Skip to main content
Log in

Prokaryoplankton and phytoplankton community compositions in five large deep perialpine lakes

  • LARGE AND DEEP PERIALPINE LAKES
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Phytoplankton (PCC) and prokaryoplankton community compositions were studied in five perialpine lakes (Garda, Maggiore, Como, Iseo, and Lugano) of different trophic conditions and mixing regimes, using inverted microscopy and CARD-FISH technique. The aim of this research was to assess, for the first time in these lakes, the relationships among PCC, bacteria, and archaea, and the effects of environmental drivers. We observed a clear difference of PCC compositions in spring and summer. All the lakes showed Bacillariophyta dominating in spring, whereas in summer, there were remarkable differences of PCC. Prokaryoplankton composition showed more pronounced differences in the vertical profile than those between spring and summer. The oligomictic lakes showed a uniform vertical gradient of prokaryotes in spring, while in the meromictic lakes, their abundances were incremented with depth. In summer, the prokaryotic community changed, and niche differentiation occurred in almost all lakes. In conclusion, our study showed a general pattern, common to all the lakes, of a first appearance of the large-sized “opportunistic” bacteria in spring, followed by ultramicrobacteria, less vulnerable to predation in summer. Significant correlations between a few PCC and bacterial groups were found, thus elucidating that functional interactions can be the key to understand plankton successions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allgaier, M. & H. P. Grossart, 2006. Diversity and seasonal dynamics of Actinobacteria populations in four lakes in northeastern Germany. Applied and Environmental Microbiology 72: 3489–3497.

    Article  CAS  Google Scholar 

  • Amann, R. I., J. Brian, R. Binder, J. Olson, S. W. Chisholm, R. Devereux & D. A. Stahl, 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Applied Environmental Microbiology 56: 1919–1925.

    CAS  PubMed  Google Scholar 

  • Amann, R. & B. Fuchs, 2008. Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nature Reviews Microbiology 6: 339–348.

    Article  CAS  Google Scholar 

  • Amaral, V., D. Graeber, D. Calliari & C. Alonso, 2016. Strong linkages between DOM optical properties and main clades of aquatic bacteria. Limnology and Oceanography 61: 906–918.

    Article  CAS  Google Scholar 

  • Ambrosetti, W. & L. Barbanti, 1992. Physical limnology in Italy: an historical review. Memorie dell’Istituto italiano di idrobiologia 50: 37–59.

    Google Scholar 

  • Ambrosetti, W. & L. Barbanti, 2002. Physical limnology of Italian lakes. Relationship between morphometry and heat content. Journal of Limnology 61: 147–157.

    Article  Google Scholar 

  • Ambrosetti, W., L. Barbanti & E. A. Carrara, 2010. Mechanisms of hypolimnion erosion in a deep lake (Lago Maggiore, N. Italy). Journal of Limnology 69: 3–14.

    Article  Google Scholar 

  • Amin, S. A., M. S. Parker & E. V. Armbrust, 2012. Interactions between diatoms and bacteria. Microbiology and Molecular Biology Reviews 76: 667–684.

    Article  CAS  Google Scholar 

  • Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.

    Google Scholar 

  • American Public Health Association, American Water Works Association & Water Pollution Control Federation, 2005. Standard Methods for the Examination of Water and Wastewater, 21st ed. American Public Health Association, Washington.

    Google Scholar 

  • Barberán, A. & E. O. Casamayor, 2010. Global phylogenetic community structure and β-diversity patterns in surface bacterioplankton metacommunities. Aquatic Microbial Ecology 59: 1–10.

    Article  Google Scholar 

  • Batani, G., G. Pérez, G. de la Martínez, C. Piccini & S. Fazi, 2016. Competition and protist predation are important regulators of riverine bacterial community composition and size distribution. Journal of Freshwater Ecology 31: 609–623.

    Article  CAS  Google Scholar 

  • Berg, K. A., Ch Lyra, K. Sivonen, L. Paulin, S. Suomalainen, P. Tuomi & J. Rapala, 2009. High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. The ISME Journal 3: 314–325.

    Article  CAS  Google Scholar 

  • Biers, E. J., S. L. Sun & E. C. Howard, 2009. Prokaryotic genomes and diversity in surface ocean waters: interrogating the global ocean sampling metagenome. Applied and Environmental Microbiology 75: 2221–2229.

    Article  CAS  Google Scholar 

  • Boucher, D., L. Jardillier & D. Debroas, 2006. Succession of bacterial community composition over two consecutive years in two aquatic systems: a natural lake and a lake-reservoir. FEMS Microbiology Ecology 55: 79–97.

    Article  CAS  Google Scholar 

  • Bruckner, C. G., C. Rehm, H. P. Grossart & P. G. Kroth, 2011. Growth and release of extracellular organic compounds by benthic diatoms depend on interactions with bacteria. Environmental Microbiology 13: 1052–1063.

    Article  CAS  Google Scholar 

  • Callieri, C., G. Corno, E. Caravati, S. Rasconi, M. Contesini & R. Bertoni, 2009. Bacteria, archaea, and crenarchaeota in the epilimnion and hypolimnion of a deep holo-oligomictic lake. Applied and Environmental Microbiology 75: 7298–7300.

    Article  CAS  Google Scholar 

  • Callieri, C., R. Bertoni, M. Contesini & F. Bertoni, 2014a. Lake level fluctuations boost toxic cyanobacterial “oligotrophic blooms”. PLoS ONE 9: e109526.

    Article  Google Scholar 

  • Callieri, C., M. Coci, E. M. Eckert, M. Salcher & R. Bertoni, 2014b. Archaea and Bacteria in deep lake hypolimnion: in situ dark inorganic carbon uptake. Journal of Limnology 73: 47–54.

    Article  Google Scholar 

  • Callieri, C., S. Hernández-Avilés, M. M. Salcher, D. Fontaneto & R. Bertoni, 2016. Distribution patterns and environmental correlates of Thaumarchaeota abundance in six deep subalpine lakes. Aquatic Sciences 78: 215–225.

    Article  CAS  Google Scholar 

  • Callieri, C., G. Corno, M. Contesini, D. Fontaneto & R. Bertoni, 2017. Transparent exopolymer particles (TEP) are driven by chlorophyll a and mainly confined to the euphotic zone in a deep subalpine lake. Inland waters 7: 118–127.

    Article  Google Scholar 

  • Coci, M., N. Odermatt, M. M. Salcher, J. Pernthaler & G. Corno, 2015. Ecology and distribution of Thaumarchaea in the deep hypolimnion of Lake Maggiore. Archaea (Article ID 590434). https://doi.org/10.1155/2015/590434.

    Article  Google Scholar 

  • Daims, H., A. Bruhl, R. Amann, K. H. Schleifer & M. Wagner, 1999. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Systematic Applied Microbiology 22: 434–444.

    Article  CAS  Google Scholar 

  • De Figueiredo, D. R., M. J. Pereira & A. Correia, 2010. Seasonal modulation of bacterioplankton community at a temperate eutrophic shallow lake. World Journal of Microbiology and Biotechnology 26: 1067–1077.

    Article  CAS  Google Scholar 

  • De Wever, A., K. Muylaert, K. Van der Gucht, S. Pirlot, Ch Cocquyt, J. P. Descy, P. D. Plisnier & W. Vyverman, 2005. Bacterial community composition in Lake Tanganyika: vertical andhorizontal heterogeneity. Applied and Environmental Microbiology 71: 5029–5037.

    Article  Google Scholar 

  • Doxey, A. C., D. A. Kurtz, M. D. J. Lynch, L. A. Sauder & J. D. Neufeld, 2015. Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production. The ISME Journal 9: 461–471.

    Article  CAS  Google Scholar 

  • Eiler, A. & S. Bertilsson, 2007. Flavobacteria blooms in four eutrophic lakes: linking population dynamics of freshwater bacterioplankton to resource availability. Applied and Environmental Microbiology 73: 3511–3518.

    Article  CAS  Google Scholar 

  • Eiler, A., J. A. Olsson & S. Bertilsson, 2006. Diurnal variations in the auto- and heterotrophic activity of cyanobacterial phycospheres (Gloeotrichia echinulata) and the identity of attached bacteria. Freshwater Biology 51: 298–311.

    Article  CAS  Google Scholar 

  • Fogg, G. E., 1983. The ecological significance of extracellular products of phytoplankton photosynthesis. Botanica Marina 26: 3–14.

    Article  CAS  Google Scholar 

  • Garibaldi, L., A. Anzani, A. Marieni, B. Leoni & R. Mosello, 2003. Studies on the phytoplankton of the deep subalpine Lake Iseo. Journal of Limnology 62: 177–189.

    Article  Google Scholar 

  • Ghai, R., M. C. Megumi, A. Picazo, A. Camacho & F. Rodríguez-Valera, 2014. Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing. Molecular Ecology 23: 6073–6090.

    Article  CAS  Google Scholar 

  • Glöckner, F. O., B. M. Fuchs & R. Amann, 1999. Bacterioplankton composition of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Applied and Environmental Microbiology 65: 3721–3726.

    PubMed  PubMed Central  Google Scholar 

  • Glöckner, F. O., E. Zaichikov, N. Belkova, I. Denissova, J. Pernthaler, A. Pernthaler & R. Amann, 2000. Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Applied and Environmental Microbiology 66: 5053–5065.

    Article  Google Scholar 

  • Grossart, H. P., F. Levold, M. Allgaier, M. Simon & T. Brinkhoff, 2005. Marine diatom species harbour distinct bacterial communities. Environmental Microbiology 7: 860–873.

    Article  CAS  Google Scholar 

  • Guildford, S. J. & R. E. Hecky, 2000. Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: is there a common relationship? Limnology and Oceanography 45: 1213–1223.

    Article  CAS  Google Scholar 

  • Hahn, M. W., M. Pöckl & Q. L. L. Wu, 2005. Low intraspecific diversity in a Polynucleobacter subcluster population numerically dominating bacterioplankton of a freshwater pond. Applied and Environmental Microbiology 71: 4539–4547.

    Article  CAS  Google Scholar 

  • Hahn, M. W., E. Lang, U. Brandt & C. Spröer, 2011. Polynucleobacter acidiphobus sp. nov., a representative of an abundant group of planktonic freshwater bacteria. International Journal of Systematic and Evolutionary Microbiology 61: 788–794.

    Article  CAS  Google Scholar 

  • Hama, T., N. Handa & J. Hama, 1987. Determination of amino acid production rate of a marine phytoplankton population with 13C and gas chromatography-mass spectrometryl. Limnology and Oceanography 32: 1144–1153.

    Article  CAS  Google Scholar 

  • Höfle, M. G., H. Haas & K. Dominik, 1999. Seasonal dynamics of bacterioplankton community structure in a eutrophic lake as determined by 5S rRNA analysis. Applied and Environmental Microbiology 65: 3164–3174.

    PubMed  PubMed Central  Google Scholar 

  • Huisman, J., R. R. Jonker, C. Zonneveld & F. J. Weissing, 1999. Competition for light between phytoplankton species: experimental tests of mechanistic theory. Ecology 80: 211–222.

    Article  Google Scholar 

  • Jackson, D. A., 1995. PROTEST: a PROcrustean randomization TEST of community environment concordance. Ecoscience 2: 297–303.

    Article  Google Scholar 

  • Kent, A. D., A. C. Yannarell, J. A. Rusak, E. W. Triplett & K. D. McMahon, 2007. Synchrony in aquatic microbial community dynamics. The ISME Journal 1: 38–47.

    Article  CAS  Google Scholar 

  • Knoll, S., W. Zwisler & M. Simon, 2001. Bacterial colonization of early stages of limnetic diatom microaggregates. Aquatic Microbial Ecology 25: 141–150.

    Article  Google Scholar 

  • Langenheder, S. & K. Jürgens, 2001. Regulation of bacterial biomass and community structure by metazoan and protozoan predation. Limnology and Oceanography 46: 121–134.

    Article  Google Scholar 

  • Legendre, P. & L. Legendre, 1998. Numerical Ecology. Elsevier Science BV, Amsterdam.

    Google Scholar 

  • Legendre, P. & E. Gallagher, 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271–280.

    Article  Google Scholar 

  • Lindström, E. S., 2000. Bacterioplankton community composition in five lakes differing in trophic status and humic content. Microbial Ecology 40: 104–113.

    PubMed  Google Scholar 

  • Lindström, E. S., M. P. Kamst-Van Agterveld & G. Zwart, 2005. Distribution of typical freshwater bacterial groups is associated with pH, temperature and lake water retention time. Applied and Environmental Microbiology 71: 8201–8206.

    Article  Google Scholar 

  • Lumley, T., 2017. leaps: Regression subset selection. R package version 3.0 (based on Fortran code by Alan Miller). https://CRAN.R-project.org/package=leaps.

  • Manz, W., R. Amann, W. Ludwig, M. Wagner & K. H. Schleifer, 1992. Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Systematic Applied Microbiology 15: 593–600.

    Article  Google Scholar 

  • Manz, W., R. Amann, W. Ludwig, M. Vancanneyt & K. H. Schleifer, 1996. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga–Flavobacter–Bacteroides in the natural environment. Microbiology 142: 1097–1106.

    Article  CAS  Google Scholar 

  • Matz, C. & K. Jürgens, 2003. Interaction of nutrient limitation and protozoan grazing determines the phenotypic composition of a bacterial community. Microbial Ecology 45: 384–398.

    Article  CAS  Google Scholar 

  • Morabito, G. & A. Pugnetti, 2000. Primary productivity and related variables in the course of the trophic evolution of Lake Maggiore. Verhandlungen des Internationalen Verein Limnologie 27: 2934–2937.

    CAS  Google Scholar 

  • Neef, A., 1997. Anwendung der in situ-Einzelzell-Identifizierung von Bakterien zur Populations analyse in komplexen mikrobiellen Biozönosen. Thesis, Univ. Munich.

  • Newton, R. J., S. E. Jones, A. Eiler, K. D. McMahon & S. Bertilsson, 2011. A guide to the natural history of freshwater lake bacteria. Microbiology and Molecular Biology Reviews 75: 14–49.

    Article  CAS  Google Scholar 

  • Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H., Stevens, E. Szoecs, & H. Wagner, 2016. Vegan: Community Ecology Package. https://cran.r-project.org/web/packages/vegan/index.html.

  • Parveen, B., J. P. Reveilliez, I. Mary, V. Ravet, G. le Bronner, F. Mangot, I. Domaizon & D. Debroas, 2011. Diversity and dynamics of free-living and particle-associated Betaproteobacteria and Actinobacteria in relation to phytoplankton and zooplankton communities. FEMS Microbiology Ecology 77: 461–476.

    Article  CAS  Google Scholar 

  • Pernthaler, J., 2005. Predation on prokaryotes in the water column and its ecological implications. Nature Reviews Microbiology 3: 537–546.

    Article  CAS  Google Scholar 

  • Pernthaler, A., J. Pernthaler & R. Amann, 2004. Sensitive multi-color fluorescence in situ hybridization for the identification of environmental microorganisms. In Akkermans, A. D. L., F. J. de Bruijn & J. D. van Elsas (eds), Molecular Microbial Ecology Manual, 2nd ed. Kluwer Academic Publishers, Dordrecht, The Netherlands: 711–726.

    Google Scholar 

  • Porter, K. G. & Y. S. Feig, 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25: 943–948.

    Article  Google Scholar 

  • R Core Team, 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.

  • Reynolds, C. S., 2006. The Ecology of Phytoplankton. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Riemann, L. & A. Winding, 2001. Community dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom. Microbial Ecology 42: 274–285.

    Article  CAS  Google Scholar 

  • Roller, C., M. Wagner, R. Amann, W. Ludwig & K. H. Schleifer, 1994. In situ probing of Gram-positive bacteria with high DNA G + C content using 23S rRNA targeted oligonucleotides. Microbiology 140: 2849–2858.

    Article  CAS  Google Scholar 

  • Rott, E., N. Salmaso & E. Hoehn, 2007. Quality control of Utermöhl-based phytoplankton counting and biovolume estimates—an easy task or a Gordian knot? Hydrobiologia 578: 141–146.

    Article  Google Scholar 

  • Salcher, M. M., J. Hofer, K. Horňák, J. Jezbera, B.- Sonntag, J. Vrba, K. Šimek & T. Posch, 2007. Modulation of microbial predator-prey dynamics by phosphorus availability: growth patterns and survival strategies of bacterial phylogenetic clades. FEMS Microbiology Ecology 60: 40–50.

    Article  CAS  Google Scholar 

  • Salcher, M. M., J. Pernthaler, M. Zeder, R. Psenner & T. Posch, 2008. Spatio-temporal niche separation of planktonic Betaproteobacteria in an oligo-mesotrophic lake. Environmental Microbiology 10: 2074–2086.

    Article  CAS  Google Scholar 

  • Salcher, M. M., J. Pernthaler, N. Frater & T. Posch, 2011a. Vertical and longitudinal distribution patterns of different bacterioplankton populations in a canyon-shaped, deep prealpine lake. Limnology and Oceanography 56: 2017–2039.

    Article  Google Scholar 

  • Salcher, M. M., J. Pernthaler & T. Posch, 2011b. Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria “that rule the waves” (LD12). The ISME Journal 5: 1242–1252.

    Article  CAS  Google Scholar 

  • Salcher, M. M., T. Posch & J. Pernthaler, 2013. In situ substrate preferences of abundant bacterioplankton populations in a prealpine freshwater lake. The ISME Journal 7: 896–907.

    Article  CAS  Google Scholar 

  • Salmaso, N., 2002. Ecological patterns of phytoplankton assemblages in Lake Garda: seasonal, spatial and historical features. Journal of Limnology 61: 95–115.

    Article  Google Scholar 

  • Salmaso, N. & R. Mosello, 2010. Limnological research in the deep southern subalpine lakes: synthesis, directions and perspectives. Advances in Oceanography and Limnology 1: 29–66.

    Article  CAS  Google Scholar 

  • Salmaso, N., G. Morabito, R. Mosello, L. Garibaldi, M. Simona, F. Buzzi & D. Ruggiu, 2003. A synoptic study of phytoplankton in the deep lakes south of the Alps (lakes Garda, Iseo, Como, Lugano and Maggiore). Journal of Limnology 62: 207–227.

    Article  Google Scholar 

  • Salmaso, N., F. Buzzi, L. Garibaldi, G. Morabito & M. Simona, 2012. Effects of nutrient availability and temperature on phytoplankton development: a case study from large lakes south of the Alps. Aquatic Science 74: 555–570.

    Article  CAS  Google Scholar 

  • Salmaso, N., C. Capelli, S. Shams & L. Cerasino, 2015. Expansion of bloom-forming Dolichospermum lemmermannii (Nostocales, Cyanobacteria) to the deep lakes south of the Alps: colonization patterns, driving forces and implications for water use. Harmful Algae 50: 76–87.

    Article  CAS  Google Scholar 

  • Salmaso, N., D. Albanese, C. Capelli, A. Boscaini, M. Pindo & C. Donati, 2017. Diversity and cyclical seasonal transitions in the bacterial community in a large and deep perialpine lake. Microbial Ecology. Springer US, 1 December, 1–19. https://doi.org/10.1007/s00248-017-1120-x.

    Article  Google Scholar 

  • Sarmento, H. & J. M. Gasol, 2012. Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. Environmental Microbiology 14: 2348–2360.

    Article  CAS  Google Scholar 

  • Schellenberger, S., H. L. Drake & S. Kolb, 2011. Functionally redundant cellobiose-degrading soil bacteria respond differentially to oxygen. Applied and Environmental Microbiology 77: 6043–6048.

    Article  CAS  Google Scholar 

  • Schiaffino, M. R., M. L. Sánchez, M. Gerea, F. Unrein, V. Balague, J. M. Gasol & I. Izaguirre, 2016. Distribution patterns of the abundance of major bacterial and archaeal groups in Patagonian lakes. Journal of Plankton Research 1: 64–82.

    Article  Google Scholar 

  • Schwenk, D., L. Nohynek & H. Rischer, 2014. Algae–bacteria association inferred by 16S rDNA similarity in established microalgae cultures. MicrobiologyOpen 3: 356–368.

    Article  CAS  Google Scholar 

  • Simona, M., 2003. Winter and spring mixing depths affect the trophic status and composition of phytoplankton in the northern meromictic basin of Lake Lugano. Journal of Limnology 62: 190–206.

    Article  Google Scholar 

  • Smith, E. M. & Y. T. Prairie, 2004. Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnology and Oceanography 49: 137–147.

    Article  CAS  Google Scholar 

  • Sorokin, D. Y. & J. G. Kuenen, 2005. Chemolithotrophic haloalkaliphiles from soda lakes. FEMS Microbiology Ecology 52: 287–295.

    Article  CAS  Google Scholar 

  • Stahl, D. A. & R. Amann, 1991. Development and application of nucleic acid probes. In Stackebrandt, E. & M. Goodfellow (eds), Nucleic Acid Techniques in Bacterial Sytematics. Wiley, Chichester: 205–248.

    Google Scholar 

  • Stefani, F., F. Salerno, D. Copetti, D. Rabuffetti, L. Guidetti, G. Torri, A. Naggi, M. Lacomini, G. Morabito & L. Guzzella, 2016. Endogenous origin of foams in lakes: a long-term analysis for Lake Maggiore (northern Italy). Hydrobiologia 767: 249–265.

    Article  CAS  Google Scholar 

  • Stoeckel, D. M. & V. J. Harwood, 2007. Performance, design, and analysis in microbial source tracking studies. Applied and Environmental Microbiology 73: 2405–2415.

    Article  CAS  Google Scholar 

  • Taipale, S., R. I. Jones & M. Tiirola, 2009. Vertical diversity of bacteria in an oxygen-stratified humic lake, evaluated using DNA and phospholipid analyses. Aquatic Microbial Ecology 55: 1–16.

    Article  Google Scholar 

  • Tapolczai, K., O. Anneville, J. Padisák, N. Salmaso, G. Morabito, T. Zohary, R. D. Tadonléké & F. Rimet, 2015. Occurrence and mass development of Mougeotia spp. (Zygnemataceae) in large, deep lakes. Hydrobiologia 745: 17–29.

    Article  CAS  Google Scholar 

  • Teeling, H., B. M. Fuchs, D. Becher, Ch Klockow, A. Gardebrecht, Ch M Bennke, M. Kassabgy, S. Huang, A. J. Mann, J. Waldmann, M. Weber, A. Klindworth, A. Otto, J. Lange, J. Bernhardt, Ch Reinsch, M. Hecker, J. Peplies, F. D. Bockelmann, U. Callies, G. Gerdts, A. Wichels, K. H. Wiltshire, F. O. Glöckner, T. Schweder & R. Amann, 2012. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336: 608–611.

    Article  CAS  Google Scholar 

  • Teeling, H., B. M. Fuchs, Ch M Bennke, K. Krüger, M. Chafee, L. Kappelmann, G. Reintjes, J. Waldmann, Ch Quast, F. O. Glöckner, J. Lucas, A. Wichels, G. Gerdts, K. H. Wiltshire & R. I. Amann, 2016. Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms. eLife 5: 1–31.

    Article  Google Scholar 

  • Teira, E., T. Reinthaler, A. Pernthaler, J. Pernthaler & G. J. Herndl, 2004. Combining catalyzed reported deposition-fluorescence in situ hybridization and automicrography to detect substrate utilization by Bacteria and Archaea in the deep ocean. Applied and Environmental Microbiology 70: 4411–4414.

    Article  CAS  Google Scholar 

  • Ter Braak, C. J. F., 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167–1179.

    Article  Google Scholar 

  • Thingstad, T. F., L. Øvreås, J. K. Egge, T. Lovdal & M. Heldal, 2005. Use of non-limiting substrates to increase size: a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs? Ecology Letters 8: 675–682.

    Article  Google Scholar 

  • Utermöhl, H., 1958. Zur Vervollkommung der quantitative phytoplankton methodik. Mitt Verhandlungen des Internationalen Verein Limnologie 9: 1–38.

    Google Scholar 

  • Wallner, G., R. Amann & W. Beisker, 1993. Optimizing fluorescent in situ hybridization with rRNA targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14: 136–143.

    Article  CAS  Google Scholar 

  • Weiss, P., B. Schweitzer, R. Amann & M. Simon, 1996. Identification in situ and dynamics of bacteria on limnetic organic aggregates (lake snow). Applied and Environmental Microbiology 62: 1998–2005.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, Q. L. & M. W. Hahn, 2006. High predictability of the seasonal dynamics of a species-like Polynucleobacter population in a freshwater lake. Environmental Microbiology 8: 1660–1666.

    Article  CAS  Google Scholar 

  • Yannarell, A. C. & E. W. Triplett, 2004. Within- and between-lake variability in the composition of bacterioplankton communities: investigations using multiple spatial scales. Applied and Environmental Microbiology 70: 214–223.

    Article  CAS  Google Scholar 

  • Zhong, Z. P., Y. Liu, L. L. Miao, F. Wang, L. M. Chu, J. L. Wang & Z. P. Liu, 2016. Prokaryotic community structure driven by salinity and ionic concentrations in plateau lakes of the Tibetan Plateau. Applied and Environmental Microbiology 82: 1846–1858.

    Article  CAS  Google Scholar 

  • Zuur, A., E. N. Ieno & M. Smith, 2007. Analyzing Ecological Data. Springer, New York: 672.

    Book  Google Scholar 

  • Zwart, G., B. C. Crump, M. P. Kamst-van Agterveld, F. Hagen & S.-K. Han, 2002. Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquatic Microbial Ecology 28: 141–155.

    Article  Google Scholar 

Download references

Acknowledgements

The research project was the result of the collaboration of Italian, Swiss, and Mexican Institutions. Bacterial analyses were performed at the Institute of Ecosystem Study (ISE), CNR, Italy and supported by the CIPAIS project (C.Callieri). Phytoplankton analyses were performed by the authors in all the different Institutions. The sabbatical research stay of the first author in the MEG Laboratory at ISE-CNR of Verbania, Italy was supported by PASPA DGAPA-UNAM grant, Mexico.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Salvador Hernández-Avilés.

Additional information

Guest editors: Nico Salmaso, Orlane Anneville, Dietmar Straile & Pierluigi Viaroli / Large and deep perialpine lakes: ecological functions and resource management

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 160 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hernández-Avilés, J.S., Callieri, C., Bertoni, R. et al. Prokaryoplankton and phytoplankton community compositions in five large deep perialpine lakes. Hydrobiologia 824, 71–92 (2018). https://doi.org/10.1007/s10750-018-3586-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3586-z

Keywords

Navigation