Synchrony of Eukaryotic and Prokaryotic Planktonic Communities in Three Seasonally Sampled Austrian Lakes
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
29963032
PubMed Central
PMC6014231
DOI
10.3389/fmicb.2018.01290
Knihovny.cz E-zdroje
- Klíčová slova
- Seasonality, diversity, eukaryotic plankton, freshwater, prokaryotic plankton, protist,
- Publikační typ
- časopisecké články MeSH
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.
Biodiversity Faculty of Biology University of Duisburg Essen Essen Germany
Institut für Populationsgenetik Veterinärmedizinische Universität Wien Vienna Austria
Institute of Hydrobiology Biology Centre CAS České Budějovice Czechia
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Abell J. M., Ozkundakci D., Hamilton D. P. (2010). Nitrogen and phosphorus limitation of phytoplankton growth in New Zealand lakes: implications for eutrophication control. DOI
Allgaier M., Grossart H. (2006). Diversity and seasonal dynamics of PubMed DOI PMC
Amend A. S., Seifert K. A., Bruns T. D. (2010). Quantifying microbial communities with 454 pyrosequencing: does read abundance count? PubMed DOI
Andersson A., Samuelsson K., Haecky P., Albertsson J. (2006). Changes in the pelagic microbial food web due to artificial eutrophication. DOI
Anneville O., Ginot V., Druart J. C., Angeli N. (2002). Long-term study (1974-1998) of seasonal changes in the phytoplankton in Lake Geneva: a multi-table approach. DOI
Azam F., Fenchel T., Field J., Gray J., Meyer-Reil L., Thingstad T. (1983). The ecological role of water-column microbes in the Sea. DOI
Baker B. J., Hugenholtz P., Dawson S. C., Banfield J. F. (2003). Extremely acidophilic protists from acid mine drainage host rickettsiales-lineage endosymbionts that have intervening sequences in their 16s rRNA genes. PubMed DOI PMC
Bass D., Cavalier-Smith T. (2004). Phylum-specific environmental DNA analysis reveals remarkably high global biodiversity of Cercozoa (Protozoa). PubMed DOI
Bell W., Mitchell R. (1972). Chemotactic and growth response of marine bacteria to algal extracellular products. DOI
Berman T., Yacobi Y. Z., Pollingher U. (1992). Lake Kinneret phytoplankton - stability and variability during 20 years (1970-1989). DOI
Bižić-Ionescu M., Amann R., Grossart H.-P. (2014). Massive regime shifts and high activity of heterotrophic bacteria in an ice-covered lake. PubMed DOI PMC
Blackburn N., Zweifel U. L., Hagstrom A. (1996). Cycling of marine dissolved organic matter. 2. A model analysis. DOI
Bock C., Medinger R., Jost S., Psenner R., Boenigk J. (2014). Seasonal variation of planktonic chrysophytes with special focus on DOI
Boenigk J., Arndt H. (2002). Bacterivory by heterotrophic flagellates: community structure and feeding strategies. PubMed DOI
Boenigk J., Beisser D., Zimmermann S., Bock C., Jakobi J., Grabner D., et al. (2014). Effects of silver nitrate and silver nanoparticles on a planktonic community: general trends after short-term exposure. PubMed DOI PMC
Boenigk J., Wodniok S., Bock C., Beisser D., Hempel C., Grossmann L., et al. (2018). Geographic distance and mountain ranges structure freshwater protist communities on a European scalå.
Borcard D., Gillet F., Legendre P. (2011). DOI
Bryant J. A., Lamanna C., Morlon H., Kerkhoff A. J., Enquist B. J., Green J. L. (2008). Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. PubMed DOI PMC
Carlsson P., Caron D. A. (2001). Seasonal variation of phosphorus limitation of bacterial growth in a small lake. DOI
Carlsson P., Graneli E., Graneli W., Rodriguez E. G., De Carvalho W. F., Brutemark A., et al. (2012). Bacterial and phytoplankton nutrient limitation in tropical marine waters, and a coastal lake in Brazil. DOI
Caron D. A., Dam H. G., Kremer P., Lessard E. J., Madin L. P., Malone T. C., et al. (1995). The contribution of microorganisms to particulate carbon and nitrogen in surface waters of the Sargasso Sea near Bermuda. DOI
Cho B. C., Azam F. (1990). Biogeochemical significance of bacterial biomass in the oceans euphotic zone. DOI
Coci M., Odermatt N., Salcher M. M., Pernthaler J., Corno G. (2015). Ecology and distribution of Thaumarchaea in the deep hypolimnion of Lake Maggiore. PubMed DOI PMC
Cole B. E., Thompson J. K., Cloern J. E. (1992). Measurement of filtration rates by infaunal bivalves in a recirculating flume.
Cole J. J. (1982). Interactions between Bacteria and algae in aquatic ecosystems. DOI
Countway P. D., Gast R. J., Savai P., Caron D. A. (2005). Protistan diversity estimates based on 18S rDNA from seawater incubations in the western North Atlantic. PubMed DOI
Denef V. J., Fujimoto M., Berry M. A., Schmidt M. L. (2016). Seasonal succession leads to habitat-dependent differentiation in ribosomal RNA:DNA ratios among freshwater lake bacteria. PubMed DOI PMC
Dray S., Dufour A. B. (2007). The ade4 package: implementing the duality diagram for ecologists. DOI
Dupont A. (2016).
Eckert E. M., Salcher M. M., Posch T., Eugster B., Pernthaler J. (2012). Rapid successions affect microbial N-acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom. PubMed DOI
Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. PubMed DOI PMC
Eiler A., Heinrich F., Bertilsson S. (2012). Coherent dynamics and association networks among lake bacterioplankton taxa. PubMed DOI PMC
Eiler A., Mondav R., Sinclair L., Fernandez-Vidal L., Scofield D. G., Schwientek P., et al. (2016). Tuning fresh: radiation through rewiring of central metabolism in streamlined bacteria. PubMed DOI PMC
Elser J. J., Marzolf E. R., Goldman C. R. (1990). Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: a review and critique of experimental enrichments. DOI
Falkowski P. G., Barber R. T., Smetacek V. (1998). Biogeochemical controls and feedbacks on ocean primary production. PubMed DOI
Falkowski P. G., Katz M. E., Knoll A. H., Quigg A., Raven J. A., Schofield O., et al. (2004). The evolution of modern eukaryotic phytoplankton. PubMed DOI
Field C. B., Behrenfeld M. J., Randerson J. T., Falkowski P. (1998). Primary production of the biosphere: integrating terrestrial and oceanic components. PubMed DOI
Filker S., Sommaruga R., Vila I., Stoeck T. (2016). Microbial eukaryote plankton communities of high-mountain lakes from three continents exhibit strong biogeographic patterns. PubMed DOI PMC
Fisher M. M., Klug J. L., Lauster G., Newton M., Triplett E. W. (2000). Effects of resources and trophic interactions on freshwater bacterioplankton diversity. PubMed
Greisen K., Loeffelholz M., Purohit A., Leong D. (1994). PCR primers and probes for the 16S rRNA gene of most species of pathogenic bacteria, including bacteria found in cerebrospinal fluid. PubMed PMC
Grossart H. P., Jezbera J., Horòák K., Hutalle K. M. L., Buck U., Šimek K. (2008). Top-down and bottom-up induced shifts in bacterial abundance, production and community composition in an experimentally divided humic lake. PubMed DOI
Grossmann L., Jensen M., Heider D., Jost S., Glucksman E., Hartikainen H., et al. (2016). Protistan community analysis: key findings of a large-scale molecular sampling. PubMed DOI PMC
Grujcic V., Nuy J. K., Salcher M. M., Shabarova T., Kasalicky V., Boenigk J., et al. (2018). Cryptophyta as major bacterivores in freshwater summer plankton. PubMed DOI PMC
Guillou L., Bachar D., Audic S., Bass D., Berney C., Bittner L., et al. (2013). The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. PubMed DOI PMC
Hahn M. W., Jezberova J., Koll U., Saueressig-Beck T., Schmidt J. (2016). Complete ecological isolation and cryptic diversity in PubMed DOI PMC
Hahn M. W., Schmidt J., Taipale S. J., Doolittle W. F., Koll U. (2014). PubMed DOI PMC
Hama T., Handa N. (1987). Pattern of organic-matter production by natural phytoplankton population in a eutrophic lake. 2. Extracellular products.
Hayden C. J., Beman J. M. (2016). Microbial diversity and community structure along a lake elevation gradient in Yosemite National Park, California, USA. PubMed DOI
Horňák K., Kasalickı V., Šimek K., Grossart H.-P. (2017). Strain-specific consumption and transformation of alga-derived dissolved organic matter by members of the PubMed DOI
Kent A. D., Yannarell A. C., Rusak J. A., Triplett E. W., Mcmahon K. D. (2007). Synchrony in aquatic microbial community dynamics. PubMed DOI
Landesregierung A. D. O. (2009). Gewässerschutzberich 43, seenaufsicht in Oberösterreich.
Lee Z. M. P., Bussema C., Schmidt T. M. (2009). rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. PubMed DOI PMC
Li J., Zhang J., Liu L., Fan Y., Li L., Yang Y., et al. (2015). Annual periodicity in planktonic bacterial and archaeal community composition of eutrophic Lake Taihu. PubMed DOI PMC
Lindstrom E. S., Langenheder S. (2012). Local and regional factors influencing bacterial community assembly. PubMed DOI
Linz A. M., Crary B. C., Shade A., Owens S., Gilbert J. A., Knight R., et al. (2017). Bacterial community composition and dynamics spanning five years in freshwater bog lakes. PubMed PMC
Liu L. M., Yang J., Lv H., Yu X. Q., Wilkinson D. M. (2015). Phytoplankton communities exhibit a stronger response to environmental changes than bacterioplankton in three subtropical reservoirs. PubMed DOI
Llirós M., Inceoǧlu Ö., García-Armisen T., Anzil A., Leporcq B., Pigneur L.-M., et al. (2014). Bacterial community composition in three freshwater reservoirs of different alkalinity and trophic status. PubMed DOI PMC
Mahé F., Rognes T., Quince C., De Vargas C., Dunthorn M. (2014). Swarm: robust and fast clustering method for amplicon-based studies. PubMed DOI PMC
Martiny J. B. H., Bohannan B. J. M., Brown J. H., Colwell R. K., Fuhrman J. A., Green J. L., et al. (2006). Microbial biogeography: putting microorganisms on the map. PubMed DOI
Medinger R., Nolte V., Pandey R. V., Jost S., Ottenwaelder B., Schloetterer C., et al. (2010). Diversity in a hidden world: potential and limitation of next-generation sequencing for surveys of molecular diversity of eukaryotic microorganisms. PubMed DOI PMC
Medlin L., Elwood H. J., Stickel S., Sogin M. L. (1988). The characterization of enzymatically amplified eukaryotic 16s-like rRNA-coding regions. PubMed DOI
Moreira D., López-Garciá P. (2002). The molecular ecology of microbial eukaryotes unveils a hidden world. PubMed DOI
Nelson C. E., Carlson C. A. (2011). Differential response of high-elevation planktonic bacterial community structure and metabolism to experimental nutrient enrichment. PubMed DOI PMC
Neuenschwander S. M., Ghai R., Pernthaler J., Salcher M. M. (2018). Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria. PubMed DOI PMC
Neuenschwander S. M., Pernthaler J., Posch T., Salcher M. M. (2015). Seasonal growth potential of rare lake water bacteria suggest their disproportional contribution to carbon fluxes. PubMed DOI
Newton R. J., Jones S. E., Eiler A., Mcmahon K. D., Bertilsson S. (2011). A guide to the natural history of freshwater lake bacteria. PubMed DOI PMC
Nolte V., Pandey R. V., Jost S., Medinger R., Ottenwaelder B., Boenigk J., et al. (2010). Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. PubMed DOI PMC
Okazaki Y., Hodoki Y., Nakano S.-I. (2013). Seasonal dominance of CL500-11 bacterioplankton (Phylum PubMed DOI
Okazaki Y., Nakano S.-I. (2016). Vertical partitioning of freshwater bacterioplankton community in a deep mesotrophic lake with a fully oxygenated hypolimnion (Lake Biwa, Japan). PubMed DOI
Oksanen J. (2015).
Oksanen J., Blanchet F. G., Kindt R., Legendre P., O’hara R. B., Simpson G. L., et al. (2011).
Pandey R. V., Nolte V., Schlotterer C. (2010). CANGS: a user-friendly utility for processing and analyzing 454 GS-FLX data in biodiversity studies. PubMed DOI PMC
Paver S. F., Hayek K. R., Gano K. A., Fagen J. R., Brown C. T., Davis-Richardson A. G., et al. (2013). Interactions between specific phytoplankton and bacteria affect lake bacterial community succession. PubMed DOI
Paver S. F., Youngblut N. D., Whitaker R. J., Kent A. D. (2015). Phytoplankton succession affects the composition of Polynucleobacter subtypes in humic lakes. PubMed DOI
Pawlowski J., Audic S., Adl S., Bass D., Belbahri L., Berney C., et al. (2012). CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PubMed DOI PMC
Pernthaler J. (2005). Predation on prokaryotes in the water column and its ecological implications. PubMed DOI
Pernthaler J. (2017). Competition and niche separation of pelagic bacteria in freshwater habitats. PubMed DOI
Pernthaler J., Posch T. (2009). “Microbial food webs,” in DOI
Peter H., Sommaruga R. (2016). Shifts in diversity and function of lake bacterial communities upon glacier retreat. PubMed DOI PMC
Peura S., Eiler A., Hiltunen M., Nykänen H., Tiirola M., Jones R. I. (2012). Bacterial and phytoplankton responses to nutrient amendments in a boreal lake differ according to season and to taxonomic resolution. PubMed DOI PMC
Pomeroy L. R. (1974). Oceans food web, a changing paradigm. DOI
Posch T., Koster O., Salcher M. M., Pernthaler J. (2012). Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming. DOI
Roesch L. F., Fulthorpe R. R., Riva A., Casella G., Hadwin A. K. M., Kent A. D., et al. (2007). Pyrosequencing enumerates and contrasts soil microbial diversity. PubMed DOI PMC
Rofner C., Sommaruga R., Teresa Pérez M. (2016). Phosphate and ATP uptake by lake bacteria: does taxonomical identity matter? PubMed DOI PMC
Salcher M. M. (2014). Same same but different: ecological niche partitioning of planktonic freshwater prokaryotes.
Salcher M. M., Neuenschwander S. M., Posch T., Pernthaler J. (2015). The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign. PubMed DOI PMC
Salcher M. M., Pernthaler J., Posch T. (2011). Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria ’that rule the waves’ (LD12). PubMed DOI PMC
Salcher M. M., Pernthaler J., Zeder M., Psenner R., Posch T. (2008). Spatio-temporal niche separation of planktonic Betaproteobacteria in an oligo-mesotrophic lake. PubMed DOI
Salmaso N. (2010). Long-term phytoplankton community changes in a deep subalpine lake: responses to nutrient availability and climatic fluctuations. DOI
Salmaso N., Padisak J. (2007). Morpho-functional groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany). DOI
Schindler D. W. (1977). Evolution of phosphorous limitation in lakes. PubMed DOI
Shabarova T., Kasalickı V., Šimek K., Nedoma J., Znachor P., Posch T., et al. (2017). Distribution and ecological preferences of the freshwater lineage LimA (genus PubMed DOI
Šimek K., Bobkova J., Macek M., Nedoma J., Psenner R. (1995). Ciliate grazing on picoplankton in a eutrophic reservoir during the summer phytoplankton maximum: a study at the species and community level. DOI
Šimek K., Horòák K., Jezbera J., Nedoma J., Vrba J., Straskrabová V., et al. (2006). Maximum growth rates and possible life strategies of different bacterioplankton groups in relation to phosphorus availability in a freshwater reservoir. PubMed DOI
Šimek K., Horòák K., Jezbera J., Nedoma J., Znachor P., Hejzlar J., et al. (2008). Spatio-temporal patterns of bacterioplankton production and community composition related to phytoplankton composition and protistan bacterivory in a dam reservoir. DOI
Šimek K., Kasalickı V., Jezbera J., Horòák K., Nedoma J., Hahn M. W., et al. (2013). Differential freshwater flagellate community response to bacterial food quality with a focus on PubMed DOI PMC
Šimek K., Kasalickı V., Zapomelova E., Horòák K. (2011). Alga-derived substrates select for distinct betaproteobacterial lineages and contribute to niche separation in PubMed DOI PMC
Šimek K., Nedoma J., Znachor P., Kasalickı V., Jezbera J., Horòák K., et al. (2014). A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring. DOI
Sommaruga R., Casamayor E. O. (2009). Bacterial ‘cosmopolitanism’ and importance of local environmental factors for community composition in remote high-altitude lakes. PubMed DOI PMC
Sommer U., Adrian R., Domis L. D., Elser J. J., Gaedke U., Ibelings B., et al. (2012). Beyond the plankton ecology group (PEG) model: mechanisms driving plankton succession. DOI
Sommer U. (ed.) (1989). DOI
Sommer U., Gliwicz Z. M., Lampert W., Duncan A. (1986). The PEG-Model of seasonal succession of planktonic events in fresh waters.
Stocker R. (2012). Marine microbes see a sea of gradients. PubMed DOI
Stoeck T., Bass D., Nebel M., Christen R., Jones M. D. M., Breiner H. W., et al. (2010). Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. PubMed DOI
Stoeck T., Epstein S. (2003). Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. PubMed DOI PMC
Tammert H., Tsertova N., Kiprovskaja J., Baty F., Noges T., Kisand V. (2015). Contrasting seasonal and interannual environmental drivers in bacterial communities within a large shallow lake: evidence from a seven year survey. DOI
Teeling H., Fuchs B. M., Becher D., Klockow C., Gardebrecht A., Bennke C. M., et al. (2012). Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. PubMed DOI
Teira E., Martínez-Garcia S., Calvo-Díaz A., Morán X. (2010). Effects of inorganic and organic nutrient inputs on bacterioplankton community composition along a latitudinal transect in the Atlantic Ocean. DOI
Thioulouse J., Dray S. (2007). Interactive multivariate data analysis in R with the ade4 and ade4TkGUI packages. DOI
Urbach E., Vergin K., Larson G., Giovannoni S. (2007). Bacterioplankton communities of Crater Lake, OR: dynamic changes with euphotic zone food web structure and stable deep water populations. DOI
Williams T. J., Wilkins D., Long E., Evans F., Demaere M. Z., Raftery M. J., et al. (2013). The role of planktonic PubMed DOI
Woodhouse J. N., Kinsela A. S., Collins R. N., Bowling L. C., Honeyman G. L., Holliday J. K., et al. (2016). Microbial communities reflect temporal changes in cyanobacterial composition in a shallow ephemeral freshwater lake. PubMed DOI PMC
Wu L., Yu Y. H., Zhang T. L., Feng W. S., Zhang X., Li W. (2009). PCR-DGGE fingerprinting analysis of plankton communities and its relationship to lake trophic status. DOI
Xing P., Hahn M. W., Wu Q. L. (2009). Low taxon richness of bacterioplankton in high-altitude lakes of the Eastern Tibetan Plateau, with a predominance of PubMed DOI PMC
Yankova Y., Neuenschwander S., Köster O., Posch T. (2017). Abrupt stop of deep water turnover with lake warming: drastic consequences for algal primary producers. PubMed DOI PMC
Yannarell A. C., Triplett E. W. (2005). Geographic and environmental sources of variation in lake bacterial community composition. PubMed DOI PMC
Zeder M., Peter S., Shabarova T., Pernthaler J. (2009). A small population of planktonic PubMed DOI
Zhu F., Massana R., Not F., Marie D., Vaulot D. (2005). Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. PubMed DOI
Zohary T. (2004). Changes to the phytoplankton assemblage of Lake Kinneret after decades of a predictable, repetitive pattern. DOI
Cryptic and ubiquitous aplastidic cryptophytes are key freshwater flagellated bacterivores