Deep, cold, and dark hypolimnia represent the largest volume of water in freshwater lakes with limited occurrences of phototrophs. However, the presence of prokaryotes supports populations of bacterivorous ciliates and heterotrophic nanoflagellates (HNF). Nevertheless, protistan bacterivory rates and the major hypolimnetic ciliate bacterivores are poorly documented. We conducted a high frequency sampling (three-times a week) in the oxic hypolimnion of a stratified mesoeutrophic reservoir during summer, characterized by stable physicochemical conditions and low water temperature. Using fluorescently labeled bacteria we estimated that ciliates and HNF contributed, on average, 30% and 70% to aggregated protistan bacterivory, respectively, and collectively removed about two thirds of daily hypolimnetic prokaryotic production. The ciliate community was analyzed by the quantitative protargol staining method. One scuticociliate morphotype dominated the hypolimnetic ciliate community, accounting for 82% of total ciliates and over 98% of total ciliate bacterivory, with average cell-specific uptake rate of 202 prokaryotes per hour. Moreover, long-amplicon sequencing revealed that the scuticociliate belongs to an unidentified clade closely related to the Ctedoctematidae and Eurystomatellidae families. The high-resolution sampling, microscopic, and sequencing methods allowed uncovering indigenous microbial food webs in the hypolimnetic environment and revealed a functional simplification of ciliate communities, dominated by a new bacterivorous scuticociliate lineage.

Biology Centre CAS Institute of Hydrobiology Na Sádkách 7 České Budějovice 37005 Czech Republic

Faculty of Science University of South Bohemia České Budějovice 37005 Czech Republic

Research Department for Limnology Mondsee University of Innsbruck Mondseestrasse 9 Mondsee A 5310 Austria

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Ezzedine  JA, Desdevises  Y, Jacquet  S. PubMed DOI

Williams  HN, Lymperopoulou  DS, Athar  R. et al. PubMed DOI PMC

Sanders  RW, Porter  KG, Bennett  SJ. et al.  Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. DOI

Boenigk  J, Arndt  H. Bacterivory by heterotrophic flagellates: community structure and feeding strategies. PubMed DOI

Jürgens  K, Matz  C. Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. PubMed DOI

Sherr  EB, Sherr  BF. Significance of predation by protists in aquatic microbial food webs. PubMed DOI

Weinbauer  MG. Ecology of prokaryotic viruses. PubMed DOI

Jürgens  K. Impact of

Jürgens  K, Jeppesen  E. The impact of metazooplankton on the structure of the microbial food web in a shallow, hypertrophic lake. DOI

Arndt  H, Dietrich  D, Auer  B. et al.  Functional diversity of heterotrophic flagellates in aquatic ecosystems.

Jones  RI. Mixotrophy in planktonic protists: an overview. DOI

Domaizon  I, Viboud  S, Fontvieille  D. Taxon-specific and seasonal variations in flagellates grazing on heterotrophic bacteria in the oligotrophic Lake Annecy—importance of mixotrophy. PubMed DOI

Fischer  R, Giebel  HA, Hillebrand  H. et al.  Importance of mixotrophic bacterivory can be predicted by light and loss rates. DOI

Šimek  K, Nedoma  J, Znachor  P. et al.  A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring.

Mukherjee  I, Grujčić  V, Salcher  MM. et al.  Integrating depth-dependent protist dynamics and microbial interactions in spring succession of a freshwater reservoir. PubMed DOI PMC

Oikonomou  A, Pachiadaki  M, Stoeck  T. Protistan grazing in a meromictic freshwater lake with anoxic bottom water. PubMed DOI

Princiotta  SD, Sanders  RW. Heterotrophic and mixotrophic nanoflagellates in a mesotrophic lake: abundance and grazing impacts across season and depth. DOI

Carrias  J-F, Amblard  C, Bourdier  G. Seasonal dynamics and vertical distribution of planktonic ciliates and their relationship to microbial food resources in the oligomesotrophic Lake Pavin.

Müller  H, Geller  W, Schöne  A. Pelagic ciliates in Lake Constance: comparison of epilimnion and hypolimnion.

Sonntag  B, Posch  T, Klammer  S. et al.  Protozooplankton in the deep oligotrophic Traunsee (Austria) influenced by discharges of soda and salt industries. DOI

Beaver  JR, Crisman  TL. The role of ciliated protozoa in pelagic freshwater ecosystems. PubMed DOI

Zingel  P, Ott  I. Vertical distribution of planktonic ciliates in strongly stratified temperate lakes. DOI

Sonntag  B, Posch  T, Klammer  S. et al.  Phagotrophic ciliates and flagellates in an oligotrophic, deep, alpine lake: contrasting variability with seasons and depths. DOI

Mieczan  T. Diversity and vertical distribution of planktonic ciliates in a stratified mesotrophic lake: relationship to environmental conditions. DOI

Bręk-Laitinen  G, Bellido  JL, Ojala  A. Response of a microbial food web to prolonged seasonal hypoxia in a boreal lake. DOI

Mundim  KC, Baraldi  S, Machado  HG. et al.  Temperature coefficient (Q10) and its applications in biological systems: beyond the Arrhenius theory. DOI

Zeder  M, Peter  S, Shabarova  T. et al.  A small population of planktonic PubMed DOI

Eckert  EM, Salcher  MM, Posch  T. et al.  Rapid successions affect microbial n-acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom. PubMed DOI

Šimek  K, Grujčić  V, Hahn  MW. et al.  Bacterial prey food characteristics modulate community growth response of freshwater bacterivorous flagellates.

Šimek  K, Grujčić  V, Mukherjee  I. et al.  Cascading effects in freshwater microbial food webs by predatory Cercozoa, Katablepharidacea and ciliates feeding on aplastidic bacterivorous cryptophytes. PubMed DOI PMC

Kavagutti  VS, Bulzu  PA, Chiriac  CM. et al.  High-resolution metagenomic reconstruction of the freshwater spring bloom. PubMed DOI PMC

Neuenschwander  SM, Pernthaler  J, Posch  T. et al.  Seasonal growth potential of rare lake water bacteria suggest their disproportional contribution to carbon fluxes. PubMed DOI

Hernandez-Aviles  JS, Bertoni  R, Macek  M. et al.  Why bacteria are smaller in the epilimnion than in the hypolimnion? A hypothesis comparing temperate and tropical lakes. DOI

Mehrshad  M, Salcher  MM, Okazaki  Y. et al.  Hidden in plain sight-highly abundant and diverse planktonic freshwater PubMed DOI PMC

Okazaki  Y, Fujinaga  S, Tanaka  A. et al.  Ubiquity and quantitative significance of bacterioplankton lineages inhabiting the oxygenated hypolimnion of deep freshwater lakes. PubMed DOI PMC

Park  H, Shabarova  T, Salcher  MM. et al.  In the right place, at the right time: the integration of bacteria into the plankton ecology group model. PubMed DOI PMC

Coci  M, Odermatt  N, Salcher  MM. et al.  Ecology and distribution of Thaumarchaea in the deep hypolimnion of Lake Maggiore. PubMed DOI PMC

Okazaki  Y, Nakano  SI. Vertical partitioning of freshwater bacterioplankton community in a deep mesotrophic Lake with a fully oxygenated hypolimnion (lake Biwa, Japan). PubMed DOI

Piwosz  K, Mukherjee  I, Salcher  MM. et al.  CARD-FISH in the sequencing era: opening a new universe of protistan ecology. PubMed DOI PMC

Gong  J, Dong  J, Liu  X. et al.  Extremely high copy numbers and polymorphisms of the rDNA operon estimated from single cell analysis of oligotrich and peritrich ciliates. PubMed DOI

Stoeck  T, Breiner  HW, Filker  S. et al.  A morphogenetic survey on ciliate plankton from a mountain lake pinpoints the necessity of lineage-specific barcode markers in microbial ecology. PubMed DOI PMC

Pitsch  G, Bruni  EP, Forster  D. et al.  Seasonality of planktonic freshwater ciliates: are analyses based on V9 regions of the 18S rRNA gene correlated with morphospecies counts? PubMed DOI PMC

Martin  JL, Santi  I, Pitta  P. et al.  towards quantitative metabarcoding of eukaryotic plankton: an approach to improve 18S rRNA gene copy number bias.

Pfister  G, Sonntag  B, Posch  T. Comparison of a direct live count and an improved quantitative protargol stain (QPS) in determining abundance and cell volumes of pelagic freshwater protozoa. DOI

Šimek  K, Grujčić  V, Nedoma  J. et al.  Microbial food webs in hypertrophic fishponds: omnivorous ciliate taxa are major protistan bacterivores. DOI

Latz  MAC, Grujčić  V, Brugel  S. et al.  Short- and long-read metabarcoding of the eukaryotic rRNA operon: evaluation of primers and comparison to shotgun metagenomics sequencing. PubMed DOI

Znachor  P, Nedoma  J, Hejzlar  J. et al.  Multiple long-term trends and trend reversals dominate environmental conditions in a man-made freshwater reservoir. PubMed DOI

Znachor  P, Hejzlar  J, Vrba  J. et al.  Brief history of long-term ecological research into aquatic ecosystems and their catchments in the Czech Republic.

Jezbera  J, Horňák  K, Šimek  K. Food selection by bacterivorous protists: insight from the analysis of the food vacuole content by means of fluorescence PubMed DOI

Fenchel  T. Ecology of Protozoa: The Biology of Free-Living Phagotropic Protists: Springer-Verlag, 2013, Vol. 187. Berlin, Heidelberg: Springer, 1987.

Sherr  BF, Sherr  EB, Fallon  RD. Use of monodispersed, fluorescently labeled bacteria to estimate PubMed DOI PMC

Kasalicky  V, Jezbera  J, Hahn  MW. et al.  The diversity of the PubMed DOI PMC

Jezbera  J, Jezberova  J, Koll  U. et al.  Contrasting trends in distribution of four major planktonic betaproteobacterial groups along a ph gradient of epilimnia of 72 freshwater habitats. PubMed DOI PMC

Šimek  K, Sirová  D. Fluorescently labeled bacteria as a tracer to reveal novel pathways of organic carbon flow in aquatic ecosystems. PubMed DOI

Skibbe  O. An improved quantitative protargol stain for ciliates and other planktonic protists.

Foissner  W, Berger  H, Kohmann  F. Taxonomische und ökologische revision der ciliaten des saprobiensystems—band iii: Hymenostomata, Protomatida, Nassulida.

Foissner  W, Berger  H. A user-friendly guide to the ciliates (protozoa, DOI

Foissner  W, Berger  H, Schaumburg  J. Identification and ecology of limnetic plankton ciliates.

Posch  T, Eugster  B, Pomati  F. et al.  Network of interactions between ciliates and phytoplankton during spring. PubMed DOI PMC

Stoeck  T, Bass  D, Nebel  M. et al.  Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. PubMed DOI

Schwelm  A, Berney  C, Dixelius  C. et al.  The large subunit rDNA sequence of PubMed DOI PMC

Callahan  BJ, Wong  J, Heiner  C. et al.  High-throughput amplicon sequencing of the full-length 16S rRNA gene with single-nucleotide resolution. PubMed DOI PMC

Guillou  L, Bachar  D, Audic  S. et al.  The protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. PubMed DOI PMC

Quast  C, Pruesse  E, Yilmaz  P. et al.  The silva ribosomal RNA gene database project: improved data processing and web-based tools. PubMed DOI PMC

Katoh  K, Standley  DM. Mafft multiple sequence alignment software version 7: improvements in performance and usability. PubMed DOI PMC

Shazib  SUA, Vďačný  P, Slovak  M. et al.  Deciphering phylogenetic relationships and delimiting species boundaries using a bayesian coalescent approach in protists: a case study of the ciliate genus PubMed DOI PMC

Zhang  G, Li  Y, Gong  R. et al.  Taxonomy and molecular phylogeny of pleurostomatid ciliates from China with a description of two new species. PubMed DOI

Nguyen  LT, Schmidt  HA, von Haeseler  A. et al.  IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. PubMed DOI PMC

Letunic  I, Bork  P. Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. PubMed DOI PMC

Li  T, Liu  M, Zhang  J. et al.  Diversity in freshwater scuticociliates (

Li  T, Zhang  T, Liu  M. et al.  Findings on three endocommensal scuticociliates (Protista, PubMed DOI PMC

Pan  M, Chen  Y, Liang  C. et al.  Taxonomy and molecular phylogeny of three freshwater scuticociliates, with descriptions of one new genus and two new species (Protista, PubMed DOI

Wieczynski  DJ, Singla  P, Doan  A. et al.  Linking species traits and demography to explain complex temperature responses across levels of organization. PubMed DOI PMC

Laybourn-Parry  J. The microbial loop in Antarctic lakes. In: Lyons  WB, Howard-Williams  C, Hawes  I. (eds.), Ecosystem Processes in Antarctic Ice-Free Landscapes. Bakelma: Rotterdam, 1997, 231–9.

Sonntag  B, Summerer  M, Sommaruga  R. Factors involved in the distribution pattern of ciliates in the water column of a transparent alpine lake. PubMed DOI PMC

Kammerlander  B, Koinig  KA, Rott  E. et al.  Ciliate community structure and interactions within the planktonic food web in two alpine lakes of contrasting transparency. PubMed DOI PMC

Wurtsbaugh  WA. Food-web modification by an invertebrate predator in the great salt lake (USA). PubMed DOI

Kamjunke  N, Gaedke  U, Tittel  J. et al.  Strong vertical differences in the plankton composition of an extremely acidic lake. DOI

Šimek  K, Jürgens  K, Nedoma  J. et al.  Ecological role and bacterial grazing of DOI

Weisse  T, Sonntag  B. Ciliates in planktonic food webs: communication and adaptive response. In: Witzany G, Nowacki M (eds.),

Auer  B, Elzer  U, Arndt  H. Comparison of pelagic food webs in lakes along a trophic gradient and with seasonal aspects: influence of resource and predation. DOI

Frantal  D, Agatha  S, Beisser  D. et al.  Molecular data reveal a cryptic diversity in the genus PubMed DOI PMC

Macek  M, Vrba  J, Hejzlar  J. et al.  Two-decade changes in the ciliate assemblage feeding pattern reflect the reservoir nutrient load. DOI

Macek  M, Šimek  K, Pernthaler  J. et al.  Growth rates of dominant planktonic ciliates in two freshwater bodies of different trophic degree. DOI

Boukheloua  R, Mukherjee  I, Park  H. et al.  Global freshwater distribution of PubMed DOI PMC

Šimek  K, Mukherjee  I, Nedoma  J. et al.  CARD-FISH and prey tracer techniques reveal the role of overlooked flagellate groups as major bacterivores in freshwater hypertrophic shallow lakes. PubMed DOI PMC

Šimek  K, Macek  M, Pernthaler  J. et al.  Can freshwater planktonic ciliates survive on a diet of picoplankton? DOI

Ptacnik  R, Gomes  A, Royer  SJ. et al.  A light-induced shortcut in the planktonic microbial loop. PubMed DOI PMC

Vrba  J, Šorf  M, Nedoma  J. et al.  Top-down and bottom-up control of plankton structure and dynamics in hypertrophic fishponds. DOI

Foissner  W. An update of 'basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa'. PubMed DOI

Fan  X, Hu  X, Al-Farraj  SA. et al.  Morphological description of three marine ciliates ( PubMed DOI

Fan  X, Xu  Y, Jiang  J. et al.  Morphological descriptions of five scuticociliates including one new species of PubMed DOI

Miao  M, Wang  Y, Song  W. et al.  Description of PubMed DOI

Macek  M, Pestová  D, Martínez Pérez  ME. Seasonal and spatial dynamics of a ciliate assemblage in a warm-monomictic Lake Alchichica (Puebla, Mexico).

Zhu  F, Massana  R, Not  F. et al.  Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. PubMed DOI

Pröschold  T, Rieser  D, Darienko  T. et al.  An integrative approach sheds new light onto the systematics and ecology of the widespread ciliate genus coleps ( PubMed PMC

Sonntag  B, Frantal  D, Kammerlander  B. et al.  Widespread occurrence of two planktonic ciliate species ( DOI

Seďa  J, Kolařová  PA. et al. DOI

Forster  D, Qu  Z, Pitsch  G. et al.  Lake ecosystem robustness and resilience inferred from a climate-stressed protistan plankton network. PubMed DOI PMC

Qu  Z, Forster  D, Bruni  EP. et al.  Aquatic food webs in deep temperate lakes: key species establish through their autecological versatility. PubMed DOI

Mukherjee  I, Hodoki  Y, Nakano  S. Kinetoplastid flagellates overlooked by universal primers dominate in the oxygenated hypolimnion of Lake Biwa, Japan. PubMed DOI

Mukherjee  I, Hodoki  Y, Okazaki  Y. et al.  Widespread dominance of kinetoplastids and unexpected presence of diplonemids in deep freshwater lakes. PubMed DOI PMC

Andrei  AŞ, Salcher  MM, Mehrshad  M. et al.  Niche-directed evolution modulates genome architecture in freshwater Planctomycetes. PubMed DOI PMC

Sommer  U. The paradox of the plankton: fluctuations of phosphorus availability maintain diversity of phytoplankton in flow-through cultures 1. DOI

Huisman  J, Weissing  FJ. Biodiversity of plankton by species oscillations and chaos. DOI

Znachor  P, Visocká  V, Nedoma  J. et al.  Spatial heterogeneity of diatom silicification and growth in a eutrophic reservoir. DOI

Chiriac  MC, Haber  M, Salcher  MM. Adaptive genetic traits in pelagic freshwater microbes. PubMed DOI

Posch  T, Jezbera  J, Vrba  J. et al.  Size selective feeding in PubMed DOI