Microbial Ecology

, Volume 52, Issue 1, pp 72–89 | Cite as

Microbial Community Structure and Dynamics in the Largest Natural French Lake (Lake Bourget)

  • J. Comte
  • S. Jacquet
  • S. Viboud
  • D. Fontvieille
  • A. Millery
  • G. Paolini
  • I. DomaizonEmail author


We investigated the dynamics and diversity of heterotrophic bacteria, autotrophic and heterotrophic flagellates, and ciliates from March to July 2002 in the surface waters (0–50 m) of Lake Bourget. The heterotrophic bacteria consisted mainly of “small” cocci, but filaments (>2 μm), commonly considered to be grazing-resistant forms under increased nanoflagellate grazing, were also detected. These elongated cells mainly belonged to the Cytophaga-Flavobacterium (CF) cluster, and were most abundant during spring and early summer, when mixotrophic or heterotrophic flagellates were the main bacterial predators. The CF group strongly dominated fluorescent in situ hybridization–detected cells from March to June, whereas clear changes were observed in early summer when Beta-proteobacteria and Alpha-proteobacteria increased concomitantly with maximal protist grazing pressures. The analysis of protist community structure revealed that the flagellates consisted mainly of cryptomonad forms. The dynamics of Cryptomonas sp. and Dinobryon sp. suggested the potential importance of mixotrophs as consumers of bacteria. This point was verified by an experimental approach based on fluorescent microbeads to assess the potential grazing impact of all protist taxa in the epilimnion. From the results, three distinct periods in the functioning of the epilimnetic microbial loop were identified. In early spring, mixotrophic and heterotrophic flagellates constituted the main bacterivores, and were regulated by the availability of their resources mainly during April (phase 1). Once the “clear water phase” was established, the predation pressure of metazooplankton represented a strong top-down force on all microbial compartments. During this period only mixotrophic flagellates occasionally exerted a significant bacterivory pressure (phase 2). Finally, the early summer was characterized by the highest protozoan grazing impact and by a rapid shift in the carbon pathway transfer, with a fast change-over of the main predators contribution, i.e., mixotrophic, heterotrophic flagellates and ciliates in bacterial mortality. The high abundance of ciliates during this period was consistent with the high densities of resources (heterotrophic nanoflagellates, algae, bacteria) in deep layers containing the most chlorophyll. Bacteria, as ciliates, responded clearly to increasing phytoplankton abundance, and although bacterial grazing impact could vary largely, bacterial abundance seemed to be primarily bottom-up regulated (phase 3).


Microbial Community Structure Heterotrophic Bacterium Bacterial Abundance Grazing Rate Grazing Impact 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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We acknowledge the valuable laboratory assistance provided by M. Ammar-Khellouf and J-P. Bosse. We are grateful to U. Dorigo for her critical reading of an earlier version of the manuscript. The English text has been checked by Monika Ghosh.


  1. 1.
    Adrian R, Whicham SA, Butler NM (2001) Trophic interactions between zooplankton and the microbial community in contrasting food webs: the epilimnion and deep chlorophyll maximum of a mesotrophic lake. Aquat Microb Ecol 24: 83–97CrossRefGoogle Scholar
  2. 2.
    Alfreider A, Pernthaler J, Amann R, Sattler B, Glöckner FO, Wille A, Psenner R (1996) Community analysis of the bacterial assemblages in the winter cover and pelagic layers of a high mountain lake by in situ hybridization. Appl Environ Microbiol 62: 2138–2144PubMedGoogle Scholar
  3. 3.
    Amann R, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56: 1919–1925PubMedGoogle Scholar
  4. 4.
    American Public Health Association (APHA) (1992) In: Greenberg, A, Clesceri, L, Eaton, A (Eds.) Standard Methods for Examination of Water and Wastewater. Washington,18th edition.Google Scholar
  5. 5.
    Auer B, Arndt H (2001) Taxonomic composition and biomass of heterotrophic flagellates in relation to lake trophy and season. Freshwater Biology 46: 959–972CrossRefGoogle Scholar
  6. 6.
    Azam F, Fenchel T, Field JG, Gray JS, Meyer LA, Thingstad TF (1983) The ecological role of water column microbes in the sea. Mar Ecol Prog Ser 10: 257–263CrossRefGoogle Scholar
  7. 7.
    Bettarel, Y, Amblard, C, Sime Ngando, T, Carrias, JF, Sargos, D, Garabétian, F, Lavandier, P (2003) Viral Lysis, Flagellate Grazing Potential and Bacterial Production in Lake Pavin. Microb Ecol 42: 119–127CrossRefGoogle Scholar
  8. 8.
    Beutler M, Wiltshire KH, Meyer B, Moldaenke C, L¨ring C, Meyerhöfer M, Hansen UP, Dau H (2002) A fluorometric method for the differentiation of algal populations in vivo and in situ. Photosynth Res 72: 39–53PubMedCrossRefGoogle Scholar
  9. 9.
    Bidneko E, Mercier C, Tremblay J, Tailliez P, Kulakauskas S (1998) Estimation of the state of the bacterial cell wall by fluorescent in situ hybridization. Appl Environ Microbiol 64: 3059–3062Google Scholar
  10. 10.
    Bouvier T, Del Giorgio PA (2003) Factors influencing the detection of bacterial cells using fluorescence in situ hybridization (FISH): a quantitative review of published reports. FEMS Microbiol Ecol 44: 3–15CrossRefPubMedGoogle Scholar
  11. 11.
    Børsheim KY, Bratbak G (1987) Cell volume to cell carbon conversion factors for a bacterivorous monas sp enriched from seawater. Mar Ecol Prog Ser 36: 171–175CrossRefGoogle Scholar
  12. 12.
    Bratbak G, Heldal M, Thingstad TF, Riemann B, Haslund OH (1992) Incorporation of viruses into the budget of microbial C-transfer: A first approach. Mar Ecol Prog Ser 83: 273–280CrossRefGoogle Scholar
  13. 13.
    Callieri C, Karjalainen SM, Passoni S (2002) Grazing by ciliates and heterotrophic nanoflagellates on picocyanobacteria in lago Maggiore. J Plankton Res 24: 785–796CrossRefGoogle Scholar
  14. 14.
    Caron DA (1983) Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluorescence microscopy, and comparison with other procedure. Appl Environ Microbiol 46: 491–498PubMedGoogle Scholar
  15. 15.
    Carrias JF, Amblard C, Bourdier G (1996) Protistan bacterivory in an oligotrophic lake: importance of ciliates and flagellates. Microb Ecol 31: 249–268PubMedCrossRefGoogle Scholar
  16. 16.
    Cleven AJ (1996) Indirectly fluorescently labelled flagellates (IFLF): a tool to estimate the predation on free-living heterotrophic flagellates. J Plankton Res 18: 429–442CrossRefGoogle Scholar
  17. 17.
    Cleven AJ, Weisse T (2001) Seasonal succession and taxon specific bacterial grazing rates of heterotrophic nanoflagellates in Lake Constance. Aquat Microb Ecol 23: 147–161CrossRefGoogle Scholar
  18. 18.
    Cottrell MT, Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of Cytophaga flavobacter cluster consuming low- and high- molecular weight dissolved organic matter. Appl Environ Microbiol 66: 1692–1697PubMedCrossRefGoogle Scholar
  19. 19.
    Crosbie ND, Teubner K, Weisse T (2003) Flow-cytometric mapping provides novel insghts into the seasonal and vertical distributions of freshwater autotrophic picoplankton. Aquat Microb Ecol 33: 53–66CrossRefGoogle Scholar
  20. 20.
    Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M (1999) The domain specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22: 434–444PubMedGoogle Scholar
  21. 21.
    Degans H, Zöllner E, Van der Gucht K, De Meester L, Jürgens K (2002) Rapid Daphnia-mediated changes in microbial community structure: an experimental study. FEMS Microbiol Ecol 42: 137–149CrossRefPubMedGoogle Scholar
  22. 22.
    Delong EF, Taylor LT, Marsh TL, Preston CM (1999) Visualization and enumeration of marine planktonic Archae and bacteria by using polyribonucleotide probes anf fluorescent in situ hybridization. Appl Environ Microbiol 65: 5554–5563PubMedGoogle Scholar
  23. 23.
    Domaizon I, Viboud S, Fontvieille D (2003) Taxon specific and seasonal variations in flagellates grazing on heterotrophic bacteria in the oligotrophic Lake Annecy — Importance of mixotrophy. FEMS Microbiol Ecol xx:00–00Google Scholar
  24. 24.
    Gasol JM (1994) A framework for the assessment of top-down vs bottom-up control of heterotrophic nanoflagellate abundance. Mar Ecol Prog Ser 113: 291–300CrossRefGoogle Scholar
  25. 25.
    Gasol JM, Vaqué D (1993) Lack of coupling between heterotrophic nanoflagellates and bacteria: a general phenomenon across aquatic systems? Limnol Oceanogr 38: 657–665CrossRefGoogle Scholar
  26. 26.
    Glöckner FO, Fuchs B, Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65: 3721–3726PubMedGoogle Scholar
  27. 27.
    Glöckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, Amann R (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. Appl Environ Microbiol 66: 5053–5065PubMedCrossRefGoogle Scholar
  28. 28.
    Hahn MW, Höfle MG (1999) Flagellate Predation on a bacterial model community: Interplay of size-selective grazing, specific bacterial cell size, and bacterial community composition. Appl Environ Microbiol 65: 4863–4872PubMedGoogle Scholar
  29. 29.
    Hahn MW, Höfle MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35: 113–121PubMedCrossRefGoogle Scholar
  30. 30.
    Hitchman RB, Jones HL J (2000) The role of mixotrophic protists in the population dynamics of the microbial food web in a small artificial ponds. Freshwater Biology 43: 231–241CrossRefGoogle Scholar
  31. 31.
    Höfle MG, Haas H, Dominik K (1999) Seasonal dynamics of bacterioplankton community structure in a eutrophic lake as determined by 5S rRNA analysis. Appl Environ Microbiol 65: 3164–3174PubMedGoogle Scholar
  32. 32.
    Hulot FD, Lacroix G, Lescher-Moutoué F, Loreau M (2000) Functional diversity governs ecosystem response to nutrient enrichment. Nature 405: 00–00PubMedCrossRefGoogle Scholar
  33. 33.
    Jardillier L, Basset M, Domaizon I, Belan A, Amblard C, Richardot M, Debroas D (2004) Bottom-up and top-down control of bacterial community composition in the euphotic zone of a reservoir. Aquat Microb Ecol 35: 259–273CrossRefGoogle Scholar
  34. 34.
    Jones RI (2000) Mixotrophy in planktonic protist: an overview. Freshwater Biology 45: 219–226CrossRefGoogle Scholar
  35. 35.
    Jürgens K (1994) Impact of Daphnia on planktonic microbial food webs-a review. Mar Microb Food Webs 8: 295–324Google Scholar
  36. 36.
    Jürgens K, Stolpe G (1995) Seasonal dynamics of crustacean, zooplankton, heterotrophic nanoflagellates and bacteria in a shallow, eutrophic lake. Freshwater Biology 33: 27–38CrossRefGoogle Scholar
  37. 37.
    Jürgens K, Pernthaler J, Schalla S, Amann R (1999) Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl Environ Microbiol 65: 1241–1250PubMedGoogle Scholar
  38. 38.
    Jürgens K, Jeppesen E (2000) The impact of metazooplankton on the structure of the microbial food web in a shallow, hypertrophic lake. J Plankton Res 22: 1047–1070CrossRefGoogle Scholar
  39. 39.
    Jürgens K, Simek K (2000) Functionnal response and particle size selection of Halteria cf. grandinella, a common freshwater oligotrichous ciliate. Aquat Microb Ecol 22: 57–68CrossRefGoogle Scholar
  40. 40.
    Jürgens K, Gasol JM, Vaqué D (2000) Bacteria-flagellate coupling in microcosm experiments in the central Atlantic ocean. J Exp Mar Biol Ecol 245: 127–147CrossRefGoogle Scholar
  41. 41.
    Jürgens K, Matz C (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie van Leeuwenhoek 81: 413–434PubMedCrossRefGoogle Scholar
  42. 42.
    Kemp PF, Lee S, LaRoch J (1993) Estimating the growth rate of slowly growing marine bacteria from RNA content. Appl Environ Microbiol 59: 2594–2601PubMedGoogle Scholar
  43. 43.
    Kirchman DL (2001) The ecology of Cytophaga flavobacterium in aquatic environments. FEMS Microbiol Ecol 39: 91–100Google Scholar
  44. 44.
    Kisand V, Zingel P (2000) Dominance of ciliate grazing on bacteria during spring in a shallow eutrophic lake. Aquat Microb Ecol 22: 142CrossRefGoogle Scholar
  45. 45.
    Lebaron P, Servais P, Trousselier M, Courties C, Muyzer G, Bernard L, Schâfer H, Pukall R, Stackebrandt E, Guindulain T, Vives-Rego J (2000) Microbial community dynamics in Mediterranean nutrient enriched seawater mesocosms: changes, activity and composition. FEMS Microbiol Ecol 34: 255–266Google Scholar
  46. 46.
    Leboulanger C, Dorigo U, Jacquet S, Le, Berre B, Paolini G, Humbert JF (2002) Application of a submersible spectrofluorometer for rapid monitoring of freshwater cyanobacterial blooms: a case study. Aquat Microb Ecol 30: 83–89CrossRefGoogle Scholar
  47. 47.
    Loferer-Krößbacher M, Klima J, Psenner R (1998) Determination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Appl Environ Microbiol 64: 688–694PubMedGoogle Scholar
  48. 48.
    Manz W, Amann R, Ludwig W, Wagner M, Schleifer KH (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15: 593–600Google Scholar
  49. 49.
    Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH (1996) Application of a suite of 16S rRNA-targeted probes designed to investigate bacteria of the phylum Cytophaga-Flavobacterium-bacteroides in the natural environment. Microbiology 142: 1097–1106PubMedCrossRefGoogle Scholar
  50. 50.
    Methé BA, Zehr JP (1999) Diversity of bacterial communities in, Adirondack lakes: do species assemblages reflect lake chemistry? Hydrobiologia 401: 77–96CrossRefGoogle Scholar
  51. 51.
    Moter A, Göbel UB (2000) Fluorescence in situ hybridisation (FISH) for direct visualization of microorganisms. J Microbial Methods 41: 85–112CrossRefGoogle Scholar
  52. 52.
    Müller H (1989) The relative importance of different ciliate taxa in the pelagic food web of lake Constance. Microb Ecol 18: 261–273CrossRefGoogle Scholar
  53. 53.
    Muylaert K Van der, Gucht K, Vloemans N, De Meester L, Gillis M, Vyverman W (2002) Relationship between bacterial community composition and bottom-up versus top-down variables in four eutrophic shallow lakes. Appl Environ Microbiol 68: 4740–4750PubMedCrossRefGoogle Scholar
  54. 54.
    Noble RT, Middelboe M, Fuhrman JA (1999) Effects of viral enrichment on the mortality and growth of heterotrophic bacterioplankton. Aquat Microb Ecol 18: 1–13CrossRefGoogle Scholar
  55. 55.
    Pernthaler A, Simek K, Sattler B, Schwarzenbacher B, Bobková J, Psenner R (1996) Short term changes of protozoan control on autotrophic picoplankton in an oligomesotrophic lake. J Plankton Res 18: 443–462CrossRefGoogle Scholar
  56. 56.
    Pernthaler J, Glöckner FO, Unterholzner S, Alfreider A, Psenner R, Amann R (1998) Seasonal community and population dynamics of pelagic bacteria and archea in high mountain lake. Appl Environ Microbiol 64: 4299–4306PubMedGoogle Scholar
  57. 57.
    Pomeroy LR (1974) The ocean’s food web, a changing paradigm. Bioscience 24: 499–504CrossRefGoogle Scholar
  58. 58.
    Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25: 943–948Google Scholar
  59. 59.
    Posch T, Simek K, Vrba J, Pernthaler J, Nedoma J, Sattler B, Sonntag B, Psenner R (1999) Predator-induced changes of bacterial size-structure and productivity studied on an experimental microbial community. Aquat Microb Ecol 18: 235–246CrossRefGoogle Scholar
  60. 60.
    Proctor LM, Fuhrman JA (1992) Mortality of marine bacteria in response to enrichments of the virus size fraction from seawater. Mar Ecol Prog Ser 87: 283–293CrossRefGoogle Scholar
  61. 61.
    Putt M, Stoecker DK (1989) An experimentally determined carbon: volume ratio for marine oligotrichous ciliates from estuarine and coastal waters. Limnol Oceanogr 34: 1097–1103Google Scholar
  62. 62.
    Ribes M, Coma R, Gili J (1999) Seasonal variation of particulate organic carbon, dissolved organic carbon and the contribution of microbial communities to the live particulate organic carbon in a shallow near-bottom ecosystem at the North western Mediterranean Sea. J Plankton Res 21: 1077–1100CrossRefGoogle Scholar
  63. 63.
    Rosenstock B, Simon M (2001) Sources and sinks of dissolved free amino acids and protein in a large and deep mesotrophic lake. Limnol Oceanogr 46: 644–654CrossRefGoogle Scholar
  64. 64.
    Sanders RW, Porter KG, Bennett SJ, Debiase AE (1989) Seasonal patterns of bacterivory by flagellates, ciliates, rotifers and cladocerans in a freshwater planktonic community. Limnol Oceanogr 34: 673–687Google Scholar
  65. 65.
    Sanders RW, Berninger UG, Lim EL, Kemp PF, Caron DA (2000) Heterotrophic and mixotrophic nanoplankton predation in the Sargasso Sea and on Georges Bank. Mar Ecol Prog Ser 192: 103–118CrossRefGoogle Scholar
  66. 66.
    Sime-Ngando T, Hartman P, Grolière CA (1990) Rapid quantification of planktonic ciliates: Comparison of improved live counting with other methods. Appl Environ Microbiol 56: 2234–2242PubMedGoogle Scholar
  67. 67.
    Sime-Ngando T, Bourdier G, Amblard C, Pinel-Alloul B (1991) Short-term variations in specific biovolumes of different bacterial forms in aquatic ecosystems. Microb Ecol 21: 211–226CrossRefGoogle Scholar
  68. 68.
    Simek K, Vrba J, Pernthaler J, Posch T, Hartman P, Nedoma J, Psenner R (1997) Morphological and composition shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Appl Environ Microbiol 63: 587–595PubMedGoogle Scholar
  69. 69.
    Simek K, Jürgens K, Nedoma J, Comerma M, Armengol J (2000) Ecological role and bacterial grazing of Halteria sp: small freshwater oligotrichs as dominant pelagic ciliate bacterivores. Aquat Microb Ecol 22: 43–56CrossRefGoogle Scholar
  70. 70.
    Simek K, Pernthaler J, Weinbauer MG, Hornak K, Dolan J, Nedoma J, Masin M, Amann R (2001) Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellates grazing in a mesoeutrophic reservoir. Appl Environ Microbiol 67: 2723–2733PubMedCrossRefGoogle Scholar
  71. 71.
    Sommaruga R, Psenner R (1995) Permanent presence of grazing-resistant bacteria in a hypertrophic lake. Appl, Environ Microbiol 61: 3457–3459PubMedGoogle Scholar
  72. 72.
    Stahl DA, Amann R (1991) Development and application of nucleic acid probes In: Nucleic Acid Techniques in Bacterial Systematics,(Eds). Goodfellow M, Stackebrandt E, John Wiley & Sons, Chichester, UK, pp 205–248Google Scholar
  73. 73.
    Thouvenot A, Richardot M, Debroas D, Dévaux J (1999) Bacterivory of metazooplankton, ciliates and flagellates in a newly flooded reservoir. J Plankton Res 21: 1659–1679CrossRefGoogle Scholar
  74. 74.
    Tsuji T, Ohki K, Fujita Y (1986) Determination of photosynthetic pigment composition in an individual phytoplankton cell in seas and lakes using fluorescence microscopy: properties of the fluorescence emitted from picophytoplankton cells. Mar Biol 93: 343–349CrossRefGoogle Scholar
  75. 75.
    Tranvik LJ, Porter J, Sieburth, JMc N (1989) Occurrence of bacterivory in Cryptomonas, a common freshwater phytoplankter. Oecologia 78: 473–476CrossRefGoogle Scholar
  76. 76.
    Verity PG, Roberson CY, Tronzo CR, Andrews MG, Nelson JR, Sieracki ME (1992) Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol Oceanogr 37: 1434–1446Google Scholar
  77. 77.
    Weisse T, Müller H, Pinto-Coehlo RM, Schweizer A, Springmann D, Baldringer G (1990) Response of the microbial loop to the phytoplankton spring bloom in a prealpine lake. Limnol Oceanogr 35: 781–794CrossRefGoogle Scholar
  78. 78.
    Weinbauer, Rassoulzadegan (2004) Are Viruses driving microbial diversification and diversity? Environmental Microbiology 6(1), 1–11Google Scholar
  79. 79.
    Wetzel RG (1982) Limnology. WB Saunders, PhiladelphiaGoogle Scholar
  80. 80.
    Wieltschnig C, Kirschner AK T, Steitz A, Velimirov B (2001) Weak coupling between heterotrophic nanoflagellates and bacteria in a eutrophic freshwater environment. Microb Ecol 42: 159–167PubMedGoogle Scholar
  81. 81.
    Wu QL, Boegnik J, Hahn MW (2004) Successful predation of filamentous bacteria by a nanoflagellate challenges current models of flagellate bacterivory. Appl Environ Microbiol 70: 332–339PubMedCrossRefGoogle Scholar
  82. 82.
    Yoshida T, Gurung TB, Kagami M, Urabe J (2001) Contrasting effects of a cladoceran (Daphnia galeata) and a calanoid copepod (Eodiaptomus japonicus) on algal and microbial plankton in a Japanese lake, Lake Biwa. Oecologia 129: 602–610Google Scholar
  83. 83.
    Zwisler W, Selje N, Simon M (2003) Seasonal patterns of the bacterioplankton community composition in a large mesotrophic lake. Aquat Microb Ecol 31: 211–225CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • J. Comte
    • 1
  • S. Jacquet
    • 2
  • S. Viboud
    • 1
  • D. Fontvieille
    • 1
  • A. Millery
    • 1
  • G. Paolini
    • 3
  • I. Domaizon
    • 1
    Email author
  1. 1.UMR CARRTEL, Université de SavoieEquipe de Microbiologie AquatiqueFrance
  2. 2.UMR CARRTEL, Station INRA d’Hydrobiologie LacustreEquipe de Microbiologie AquatiqueFrance
  3. 3.Cellule Technique de l’Aquarium du BourgetFrance

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