Microcystis spp. from these reservoirs as well as from lakes in Europe, Asia, and North-America. We consistently determined the occurrence of archaea, in particular methanogenic archaea, in both reservoirs throughout the year. However, archaea were only associated with two strains (Microcystis sp. UFMG 165 and UFMG 175) recently isolated from these reservoirs. These findings do not implicate archaea in the occurrence of methane in the epilimnion of inland waters, but rather serve to highlight the potential of microhabitats associated with particles, including phytoplankton, to shelter unique microbial communities.


Cyanobacteria Methanogenic archaea Bacterial community composition Microcystis sp. Tropical reservoir 



We acknowledge the Phycology Laboratory team for field sampling, Solvig Pinnow, and Katharina Frindte for technical support on DGGE analysis, and Danilo Neves, Ivette Salka, and Katrin Attermeyer for support in statistical analysis. Algirdas Svanys is acknowledged for providing M. aeruginosa strains. We also acknowledge grant funding from CAPES (Coordenação Aperfeiçoamento do Pessoal Docente—PDSE program) which supported A.M.M.B., CEMIG (Companhia Eletrica de Minas Gerais) and FAPEMIG (Fundação de Amparo a Pesquisa de Minas Gerais) for grants provided to A.G, and DFG (Deutsche Forschungsgemeinschaft) for providing H-P.G. with two grants (GR 1540/20-1 and 21-1).

Supplementary material

10750_2018_3655_MOESM1_ESM.png (2.7 mb)
Fig S1. Archaeal DGGE banding profiles resulting from cultured Microcystis cultures derived from Brazil, Netherlands, Japan and Germany. L = Ladder. Supplementary material 1 (PNG 2752 kb)
10750_2018_3655_MOESM2_ESM.png (645 kb)
Figure S2. Linear regression exploring relationship between dissolved oxygen concentration (calculated as the median value over the integrated sampling depth; Pampulha 1-2 m, Volta Grande 5-10 m (Table S1, 2) and archaeal DGGE band number (Fig. 2) in A) Pampulha reservoir, B) Volta Grande reservoir and C) both Pampulha and Volta Grande reservoir. Supplementary material 2 (PNG 645 kb)
10750_2018_3655_MOESM3_ESM.png (56 kb)
Supplementary material 3 (PNG 55 kb)
10750_2018_3655_MOESM4_ESM.docx (14 kb)
Tab. S1: Concentration of dissolved oxygen in Pampulha reservoir from October 2009 to December 2010. Supplementary material 4 (DOCX 14 kb)
10750_2018_3655_MOESM5_ESM.docx (16 kb)
Tab. S2: Concentration of dissolved oxygen in Volta Grande reservoir (sampling site VG3) from January to December 2011. Supplementary material 5 (DOCX 16 kb)


  1. Andrade, G. S. D., 2014. Green house gases emission (GHG) and atmospheric impacts as a consequence of hydroelectricity production: case of study of Volta Grande reservoir. M.Sc. dissertation in “Sanitation, Environment and Water Resources” Graduate Program of the Universidade Federal de Minas Gerais (UFMG), 126 p. (original in Portuguese).Google Scholar
  2. Angel, R., D. Matthies & R. Conrad, 2011. Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen. PLoS ONE 6(5): e20453.CrossRefGoogle Scholar
  3. Barros, N., J. J. Cole, L. J. Tranvik, Y. T. Prairie, D. Bastviken, V. L. M. Huszar, P. del Giorgio & F. Roland, 2011. Carbon emission from hydroelectric reservoirs linked to reservoir age and latitude. Nature Geoscience 4: 593–596.CrossRefGoogle Scholar
  4. Bogard, M. J., P. A. del Giorgio, L. Boutet, M. C. Garcia Chaves, Y. T. Prairie, A. Merante & A. M. Derry, 2014. Oxic water column methanogenesis as a major component of aquatic CH4 fluxes. Nature Communication. Scholar
  5. Braga, F. M. S. & L. M. Gomiero, 1997. Análise da pesca experimental realizada no reservatório de Volta Grande, rio Grande (MG-SP). Boletim do Instituto de Pesca 24: 131–138.Google Scholar
  6. Dziallas, C. & H.-P. Grossart, 2012. Microbial interactions with the cyanobacterium Microcystis aeruginosa and their dependence on temperature. Marine Biology 159: 2389–2398.CrossRefGoogle Scholar
  7. Eigemann, F., S. Hilt, I. Salka & H.-P. Grossart, 2013. Bacterial community composition associated with freshwater algae: species specificity vs. dependency on environmental conditions and source community. FEMS Microbiology Ecology 83(3): 650–663.CrossRefGoogle Scholar
  8. Eilers, H., J. Pernthaler & R. Amann, 2000. Succession of pelagic marine bacteria during enrichment: a close look on cultivation-induced shifts. Applied and Environmental Microbiology 66: 4634–4640.CrossRefGoogle Scholar
  9. Fan, X. & Q. L. Wu, 2014. Intra-habitat differences in the composition of the methanogenic archaeal community between the Microcystis-dominated and the macrophyte-dominated bays in Taihu Lake. Geomicrobiology Journal 31: 907–916.CrossRefGoogle Scholar
  10. Figueredo, C. C., R. M. Pinto-Coelho, A. M. M. B. Lopes, P. H. O. Lima, B. Gücker & A. Giani, 2016. From intermittent to persistent cyanobacterial blooms: identifying the main drivers in an urban tropical reservoir. Journal of Limnology 75: 445–454.Google Scholar
  11. Giani, A., R. M. Pinto-Coelho, S. J. M. Oliveira & A. Pelli, 1988. Ciclo sazonal de parâmetros físico-químicos da água e distribuição horizontal de nitrogênio e fósforo no reservatório da Pampulha (Belo Horizonte, MG, Brasil). Ciência e Cultura 40: 69–77.Google Scholar
  12. Grossart, H.-P., K. Frindte, C. Dziallas, W. Eckert & K. W. Tang, 2011. Microbial methane production in oxygenated water column of an oligotrophic lake. PNAS Environmental Science 108(49): 19657–19661.CrossRefGoogle Scholar
  13. Karl, D. M., F. L. Beversdor, K. M. Bjorkman, M. J. Church, A. Martinez & E. F. Delong, 2008. Aerobic production of methane in the sea. Nature Geoscience 1: 473–478.CrossRefGoogle Scholar
  14. Mello NAST., 2015. Climate change as positive feedback for methane (CH4) emissions from aquatic tropical ecosystems. PhD Thesis in “Ecology, Conservation and Management” Graduate Program of the Universidade Federal de Minas Gerais (UFMG). 117 p. Original in Portuguese.Google Scholar
  15. Muyzer, G., E. C. Waal & A. G. Uitierlinden, 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of Polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59: 695–700.PubMedPubMedCentralGoogle Scholar
  16. Paerl, H. W., 1982. Interactions with bacteria. In Carr, N. G. & B. A. Whitton (eds), The Biology of Cyanobacteria. Blackwell Scientific Publications, Oxford: 441–461.Google Scholar
  17. Pinhassi, J., L. Gómez-Consarnau, L. Alonso-Sáez, M. M. Sala, M. Vidal, C. Pedrós-Alió & J. M. Gasol, 2006. Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquatic Microbial Ecology 44: 241–252.CrossRefGoogle Scholar
  18. Ploug, H., 2008. Cyanobacterial surface blooms formed by Aphanizomenon sp. and Nodularia spumigena in the Baltic Sea: small-scale Xuxes, pH, and oxygen microenvironments. Limnology and Oceanography 53: 914–921.CrossRefGoogle Scholar
  19. Pouliot, J., P. E. Galand, C. Lovejoy & W. F. Vincent, 2009. Vertical structure of archaeal communities and the distribution of ammonia monooxygenase A gene variants in two meromictic High Arctic lakes. Environmental Microbiology 11(3): 687–699.CrossRefGoogle Scholar
  20. Repeta, D. J., S. Ferron, O. A. Sosa, C. G. Johnson, L. D. Repeta, M. Acker, E. F. DeLong & D. M. Karl, 2016. Marine methane paradox explained by bacterial degradation of dissolved organic matter. Nature Geoscience 9(12): 884.CrossRefGoogle Scholar
  21. Stocker, R., 2012. Marine microbes see a sea of gradients. Science 338(6107): 628–633.CrossRefGoogle Scholar
  22. Tang, K., D. McGinnis, D. Ionescu & H. P. Grossart, 2016. Methane production in oxic lake waters potentially increases aquatic methane flux to air. Environmental Science & Technology Letters 6: 227–233.CrossRefGoogle Scholar
  23. Verspagen, J. M. H., E. O. F. M. Snelder, P. M. Visser, K. D. Jöhnk, B. W. Ibelings, L. R. Mur & J. Huisman, 2005. Benthic-pelagic coupling in the population dynamics of the harmful cyanobacterium Microcystis. Freshwater Biology 50(5): 854–867.CrossRefGoogle Scholar
  24. Watanabe, T., S. Asakawa, A. Nakamura, K. Nagaoka & M. Kimura, 2004. DGGE method for analyzing 16S rDNA of methanogenic archaeal community in paddy field soil. FEMS Microbiology Letter 232: 153–163.CrossRefGoogle Scholar
  25. Woodhouse, J. N., A. S. Kinsela, R. N. Collins, L. C. Bowling, G. L. Honeyman, J. K. Holliday & B. A. Neilan, 2016. Microbial communities reflect temporal changes in cyanobacterial composition in a shallow ephemeral freshwater lake. ISME J 10(6): 1337–1351.CrossRefGoogle Scholar
  26. Zhou, J., M. A. Bruns & J. M. Tiedje, 1996. DNA recovery from soils of diverse composition. Applied and Environmental Microbiology 62: 695–724.Google Scholar
  27. Zhou, Y. L., H. L. Jiang & H. Y. Cai, 2015. To prevent the occurrence of black water agglomerate through delaying decomposition of cyanobacterial bloom biomass by sediment microbial fuel cell. Journal of Hazardous Materials 287: 7–15.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BotanyUniversidade Federal de Minas Gerais (UFMG)Belo HorizonteBrazil
  2. 2.Department of Limnology of Stratified LakesInstitute of Freshwater Ecology and Inland FisheriesNeuglobsowGermany
  3. 3.Institute of Biochemistry and BiologyPotsdam UniversityPotsdamGermany

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