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Seasonal patterns of viral, microbial and planktonic communities in Sidi Salem: a freshwater reservoir (North of Tunisia)

Published online by Cambridge University Press:  28 October 2014

Samira Ben Romdhane*
Institut National des Sciences et Technologies de la Mer (INSTM), 28 rue du 2 mars 1934 -Salammbô, Tunisie
Monia El Bour
Institut National des Sciences et Technologies de la Mer (INSTM), 28 rue du 2 mars 1934 -Salammbô, Tunisie
Asma Hamza
Institut National des Sciences et Technologies de la Mer (INSTM), 28 rue du 2 mars 1934 -Salammbô, Tunisie
Fourat Akrout
Institut National des Sciences et Technologies de la Mer (INSTM), 28 rue du 2 mars 1934 -Salammbô, Tunisie
Mohamed Mejdeddine Kraiem
Institut National des Sciences et Technologies de la Mer (INSTM), 28 rue du 2 mars 1934 -Salammbô, Tunisie
Stéphan Jacquet
INRA UMR 42, Centre Alpin de Recherches sur les Réseaux Trophiques des Ecosystèmes Limniques, 74203 Thonon Cedex, France
*Corresponding author:
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We investigated the distribution and dynamics of viruses, prokaryotes and small eukaryotic phytoplankton in Sidi Salem freshwater reservoir (Northern Tunisia). Samples were collected from the deepest station at different depths throughout the water column for 2 years (February 2009 to January 2011). The reservoir was characterized by seasonal alternations of thermal stratification and homothermy. Among the different microbial communities counted using flow cytometry (FCM), picocyanobacteria constituted an important autotrophic component since they were always present and their highest concentration reached 3.02 and 2.65×105 cells.mL−1 in March 2009 and June 2010, respectively. The heterotrophic prokaryotic communities (represented mainly by bacteria) were characterized by a clear separation between two subgroups referred to as high-DNA and low-DNA content populations, and the highest concentrations of heterotrophic bacteria (i.e., 3.8×107 cells.mL−1) were recorded in spring 2009. Several viral groups referred to as virus-like particles (VLP) groups 1, 2 and 3 could also be discriminated using FCM. VLP1 and VLP2 displayed a significant correlation with the heterotrophic bacteria (r=0.80 and 0.78, P<0.001) but seem to be independent from picocyanobacteria and/or chlorophyll a, suggesting these VLPs were mainly bacteriophages. At last, the virus to prokaryotic ratio could be high, especially in summer (mean=22, max=487), suggesting a strong coupling between bacteria and viruses, at least at certain periods of the year.

Research Article
© EDP Sciences, 2014

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Abedon, S.T., 2006. Phage ecology. In: Abedon, C.S.T. (ed.), The Bacteriophages, Oxford University Press, Oxford, 3746.Google ScholarPubMed
Agawin, N.S.R., Duarte, C.M. and Agustí, S., 2000. Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production. Limnol. Oceanogr., 45, 591600.CrossRefGoogle Scholar
Anneville, O. and Leboulanger, C., 2001. Long-terms changes in the vertical distribution of phytoplankton biomass and primary production in Lake Geneva: a response to the oligotrophication. Atti. Assoc. Ital. Oceanol. Limnol., 14, 2535.Google Scholar
Auguet, J.C., Barberan, A. and Casamayor, E.O., 2010. Global ecological patterns in uncultured archaea. ISME J. 4, 182190.CrossRefGoogle ScholarPubMed
Baines, S.B. and Pace, M.L., 1991. The production of dissolved organic matter by phytoplankton and its importance to bacteria: patterns across marine and freshwater system. Limnol. Oceanogr., 36, 10781090.CrossRefGoogle Scholar
Bell, T. and Kalff, J., 2001. The contribution of picophytoplankton in marine and freshwater systems of different trophic status and depth. Limnol. Oceanogr., 46, 12431248.CrossRefGoogle Scholar
Ben Mammou, A., 1998. Barrages Nebraska, Sidi Salem, Sidi Saâd et Sidi Boubaker. Quantification, étude sédimentologique et géotechnique des sédiments piégés. Apports des images satellitaires. Thèse Doct. Univ. Tunis, II, 345 p.Google Scholar
Ben Mammou, A. and Louati, M.H., 2007. Evolution temporelle de l'envasement des retenues de barrages de Tunisie. Rev. Sci. Eau, 20, 201211.Google Scholar
Ben Rejeb Jenhani, A., Bouaïcha, N., El Herry, S., Fathalli, A., Zekri, I., Haj Zekri, S., Limam, L., Alouini, S. and Romdhane, M.S., 2006. Les cyanobactéries et leurs potentialités toxiques dans les retenues des barrages du Nord de la Tunisie. Archs. Inst. Pasteur Tunis, 83, 7181.Google Scholar
Ben Rejeb Jenhani, A., Fathalli, A. and Romdhane, M.S., 2012. Phytoplankton assemblages in Bir M'Cherga freshwater reservoir (Tunisia). Water Resour. Wetlands, 136141.Google Scholar
Benzarti, Z., 2003. La pluviométrie en Tunisie: Analyse des années très pluvieuse. In: Arnould, P. and Hotyat, M. (eds.), Eau et environnement: Tunisie et milieux méditerranéens, ENS Edition, Lyon, 6378.CrossRefGoogle Scholar
Berdjeb, L., Pollet, T., Domaizon, I. and Jacquet, S., 2011. Effects of grazers and viruses on bacterial community structure and production in two contrasting trophic lakes. BMC Microb., 11, 118.CrossRefGoogle ScholarPubMed
Bergh, O., Borsheim, K.Y., Bratbak, G. and Heldal, M., 1989. High abundance of viruses found in aquatic environments. Nature, 340, 467468.CrossRefGoogle ScholarPubMed
Bettarel, Y., Sime-NGando, T., Amblard, C., Carrias, J.-F. and Portelli, C., 2003. Virioplankton and microbial communities in aquatic systems: a seasonal study in two lakes of different trophy. Freshw. Biol., 48, 810822.CrossRefGoogle Scholar
Bettarel, Y., Sime-NGando, T., Amblard, C. and Dolan, J., 2004. Viral activity in two contrasting lake ecosystems. Appl. Environ. Microb., 70, 29412951.CrossRefGoogle ScholarPubMed
Bratbak, G., Heldal, M., Thingstad, T.F. and Tuomi, P.I., 1996. Dynamics of virus abundance in coastal sea water. FEMS Microb. Ecol., 19, 263269.CrossRefGoogle Scholar
Breitbart, M., 2012. Marine viruses: truth or dare. Annu. Rev. Mar. Sci., 4, 425448.CrossRefGoogle ScholarPubMed
Brum, J.R., Stewart, G.F., Jiang, S.C. and Jellison, R., 2005. Spatial and temporal variability of prokaryotes, viruses, and viral infections of prokaryotes in an alkaline, hypersaline lake. Aqua. Microb. Ecol., 41, 247260.CrossRefGoogle Scholar
Brussaard, C.P.D., 2004. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ. Microb., 70, 15061513.CrossRefGoogle ScholarPubMed
Callieri, C., 2007. Picophytoplankton in freshwater ecosystems: the importance of small-sized phototrophs. Freshw. Rev., 1, 128.CrossRefGoogle Scholar
Callieri, C. and Pinolini, M.L., 1995. Picoplankton in lake maggiore, Italy. Int. Rev. Gesamten. – Hydrobiol., 80, 491501.CrossRefGoogle Scholar
Callieri, C. and Stockner, J.G., 2002. Freshwater autotrophic picoplankton: a review. J. Limnol., 61, 114.CrossRefGoogle Scholar
Carrias, J.F., Amblard, C. and Bourdier, G., 1996. Protistan bacterivory in a oligo mesotrophic lake: importance of attached ciliates and flagellates. Microb. Ecol., 31, 249268.CrossRefGoogle Scholar
Casamayor, E.O., Schafer, H., Baneras, L., Pedro-Alio, C. and Muyzer, G., 2000. Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl. Environ. Microb., 66, 499508.CrossRefGoogle ScholarPubMed
Castberg, T., Larsen, A., Sandaa, R.A., Brussaard, C.P.D., Egge, J.K., Heldal, M., Thyrhaug, R., Van Hannen, E.J. and Bratbak, G., 2001. Microbial population dynamics and diversity during a bloom of the marine coccolithophorid Emiliania huxleyi (Haptophyta). Mar. Ecol. Prog. Ser., 221, 3946.CrossRefGoogle Scholar
Cellamare, M., Rolland, A. and Jacquet, S., 2010. Flow cytometry sorting of freshwater phytoplankton. J. Appl. Phycol., 22, 87100.CrossRefGoogle Scholar
Chang, J., Lin, K.H., Chen, K.M., Gong, G.C. and Chiang, K.P., 2003. Synechococcus growth and mortality rates in the East China Sea: range of variations and correlation with environmental factors. Deep Sea Res. II, 50, 12651278.CrossRefGoogle Scholar
Chen, F., Lu, J.R., Binder, B.J., Liu, Y.C. and Hodson, R.E., 2001. Application of digital image analysis and flow cytometry to enumerate marine viruses stained with SYBR gold. Appl.  Environ. Microb., 67, 539545.CrossRefGoogle ScholarPubMed
Chisholm, S.W., Armbrust, E.W. and Olson, R.J., 1986. The individual cell in phytoplankton ecology: cell cycles and applications of flow cytometry. In: Platt, T. and Li, W.K.W. (eds.), Photosynthetic Picoplankton. Can. J. Fish. Aqua. Sci. Ottawa, 343369.Google Scholar
Clasen, J.L., Brigden, S.M., Payet, J.P. and Suttle, C.A., 2008. Evidence that viral abundance across oceans and lakes is driven by different biological factors. Freshw. Biol., 53, 10901100.CrossRefGoogle Scholar
Cochlan, W.P., Wilkner, J., Steward, G.F., Smith, D.C. and Azam, F., 1993. Spatial distribution of viruses, bacteria, chorophyll a in neritic, oceanic and estuarine environments. Mar. Ecol. Prog. Ser., 92, 7787.CrossRefGoogle Scholar
Colombet, J., Sime-Ngando, T., Cauchie, H.M., Fonty, G., Hoffmann, L. and Demeure, G., 2006. Depth-related gradients of viral activity in Lake Pavin. Appl. Environ. Microb., 72, 44404445.CrossRefGoogle ScholarPubMed
Culley, A.I. and Welschmeyer, N.A., 2002. The abundance, distribution and correlation of viruses, phytoplankton and prokaryotes along a Pacific Ocean transect. Limnol. and Ocean., 47, 15081513.CrossRefGoogle Scholar
Dauta, A. and Feuillade, J., 1995. Croissance et dynamique des populations algales. In: Pourriot, R. and Meybeck, M. (eds.), Limnologie générale, Masson, Paris Milan, Barcelone. Collec. Ecol. 328350.Google Scholar
DeBruyn, J.M., Leigh-Bell, J.A., McKay, R.M.L., Bourbonniere, R.A. and Wilheim, S.W., 2004. Microbial distributions and the impact of phosphorus on bacterial activity in Lake Erie. J. Great Lake Res. 30, 166183.CrossRefGoogle Scholar
Djemali, I., Kraïem, M.M., Cadic, N., Porteau, J.P., El Abed, A. and Jarboui, O., 2003. Evaluation de la biomasse piscicole en eau douce par echoprospection: application à la retenue de Sidi Salem. Bull. Inst. Natn. Sci. Tech. Mer Salammbô, 30, 2332.Google Scholar
Dolédec, S. and Chessel, D., 1989. Rythmes saisonniers et composantes stationnelles en milieu aquatique. II. Prise en compte et élimination d'effets dans un tableau faunistique. Acta Oecol. Oec. Gen., 10, 207332.Google Scholar
Dorigo, U., Jacquet, S. and Humbert, J.F., 2004. Cyanophage diversity, inferred from 20 gene analyses, in the largest natural lake in France, Lake Bourget. Appl. Environ. Microb., 70, 10171022.CrossRefGoogle Scholar
Ducklow, H.W., Schultz, G., Raymond, P., Bauer, J. and Shiah, F.K., 1999. Bacterial dynamics in large and small estuaries. In: Bell, C.R., Brylinsky, M. and Johnson-Green, P. (eds.), Microb. Ecol. of estua. – Atlan. Can, Society for Microb. Ecol., Halifax Canada, 105111.Google Scholar
Duhamel, S. and Jacquet, S., 2006. Flow cytometric analysis of bacteria- and virus-like particles in lake sediments. J. Microb. Methods, 64, 316332.CrossRefGoogle ScholarPubMed
El Herry, S., Fathalli, A., Ben Rejeb Jenhani, A. and Bouaïcha, N., 2008. Seasonal occurrence and toxicity of Microcytis spp. and Oscillatoria tenuis in the Lebna Dam, Tunisia. Water Res., 42, 12631273.CrossRefGoogle Scholar
Fahnenstiel, G.L. and Carrick, H.J., 1992. Phototrophic picoplankton in lakes Huron and Michigan: abundance, distribution, composition and contribution to biomass and production. Can. J. Fish. Aqua. Sci., 49, 379388.CrossRefGoogle Scholar
Fathalli, A., Ben Rejeb Jenhani, A., Romdhane, M.S. and Bouaïcha, N., 2006. Contribution à la caractérisation phytoplanctonique et écotoxicologique des eaux de la retenue de barrage Kasseb. Water, Waste and Environment Research, 6, 3342.Google Scholar
Fischer, U.R. and Velimirov, B., 2002. High control of bacterial production by viruses in a eutrophic oxbow lake. Aqua. Microb. Ecol., 27, 112.CrossRefGoogle Scholar
Fouilland, E. and Mostajir, B., 2010. Revisited phytoplanktonic carbon dependency of heterotrophic bacteria in freshwater, transitional, coastal and oceanic waters. FEMS – Microb. Ecol., 73, 419429.CrossRefGoogle ScholarPubMed
Frederickson, C.M., Short, S.M. and Suttle, C.A., 2003. The physical environment affects cyanophage communities in British Columbia inlets. Microb. Ecol. 46, 348357.CrossRefGoogle ScholarPubMed
Fuhrman, J.A., 1999. Marine viruses and their biogeochemical and ecological effects. Nature, 399, 541548.CrossRefGoogle ScholarPubMed
Fuhrman, J.A. and Suttle, C.A., 1993. Viruses in marine planktonic system. Oceanography, 6, 5163.CrossRefGoogle Scholar
Goddard, V., Baker, A.C., Davy, J.E. et al., 2005. Temporal distribution of viruses, bacteria and phytoplankton throughout the water column in a freshwater hypereutrophic lake. Aquat. Microb. Ecol. 39, 211223.CrossRefGoogle Scholar
Harris, G.P., 1980. Temporal and spatial scales in phytoplankton ecology. Mechanisms, methods, model and management. Can. J. Fish. Aqua. Sci., 37, 877900.CrossRefGoogle Scholar
Hennes, K.P. and Simon, M., 1995. Significance of bacteriophages for controlling bacterioplankton growth in a mesotrophic lake. Appl. Environ. Microb., 61, 333340.Google Scholar
Herbland, A., Le Bouteiller, A. and Raimbault, P., 1985. Size structure of phytoplankton biomass in the equatorial Atlantic Ocean. Deep Sea Res., 32, 819836.CrossRefGoogle Scholar
Houlahan, J.E., Currie, D.J., Cottenie, K., Cumming, G.S., Ernest, S.K., Findlay, C.S., Fuhlendorf, S.D., Gaedke, U., Legendre, P., Magnuson, J.J., McArdle, B.H., Muldavin, E.H., Noble, D., Russell, R., Stevens, R.D., Willis, T.J., Woiwod, I.P. and Wondzell, S.M., 2007. Compensatory dynamics are rare in natural ecological communities. Proc. Natl. Acad. Sci. USA, 104, 32733277.CrossRefGoogle ScholarPubMed
Jacquet, S., Heldal, M., Iglesias-Rodriguez, D., Larsen, A., Wilson, W.H. and Bratbak, G., 2002. Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aqua. Microb. Ecol., 27, 111124.CrossRefGoogle Scholar
Jacquet, S., Domaizon, I., Personnic, S., Duhamel, S., Heldal, M., Pradeep Ram, A.S. and Sime-Ngando, T., 2005. Estimates of protozoan and virus-mediated mortality of bacterioplankton in Lake Bourget (France). Freshw. Biol., 50, 627645.CrossRefGoogle Scholar
Jacquet, S., Miki, T., Noble, R., Peduzzi, P. and Wilhelm, S., 2010. Viruses in aquatic ecosystems: important advancements of the last 20 years and prospects for the future in microbial oceanography and limnology. Adv. Oceanogr. Limnol., 1, 71101.CrossRefGoogle Scholar
Jacquet, S., Dorigo, U. and Personnic, S., 2013. A few tests prior to flow cytometry and epifluorescence analyses of freshwater bacterioand virioplankton communities, in: Flow Cytometry: Principles,Methodology and Applications, Chapter 1, Related Nova publication, Nova Publishers Inc., New York, 130 p.
Kelley, C.A., Coffin, R.B. and Cifuentes, L.A., 1998. Stable isotope evidence for alternative bacterial carbon sources in the Gulf of Mexico. Limnol. Oceanogr., 43, 19621969.CrossRefGoogle Scholar
Koroleff, F., 1976. Determination of phosphorus. In: Grass-hoff, K. (ed.), Methods of Seawater Analysis. Verlag Chemie, Weinheim, New York.Google Scholar
Larsen, A., T. Castberg, R.A., Sandaa, C.P.D., Brussaard, J., Egge, M., Heldal, A., Paulino, R., Thyrhaug, E., VanHannen, J. and Bratbak, G., 2001. Population dynamics and diversity of phytoplankton, bacteria and viruses in a seawater enclosure. Mar. Ecol. Prog. Ser., 221, 4757.CrossRefGoogle Scholar
Lebaron, P., Servais, P., Baudoux, A.C., Bourrain, M., Courties, C. and Parthuisot, N., 2002. Variations of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry. Aqua. Microb. Ecol., 28, 131140.CrossRefGoogle Scholar
Li, W.K.W. and Dickie, P.M., 2001. Monitoring phytoplankton, bacterioplankton, and virioplankton in a coastal Inlet (Belford bassin) by flow cytometry. Cytometry 44, 236246.3.0.CO;2-5>CrossRefGoogle Scholar
Li, W.K.W., Subba-Rao, D.V., Harrison, W.G., Smith, J.C., Cullen, J.J., Irwin, B. and Platt, T., 1983. Autotrophic picoplankton in the tropical ocean. Science, 219, 29229.CrossRefGoogle ScholarPubMed
Liu, H.B., Dagg, M., Campbell, L. and Urban-Rich, J., 2004. Picophytoplankton and bacterioplankton in the Mississippi River Plume and its adjacent waters. Estuaries, 27, 147156.CrossRefGoogle Scholar
Marie, D., Brussaard, C.P.D., Thyrhaug, R., Bratbak, G. and Vaulot, D., 1999. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl. Environ. Microb. 65, 4552.Google ScholarPubMed
Marie, D., Partensky, F., Simon, N., Guillou, L. and Vaulot, D., 2000. Flow cytometry analysis of marine picoplankton. In: DeMaggio, S. (ed.), Living Colors: Protocols in Flow Cytometry and Cell Sorting, Springer, Berlin, 421454.CrossRefGoogle Scholar
Mathias, C.B., Kirchner, A.K.T. and Velimirov, B., 1995. Seasonal variations of virus abundance and viral control the bacterial production in a backwater system of the Danube River. Appl. Environ. Microb., 61, 37343740.Google Scholar
Mouelhi, S., Defaye, D. and Balvay, G., 2000. Présence de Mesocyclops ogunnus Onabamiro, 1957 (Crustacea: Copepoda) en Tunisie. Ann. Limnol. - Int. J. Lim., 36, 9599.CrossRefGoogle Scholar
Nagata, T., Takai, K. and Kawanobe, K., 1994. Autotrophic picoplankton in southern Lake Baikal abundance, growth and grazing mortality during summer. J.  Plank. Res., 16, 945959.CrossRefGoogle Scholar
Padisák, J., Krienitz, L., Scheffler, W., Koschel, R., Kristiansen, J. and Grigorszky, I.,1998. Phytoplankton succession in the oligotrophic Lake Stechlin (Germany) in 1994 and 1995. Hydrobiologia, 369/370, 179197.CrossRefGoogle Scholar
Padisák, J., Barbosa, F.A.R., Koschel, R. and Krienitz, L., 2003. Deep layer cyanoprokaryota maxima are constitutional features of lakes: examples from temperate and tropical regions. Arch. Hydrobiol. Spec. Issues. Adv. Limnol., 58, 175199.Google Scholar
Pan, L.A., Zhang, L.H., Zhang, J., Gasol, J.M. and Chao, M., 2005. On-board flow cytometric observation of picoplankton community structure in the East China Sea during the fall of different years. FEMS Microbiol. Ecol., 52, 243253.CrossRefGoogle ScholarPubMed
Parvathi, A., Zhong, X., Pradeep Ram, A.S. and Jacquet, S., 2014. Dynamics of auto- and heterotrophic picoplankton and associated viruses in Lake Geneva. Hydrol. Earth Syst. Sci., 18, 10731087.CrossRefGoogle Scholar
Payet, J.P. and Suttle, C.A., 2008. Physical and biological correlates of virus dynamics in the southern Beaufort Sea and Amundsen Gulf. J. Mar. Syst., 74, 933945.CrossRefGoogle Scholar
Personnic, S., Domaizon, I., Dorigo, U., Berdjeb, L. and Jacquet, S., 2009. Seasonal and spatial variability of virio-, bacterio-, and picophytoplanktonic abundances in three peri-alpine lakes. Hydrobiologia, 627, 99116.CrossRefGoogle Scholar
Pradeep Ram, A.S., Arnous, B., Danger, M., Carrias, J.F., Lacroix, G. and Sime-Ngando, T., 2010. High and differential viral infection rates within bacterial ‘morphopopulations’ in a shallow sand pit lake (Lac de Creteil, France). FEMS Microbiol. Ecol., 74, 8392.CrossRefGoogle Scholar
Rachiq, S., Raoui, M., Chadli, N., Amblard, C., Alaoui, M.M., Carria, J.F., Sime-Ngando, T. and Sargos, D., 2002. Potentialités phagotrophes des phytoflagellés dans la retenue de barrage Allal El Fassi (Maroc). Rev. Sci. Eau, 15, 8799.Google Scholar
Ryding, S.O. and Rast, W., 1994. Le contrôle de l'eutrophisation des lacs et des réservoirs. Collection Sciences de l'environnement. Masson UNESCO Paris, 261 p.
Sarmiento, J.L. and Gruber, N., 2006. Ocean Biogeochemical Dynamics, Princeton University Press, Princeton, New Jersey, USA.Google Scholar
Schallenberg, M. and Burns, C.W., 2001. Tests of autotrophic picoplankton as early indicators of nutrient enrichment in an ultra-oligotrophic lake. Freshw. Biol., 46, 2737.CrossRefGoogle Scholar
Sellami, I., Ayadi, H., Bouain, A., Aleya, L. and Mhamdi, M.H., 2009. Distribution of zooplankton related to environmental factors in three interconnected reservoirs: Kasseb, Mornaguia and Ghdir El Goulla (North of Tunisia). Ann. Limnol. - Int. J. Lim. 45, 107117.CrossRefGoogle Scholar
Sellami, I., Ben Romdhane, S., Guermazi, W., El Bour, M., Hamza, A., Mhamdi, M.H., Pinel-Alloul, B., Aleya, L. and Ayadi, H., 2012. Seasonal dynamics of plankton communities coupled with environmental factors in a semi arid area: Sidi Saâd reservoir (Center of Tunisia). Afric. J. Biotechnol., 11, 865877.Google Scholar
Shiah, F.K. and Ducklow, H.W., 1994. Temperature regulation of heterotrophic bacterioplankton biomass, production and specific growth rate in the Chesapeake Bay. Limnol. Oceanogr., 39, 12431258.CrossRefGoogle Scholar
Short, S.M. and Suttle, C.A., 2003. Temporal dynamics of natural communities of marine algal viruses and eukaryotes. Aquat. Microb. Ecol., 32, 107119.CrossRefGoogle Scholar
Simek, K., Pernthaller, J., Weinbauer, M.G., Hornak, K., Dolan, J.R., Nedoma, J., Masin, M. and Amann, R., 2001. Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl. Environ. Microb., 67, 27232733.CrossRefGoogle Scholar
Stockner, J.G. and Antia, N.J., 1986. Algal picoplankton from marine and freshwater: a multidisciplinary perspective. Can. J. Fish. Aquat. Sci., 43, 24722503.CrossRefGoogle Scholar
Stockner, J.G. and Shortreed, K.S., 1994. Autotrophic picoplankton community dynamics in a pre-alpine lake in British Columbia, Canada. Hydrobiologia, 274, 133142.CrossRefGoogle Scholar
Stockner, J.G., Callieri, C. and Cronberg, G., 2000. Picoplankton and other non-bloom forming cyanobacteria in lakes. In: Whitton, B. and Potts, M. (eds.), Ecology of Cyanobacteria: Their Diversity in Time and Space, Kluwer Academic Publishers, Dordrect, 195231 p.Google Scholar
Suttle, C.A., 2005. Viruses in the sea. Nature, 437, 356361.CrossRefGoogle Scholar
Szelag-Wasielewska, E., 1999. Picoplankton and other size groups of phytoplankton in various shallow lakes. Hydrobiologia, 342/343, 7985.CrossRefGoogle Scholar
Tijdens, M., Hans, L., Hoogveld Miranda, P., Kamst-van, A., Stefan, G.H., Simis Baudoux, A., Hendrikus, C., Laanbroek, J. and Herman, J.G., 2008. Population dynamics and diversity of viruses, bacteria and phytoplankton in a shallow eutrophic lake. Microb. Ecol., 56, 2942.CrossRefGoogle Scholar
Tsai, A.Y., Gong, G.C., Chiang, K.P., Chao, C.F., Liao, H.K. and Shiah, F.K., 2011. Temporal and spatial variations of picoplankton and nanoplankton and short-term variability related to stormy weather in the Danshui River estuary in northern Taiwan. Terrest. Atmos. Ocea. Sci., 22, 7989.Google Scholar
Turki, S., 2002. Contribution à l'étude bio-écologique des rotifères, cladocères, copépodes des eaux continentales Tunisiennes et dynamique saisonnière du zooplancton de la retenue du barrage Bir M'Chergua. Thèse doct. instit. Nat. Sci. Tech. de la mer. 203 p.Google Scholar
Vaque, D., Casamayor, E.O. and Gasol, J.M., 2001. Dynamics of whole community bacterial production and grazing losses in seawater incubations as related to the changes in the proportions of bacteria with different DNA content. Aquat. Microb. Ecol., 25, 163177.CrossRefGoogle Scholar
Vaulot, D., 1989. CYTOPC: processing software for flow cytometric data. Signal Noise, 2, 8.Google Scholar
Vila, X. and Abella, C.A., 2001. Light- harvesting adaptations of planktonic phototrophic micro-organisms to different light quality conditions. Hydrobiologia, 452, 1530.CrossRefGoogle Scholar
Voros, L., Callieri, C., Balogh, K.V. and Bertoni, R., 1998. Freshwater picocyanobacteria along a trophic gradient and light quality range. Hydrobiologia, 369/370, 117125.CrossRefGoogle Scholar
Vrede, K., Vrede, T., Isaksson, A. and Karlsson, A., 1999. Effects of nutrients (phosphorous, nitogen and carbon) and zooplankton on bacterioplankton and phytoplankton - a seasonal study. Limnol. Oceanogr., 44, 16161624.CrossRefGoogle Scholar
Waite, A.M., Safi, K.A., Hall, J.A. and Nodder, S.D., 2000. Mass sedimentation of picoplankton embedded in organic aggregates. Limnol. Oceanogr., 45, 8797.CrossRefGoogle Scholar
Wakabayashi, T. and Ichise, S., 2004. Seasonal variation ofphototrophic picoplankton in Lake Biwa (1994–1998). Hydrobiologia, 528, 116.CrossRefGoogle Scholar
Wang, B., Liu, F., Wang, C.Q., Yu, Y. and Wu, Y., 2009. Flow cytometric observation of picophytoplankton community structure in the cascade reservoirs along the Wujiang River, SW China. J. Limnol., 68, 5363.CrossRefGoogle Scholar
Wehr, J.D., 1993. Effects of experimental manipulation of light and phosphorus supply on competition among picoplankton and nanoplankton in oligotrophic lake. Can. J. Fish. Aquat. Sci. 50, 936945.CrossRefGoogle Scholar
Weinbauer, M.G., 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev., 28, 127181.CrossRefGoogle ScholarPubMed
Weinbauer, M.G. and Hofle, M.G., 1998. Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Appl. Environ. Microb., 64, 431438.Google Scholar
Weinbauer, M.G. and Peduzzi, P., 1995. Effect of virus-rich high molecular weight concentrates of seawater on the dynamics of dissolved amino acids and carbohydrates. Mar. Ecol. Prog. Ser., 127, 245253.CrossRefGoogle Scholar
Weinbauer, M.G. and Rassoulzadegan, F., 2004. Are viruses driving microbial diversification and diversity. Environ. Microb., 6, 111.CrossRefGoogle ScholarPubMed
Weisse, T., 1993. Dynamics of autotrophic picoplankton in marine and freshwater ecosystems. In: Jones, J.G. (ed.), Advances in Microbial Ecology, Plenum, New York, 327370.CrossRefGoogle Scholar
Weisse, T. and Schweizer, A., 1991. Seasonal and interannual variation of autotrophic picoplankton in a large prealpine lake (Lake Constance). Verhand lungender Internationale Vereinigung fur Theoretische undangewandte Limnologie, 24, 821825.Google Scholar
Welschmeyer, NA., 1994. Fluorimetric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol. Ocean., 39, 19851992.CrossRefGoogle Scholar
Whitman, W.B., Coleman, D.C. and Wiebe, W.J., 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA, 95, 65786583.CrossRefGoogle ScholarPubMed
Wilson, W.H. and Mann, N.H., 1997. Lysogenic and lytic viral production in marine microbial communities. Aquat. Microb. Ecol., 13, 95100.CrossRefGoogle Scholar
Wommack, K.E. and Colwell, R.R., 2000. Virioplankton: viruses in aquatic ecosystems. Microb. Mol. Biol. Rev., 64, 69114.CrossRefGoogle ScholarPubMed
Wommack, K., Hill, R.T., Kessel, M., Russek-Cohen, E. and Colwell, R.R., 1992. Distribution of viruses in the Chesapeake Bay. Appl. Environ. Microb., 58, 29652970.Google ScholarPubMed
Wommack, K., Ravel, J., Hill, R.T., Chun, J.S. and Colwell, R.R., 1999. Population dynamics of Chesapeake bay virioplankton: total community analysis by pulsed-field gel electrophoresis. Appl. Environ. Microbiol., 65, 231240.Google ScholarPubMed
Worden, A.Z. and Not, F., 2008. Ecology and diversity of picoeukaryotes In: Kirchman, D. (ed.), Book Chapter in: Microbial Ecology of the Ocean (2nd edn), Wiley, San Francisco.Google Scholar
Yuan, X.C., He, L., Yin, K.D., Pan, G. and Harrison, P.G., 2011. Bacterial distribution and nutrient limitation in relation to different water masses in the coastal and northwestern South China Sea in late summer. Continent. Shelf Res., 31, 12141223.CrossRefGoogle Scholar
Zhang, X., Zhen, S., Qingxia, L., Feng, Y., Lei, T. and Xiaoping, H., 2013. Spatial and temporal variations of picoplankton in three contrasting periods in the Pearl River Estuary, South China. Continent. Shelf Res., 15, 10162013.Google Scholar

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Seasonal patterns of viral, microbial and planktonic communities in Sidi Salem: a freshwater reservoir (North of Tunisia)
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Seasonal patterns of viral, microbial and planktonic communities in Sidi Salem: a freshwater reservoir (North of Tunisia)
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