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

  • PHYTOPLANKTON & BIOTIC INTERACTIONS
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Abstract

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.

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References

  • 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).

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1038/ncomms6350.

    Article  Google Scholar 

  • 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 

  • Dziallas, C. & H.-P. Grossart, 2012. Microbial interactions with the cyanobacterium Microcystis aeruginosa and their dependence on temperature. Marine Biology 159: 2389–2398.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Stocker, R., 2012. Marine microbes see a sea of gradients. Science 338(6107): 628–633.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

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Acknowledgements

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).

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Correspondence to H.-P. Grossart or A. Giani.

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Guest editors: Hugo Sarmento, Irina Izaguirre, Vanessa Becker & Vera L. M. Huszar / Phytoplankton and its Biotic Interactions

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10750_2018_3655_MOESM1_ESM.png

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

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)

Supplementary material 3 (PNG 55 kb)

10750_2018_3655_MOESM4_ESM.docx

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

Tab. S2: Concentration of dissolved oxygen in Volta Grande reservoir (sampling site VG3) from January to December 2011. Supplementary material 5 (DOCX 16 kb)

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Batista, A.M.M., Woodhouse, J.N., Grossart, HP. et al. Methanogenic archaea associated to Microcystis sp. in field samples and in culture. Hydrobiologia 831, 163–172 (2019). https://doi.org/10.1007/s10750-018-3655-3

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  • DOI: https://doi.org/10.1007/s10750-018-3655-3

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