Synchrony of Eukaryotic and Prokaryotic Planktonic Communities in Three Seasonally Sampled Austrian Lakes

Freshwater systems are characterized by an enormous diversity of eukaryotic protists and prokaryotic taxa. The community structures in different lakes are thereby influenced by factors such as habitat size, lake chemistry, biotic interactions, and seasonality. In our study, we used high throughput 454 sequencing to study the diversity and temporal changes of prokaryotic and eukaryotic planktonic communities in three Austrian lakes during the ice-free season. In the following year, one lake was sampled again with a reduced set of sampling dates to observe reoccurring patterns. Cluster analyses (based on SSU V9 (eukaryotic) and V4 (prokaryotic) OTU composition) grouped samples according to their origin followed by separation into seasonal clusters, indicating that each lake has a unique signature based on OTU composition. These results suggest a strong habitat-specificity of microbial communities and in particular of community patterns at the OTU level. A comparison of the prokaryotic and eukaryotic datasets via co-inertia analysis (CIA) showed a consistent clustering of prokaryotic and eukaryotic samples, probably reacting to the same environmental forces (e.g., pH, conductivity). In addition, the shifts in eukaryotic and bacterioplanktonic communities generally occurred at the same time and on the same scale. Regression analyses revealed a linear relationship between an increase in Bray–Curtis dissimilarities and elapsed time. Our study shows a pronounced coupling between bacteria and eukaryotes in seasonal samplings of the three analyzed lakes. However, our temporal resolution (biweekly sampling) and data on abiotic factors were insufficient to determine if this was caused by direct biotic interactions or by reacting to the same seasonally changing environmental forces.

[1]  J. Boenigk,et al.  Cryptophyta as major bacterivores in freshwater summer plankton , 2018, The ISME Journal.

[2]  C. Bock,et al.  Geographic distance and mountain ranges structure freshwater protist communities on a European scalе , 2018 .

[3]  J. Pernthaler,et al.  Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria , 2017, The ISME Journal.

[4]  H. Grossart,et al.  Strain‐specific consumption and transformation of alga‐derived dissolved organic matter by members of the Limnohabitans‐C and Polynucleobacter‐B clusters of Betaproteobacteria , 2017, Environmental microbiology.

[5]  O. Köster,et al.  Abrupt stop of deep water turnover with lake warming: Drastic consequences for algal primary producers , 2017, Scientific Reports.

[6]  A. Dupont.  Predator control of diversity: case studies using microcosms , 2017 .

[7]  J. Pernthaler.  Competition and niche separation of pelagic bacteria in freshwater habitats , 2017, Environmental microbiology.

[8]  R. Knight,et al.  Bacterial Community Composition and Dynamics Spanning Five Years in Freshwater Bog Lakes , 2017, mSphere.

[9]  J. Pernthaler,et al.  Distribution and ecological preferences of the freshwater lineage LimA (genus Limnohabitans) revealed by a new double hybridization approach , 2017, Environmental microbiology.

[10]  Y. Okazaki,et al.  Vertical partitioning of freshwater bacterioplankton community in a deep mesotrophic lake with a fully oxygenated hypolimnion (Lake Biwa, Japan). , 2016, Environmental microbiology reports.

[11]  R. Sommaruga,et al.  Phosphate and ATP uptake by lake bacteria: does taxonomical identity matter? , 2016, Environmental microbiology.

[12]  J. Beman,et al.  Microbial diversity and community structure along a lake elevation gradient in Yosemite National Park, California, USA. , 2016, Environmental microbiology.

[13]  R. Sommaruga,et al.  Microbial eukaryote plankton communities of high‐mountain lakes from three continents exhibit strong biogeographic patterns , 2016, Molecular ecology.

[14]  V. Denef,et al.  Seasonal Succession Leads to Habitat-Dependent Differentiation in Ribosomal RNA:DNA Ratios among Freshwater Lake Bacteria , 2016, Front. Microbiol..

[15]  M. Hahn,et al.  Complete ecological isolation and cryptic diversity in Polynucleobacter bacteria not resolved by 16S rRNA gene sequences , 2016, The ISME Journal.

[16]  Dominik Heider,et al.  Protistan community analysis: key findings of a large-scale molecular sampling , 2016, The ISME Journal.

[17]  D. Torrents,et al.  Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria , 2016, The ISME Journal.

[18]  H. Peter,et al.  Shifts in diversity and function of lake bacterial communities upon glacier retreat , 2016, The ISME Journal.

[19]  B. Neilan,et al.  Microbial communities reflect temporal changes in cyanobacterial composition in a shallow ephemeral freshwater lake , 2015, The ISME Journal.

[20]  Yunfeng Yang,et al.  Annual periodicity in planktonic bacterial and archaeal community composition of eutrophic Lake Taihu , 2015, Scientific Reports.

[21]  Lemian Liu,et al.  Phytoplankton Communities Exhibit a Stronger Response to Environmental Changes than Bacterioplankton in Three Subtropical Reservoirs. , 2015, Environmental science & technology.

[22]  J. Pernthaler,et al.  Ecology and Distribution of Thaumarchaea in the Deep Hypolimnion of Lake Maggiore , 2015, Archaea.

[23]  J. Pernthaler,et al.  The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign , 2015, The ISME Journal.

[24]  T. Nõges,et al.  Contrasting seasonal and interannual environmental drivers in bacterial communities within a large shallow lake: evidence from a seven year survey , 2015 .

[25]  Nicholas D. Youngblut,et al.  Phytoplankton succession affects the composition of Polynucleobacter subtypes in humic lakes. , 2015, Environmental microbiology.

[26]  J. Pernthaler,et al.  Seasonal growth potential of rare lake water bacteria suggest their disproportional contribution to carbon fluxes. , 2015, Environmental microbiology.

[27]  P. Servais,et al.  Bacterial Community Composition in Three Freshwater Reservoirs of Different Alkalinity and Trophic Status , 2014, PloS one.

[28]  R. Amann,et al.  Massive Regime Shifts and High Activity of Heterotrophic Bacteria in an Ice-Covered Lake , 2014, PloS one.

[29]  Frédéric Mahé,et al.  Swarm: robust and fast clustering method for amplicon-based studies , 2014, PeerJ.

[30]  Petr Znachor,et al.  A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring , 2014 .

[31]  W. Doolittle,et al.  Rhodoluna lacicola gen. nov., sp. nov., a planktonic freshwater bacterium with stream-lined genome , 2014, International journal of systematic and evolutionary microbiology.

[32]  S. Barcikowski,et al.  Effects of Silver Nitrate and Silver Nanoparticles on a Planktonic Community: General Trends after Short-Term Exposure , 2014, PloS one.

[33]  C. Bock,et al.  Seasonal variation of planktonic chrysophytes with special focus on Dinobryon , 2014 .

[34]  Austin G. Davis-Richardson,et al.  Interactions between specific phytoplankton and bacteria affect lake bacterial community succession. , 2013, Environmental microbiology.

[35]  M. Salcher.  Same same but different: ecological niche partitioning of planktonic freshwater prokaryotes , 2013 .

[36]  D. Bass,et al.  Differential freshwater flagellate community response to bacterial food quality with a focus on Limnohabitans bacteria , 2013, The ISME Journal.

[37]  T. Williams,et al.  The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. , 2013, Environmental microbiology.

[38]  Stéphane Audic,et al.  The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy , 2012, Nucleic Acids Res..

[39]  Y. Okazaki,et al.  Seasonal dominance of CL500-11 bacterioplankton (phylum Chloroflexi) in the oxygenated hypolimnion of Lake Biwa, Japan. , 2013, FEMS microbiology ecology.

[40]  Miquel Lürling,et al.  Beyond the Plankton Ecology Group (PEG) Model : Mechanisms Driving Plankton Succession , 2012 .

[41]  R. Stocker.  Marine Microbes See a Sea of Gradients , 2012, Science.

[42]  Oliver Köster,et al.  Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming , 2012 .

[43]  J. Spouge,et al.  CBOL Protist Working Group: Barcoding Eukaryotic Richness beyond the Animal, Plant, and Fungal Kingdoms , 2012, PLoS biology.

[44]  A. Eiler,et al.  Bacterial and Phytoplankton Responses to Nutrient Amendments in a Boreal Lake Differ According to Season and to Taxonomic Resolution , 2012, PloS one.

[45]  R. Amann,et al.  Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom , 2012, Science.

[46]  W. Granéli,et al.  Bacterial and phytoplankton nutrient limitation in tropical marine waters, and a coastal lake in Brazil , 2012 .

[47]  J. Pernthaler,et al.  Rapid successions affect microbial N-acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom. , 2012, Environmental microbiology.

[48]  S. Langenheder,et al.  Local and regional factors influencing bacterial community assembly. , 2012, Environmental microbiology reports.

[49]  Stefan Bertilsson,et al.  Coherent dynamics and association networks among lake bacterioplankton taxa , 2011, The ISME Journal.

[50]  K. Šimek,et al.  Alga-Derived Substrates Select for Distinct Betaproteobacterial Lineages and Contribute to Niche Separation in Limnohabitans Strains , 2011, Applied and Environmental Microbiology.

[51]  J. Pernthaler,et al.  Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria ‘that rule the waves’ (LD12) , 2011, The ISME Journal.

[52]  Rob Knight,et al.  UCHIME improves sensitivity and speed of chimera detection , 2011, Bioinform..

[53]  Craig E. Nelson,et al.  Differential Response of High-Elevation Planktonic Bacterial Community Structure and Metabolism to Experimental Nutrient Enrichment , 2011, PloS one.

[54]  Katherine D. McMahon,et al.  A Guide to the Natural History of Freshwater Lake Bacteria , 2011, Microbiology and Molecular Reviews.

[55]  Pierre Legendre,et al.  Numerical Ecology with R , 2011 .

[56]  T. Bruns,et al.  Quantifying microbial communities with 454 pyrosequencing: does read abundance count? , 2010, Molecular ecology.

[57]  David P. Hamilton,et al.  Nitrogen and Phosphorus Limitation of Phytoplankton Growth in New Zealand Lakes: Implications for Eutrophication Control , 2010, Ecosystems.

[58]  Sandra Martínez-García,et al.  Effects of inorganic and organic nutrient inputs on bacterioplankton community composition along a latitudinal transect in the Atlantic Ocean , 2010 .

[59]  B. Ottenwälder,et al.  Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity , 2010, Molecular ecology.

[60]  Nico Salmaso,et al.  Long‐term phytoplankton community changes in a deep subalpine lake: responses to nutrient availability and climatic fluctuations , 2010 .

[61]  B. Ottenwälder,et al.  Diversity in a hidden world: potential and limitation of next‐generation sequencing for surveys of molecular diversity of eukaryotic microorganisms , 2010, Molecular ecology.

[62]  T. Stoeck,et al.  Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water , 2010, Molecular ecology.

[63]  Christian Schlötterer,et al.  CANGS: a user-friendly utility for processing and analyzing 454 GS-FLX data in biodiversity studies , 2010, BMC Research Notes.

[64]  X. Zhang,et al.  PCR‐DGGE Fingerprinting Analysis of Plankton Communities and Its Relationship to Lake Trophic Status , 2009 .

[65]  Michael Zeder,et al.  A small population of planktonic Flavobacteria with disproportionally high growth during the spring phytoplankton bloom in a prealpine lake. , 2009, Environmental microbiology.

[66]  Peng Xing,et al.  Low Taxon Richness of Bacterioplankton in High-Altitude Lakes of the Eastern Tibetan Plateau, with a Predominance of Bacteroidetes and Synechococcus spp , 2009, Applied and Environmental Microbiology.

[67]  E. Casamayor,et al.  Bacterial 'cosmopolitanism' and importance of local environmental factors for community composition in remote high-altitude lakes. , 2009, Freshwater biology.

[68]  Thomas M. Schmidt,et al.  rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea , 2008, Nucleic Acids Res..

[69]  J. Pernthaler,et al.  Microbial Food Webs , 2009 .

[70]  A. Kerkhoff,et al.  Microbes on mountainsides: Contrasting elevational patterns of bacterial and plant diversity , 2008, Proceedings of the National Academy of Sciences.

[71]  Michael Zeder,et al.  Spatio-temporal niche separation of planktonic Betaproteobacteria in an oligo-mesotrophic lake. , 2008, Environmental microbiology.

[72]  J. Hejzlar,et al.  Spatio-temporal patterns of bacterioplankton production and community composition related to phytoplankton composition and protistan bacterivory in a dam reservoir , 2008 .

[73]  H. Grossart,et al.  Top-down and bottom-up induced shifts in bacterial abundance, production and community composition in an experimentally divided humic lake. , 2008, Environmental microbiology.

[74]  Anne-Béatrice Dufour,et al.  The ade4 Package: Implementing the Duality Diagram for Ecologists , 2007 .

[75]  Jean Thioulouse,et al.  Interactive Multivariate Data Analysis in R with the ade4 and ade4TkGUI Packages , 2007 .

[76]  G. Casella,et al.  Pyrosequencing enumerates and contrasts soil microbial diversity , 2007, The ISME Journal.

[77]  K. McMahon,et al.  Synchrony in aquatic microbial community dynamics , 2007, The ISME Journal.

[78]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[79]  N. Salmaso,et al.  Morpho-Functional Groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany) , 2007, Hydrobiologia.

[80]  K. Šimek,et al.  Maximum growth rates and possible life strategies of different bacterioplankton groups in relation to phosphorus availability in a freshwater reservoir. , 2006, Environmental microbiology.

[81]  A. Andersson,et al.  Changes in the pelagic microbial food web due to artificial eutrophication , 2006, Aquatic Ecology.

[82]  H. Grossart,et al.  Diversity and Seasonal Dynamics of Actinobacteria Populations in Four Lakes in Northeastern Germany , 2006, Applied and Environmental Microbiology.

[83]  James H. Brown,et al.  Microbial biogeography: putting microorganisms on the map , 2006, Nature Reviews Microbiology.

[84]  S. Giovannoni,et al.  Bacterioplankton communities of Crater Lake, OR: dynamic changes with euphotic zone food web structure and stable deep water populations , 2006, Hydrobiologia.

[85]  J. Pernthaler.  Predation on prokaryotes in the water column and its ecological implications , 2005, Nature Reviews Microbiology.

[86]  D. Vaulot,et al.  Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. , 2005, FEMS microbiology ecology.

[87]  D. Caron,et al.  Protistan Diversity Estimates Based on 18S rDNA from Seawater Incubations in the Western North Atlantic 1 , 2005, The Journal of eukaryotic microbiology.

[88]  Eric W. Triplett,et al.  Geographic and Environmental Sources of Variation in Lake Bacterial Community Composition , 2005, Applied and Environmental Microbiology.

[89]  T. Cavalier-smith,et al.  Phylum-specific environmental DNA analysis reveals remarkably high global biodiversity of Cercozoa (Protozoa). , 2004, International journal of systematic and evolutionary microbiology.

[90]  Tamar Zohary,et al.  Changes to the phytoplankton assemblage of Lake Kinneret after decades of a predictable, repetitive pattern , 2004 .

[91]  Paul G. Falkowski,et al.  The Evolution of Modern Eukaryotic Phytoplankton , 2004, Science.

[92]  J. Boenigk,et al.  Bacterivory by heterotrophic flagellates: community structure and feeding strategies , 2002, Antonie van Leeuwenhoek.

[93]  T. Berman,et al.  Lake Kinneret phytoplankton: Stability and variability during twenty years (1970–1989) , 1992, Aquatic Sciences.

[94]  J. Banfield,et al.  Extremely Acidophilic Protists from Acid Mine Drainage Host Rickettsiales-Lineage Endosymbionts That Have Intervening Sequences in Their 16S rRNA Genes , 2003, Applied and Environmental Microbiology.

[95]  T. Stoeck,et al.  Novel Eukaryotic Lineages Inferred from Small-Subunit rRNA Analyses of Oxygen-Depleted Marine Environments , 2003, Applied and Environmental Microbiology.

[96]  O. Anneville,et al.  Long-term study (1974–1998) of seasonal changes in the phytoplankton in Lake Geneva: a multi-table approach , 2002 .

[97]  Purificación López-García,et al.  The molecular ecology of microbial eukaryotes unveils a hidden world. , 2002, Trends in microbiology.

[98]  D. Caron,et al.  Seasonal variation of phosphorus limitation of bacterial growth in a small lake , 2001 .

[99]  E. Triplett,et al.  Effects of Resources and Trophic Interactions on Freshwater Bacterioplankton Diversity , 2000, Microbial Ecology.

[100]  P. Falkowski,et al.  Biogeochemical Controls and Feedbacks on Ocean Primary Production , 1998, Science.

[101]  J. Randerson,et al.  Primary production of the biosphere: integrating terrestrial and oceanic components , 1998, Science.

[102]  N. Blackburn,et al.  Cycling of marine dissolved organic matter. II. A model analysis , 1996 .

[103]  K. Šimek,et al.  Ciliategrazing on picoplankton in a eutrophic reservoir during the summer phytoplankton maximum: A study at the species and community level , 1995 .

[104]  D. Caron,et al.  The contribution of microorganisms to particulate carbon and nitrogen in surface waters of the Sargasso Sea near Bermuda , 1995 .

[105]  M. Loeffelholz,et al.  PCR primers and probes for the 16S rRNA gene of most species of pathogenic bacteria, including bacteria found in cerebrospinal fluid , 1994, Journal of clinical microbiology.

[106]  Janet K. Thompson,et al.  Measurement of filtration rates by infaunal bivalves in a recirculating flume , 1992 .

[107]  Charles R. Goldman,et al.  Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America : a review and critique of experimental enrichments , 1990 .

[108]  F. Azam,et al.  Biogeochemical significance of bacterial biomass in the ocean's euphotic zone , 1990 .

[109]  B. Bowien.  Plankton Ecology , 1989, Brock/Springer Series in Contemporary Bioscience.

[110]  M. Sogin,et al.  The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. , 1988, Gene.

[111]  T. Hama,et al.  Pattern of organic matter production by natural phytoplankton population in a eutrophic lake 2. Extracellular products , 1987, Archiv für Hydrobiologie.

[112]  Ulrich Sommer,et al.  The PEG-model of seasonal succession of planktonic events in fresh waters , 1986, Archiv für Hydrobiologie.

[113]  J. G. Field,et al.  The Ecological Role of Water-Column Microbes in the Sea* , 1983 .

[114]  Jonathan J. Cole,et al.  INTERACTIONS BETWEEN BACTERIA AND ALGAE IN AQUATIC ECOSYSTEMS , 1982 .

[115]  P. Zahradník,et al.  Phosphorus and nitrogen , 1979 .

[116]  D. Schindler.  Evolution of phosphorus limitation in lakes. , 1977, Science.

[117]  L. Pomeroy.  The Ocean's Food Web, A Changing Paradigm , 1974 .

[118]  Ralph Mitchell,et al.  Studies in Bacterial Chemoreception. I. The Effect of Biogenic Amines and Cannabinoids on Bacterial Chemoreception. II. Chemotactic and Growth Responses of Marine Bacteria to Algal Extracellular Products. , 1972 .