HESS Hydrology and Earth System Sciences HESS Hydrol. Earth Syst. Sci. 1607-7938 Copernicus Publications Göttingen, Germany 10.5194/hess-18-1073-2014 Dynamics of auto- and heterotrophic picoplankton and associated viruses in Lake Geneva Parvathi A. 1 2 Zhong X. 2 Pradeep Ram A. S. 3 Jacquet S. 2 National Institute of Oceanography, Dr Salim Ali Road, P.O. Box 1913, 682018 Kochi, India INRA – UMR042 CARRTEL, 75 Avenue de Corzent, 74203 Thonon-les-Bains cx, France Laboratoire Microorganismes, Génome et Environnment, CNRS – UMR6023, Clermont Université, Université Blaise Pascal, BP 80026, 63171 Aubière Cedex, France 19 03 2014 18 3 1073 1087 Copyright: © 2014 A. Parvathi et al. 2014 This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/ This article is available from https://hess.copernicus.org/articles/18/1073/2014/hess-18-1073-2014.html The full text article is available as a PDF file from https://hess.copernicus.org/articles/18/1073/2014/hess-18-1073-2014.pdf

Microbial dynamics have rarely been investigated in Lake Geneva, known as the largest lake in western Europe. From a 5-month survey, we report dynamic patterns of free-living virus, bacteria and small phytoplankton abundances in response to a variety of environmental parameters. For the first time, we fractionated the primary production to separate the contribution of different size-related biological compartments and measured both bacterial and viral production in addition to experiments conducted to quantify the virus-induced bacterial mortality. We observed marked seasonal and vertical variations in picocyanobacteria, bacteria and virus abundances and production. The contribution of picoplankton and nanoplankton production to the total primary production was high (reaching up to 76% of total primary production) in November and the spring–summer transition period, respectively. The impact of viral lysis on both bacteria and picocyanobacteria was significantly higher than grazing activities. Virus-induced picocyanobacterial mortality reached up to 66% of cell removal compared to virus induced (heterotrophic) bacterial mortality, which reached a maximum of 34% in July. Statistical analyzes revealed that temperature and top-down control by viruses are among important factors regulating the picocyanobacterial dynamics in this lake. More generally speaking, our results add to the growing evidence and accepted view nowadays that viruses are an important actor of freshwater microbial dynamics and more globally of the functioning of the microbial food webs.

 References Anneville, O., Souissi, S., Ibanez, F., Ginot, V., Druart, J. C., and Angeli, N.: Temporal mapping of phytoplankton assemblages in Lake Geneva: Annual and interannual changes in their patterns of succession, Limnol. Oceanogr., 47, 1355–1366, 2002. Anneville, O., Gammeter, S., and Straile, D.: Phosphorus decrease and climate variability: mediator of synchrony in phytoplankton changes among European peri-alpine lakes, Freshwater Biol., 50, 1731–1746, 2005. Anneville, O., Molinero, J. C., Souissi, S., Balvay, G., and Gerdeaux D.: Long-term changes in the copepod community of Lake Geneva, J. Plankton Res., 29, 49–59, 2007. Anneville, A., Beniston, M., Gallina, N., Gillet, C., Jacquet, S., and Perroud, M.: L'empreinte du changement climatique dans le Léman, Arch. Sci., 66, 157–172, 2013. Auguet, J. C., Barberan, A., and Casamayor, E. O.: Global ecological patterns in uncultured archaea, ISME J., 4, 182–190, 2010. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., and Thingstad, F.: The ecological role of watercolumn microbes in the sea, Mar. Ecol.-Prog. Ser., 10, 257–263, 1983. Berdjeb, L., Pollet, T., Domaizon, I., and Jacquet, S.: Effects of grazers and viruses on bacterial community structure and production in two contrasting trophic lakes, BMC Microb., 11, 1–18, 2011. Bettarel, Y., Sime-Ngando, T., Amblard, C., and Dolan, J. R.: Viral activity in two contrasting lake ecosystems, Appl. Environ. Microbiol., 70, 2941–2951, 2004. Bettarel, Y., Sime-Ngando, T., Bouvy, M., Arfi, R., and Amblard, C.: Low consumption of virus-sized particles by heterotrophic nanoflagellates in two lakes of the French Massif Central, Aquat. Microb. Ecol., 39, 205–209, 2005. Binder, B. J.: Reconsidering the relationship between virally-induced bacterial mortality and frequency of infected cells, Aquat. Microb. Ecol., 18, 207–215, 1999. Bird, C. and Wyman, M.: Nitrate/nitrite assimilation system of the marine cyanobacterium <i>Synechococcus</i> sp. strain WH8103: Effect of nitrogen source and availability on gene expression, Appl. Environ. Microbiol., 69, 7009–7018, 2003. Breitbart, M.: Marine viruses: truth or dare, Ann. Rev. Mar. Sci., 4, 425–448, 2012. Callieri, C.: Picophytoplankton in freshwater ecosystems: the importance of small-sized phototrophs, Freshwater Rev., 1, 1–28, 2008. Callieri, C.: Single cells and microcolonies of freshwater picocyanobacteria: a common ecology, J. Limnol., 69, 257–277, 2010. Callieri, C. and Stockner, J. G.: Freshwater autotrophic picoplankton: a review, J. Limnol., 61, 1–14, 2002. Chen, C. Y. and Durbin, E. G.: Effects of pH on the growth and carbon uptake of marine phytoplankton, Mar. Ecol.-Prog. Ser., 109, 83–94, 1994. Clasen, J. L., Brigden, S. M., Payet, J. P., and Suttle, C. A.: Evidence that viral abundance across oceans and lakes is driven by different biological factors, Freshwater Biol., 53, 1090–1100, 2008. Colombet, J., Sime-Ngando, T., Cauchie, H. M., Fonty, G., Hoffmann, L., and Demeure, G.: Depth-related gradients of viral activity in Lake Pavin, Appl. Environ. Microbiol., 72 , 4440–4445, 2006. Dilon, P. J. and Rigler, F. H.: The phosphorus-chlorophyll relationship in lakes, Limnol. Oceanogr. 19, 767–773, 1974. Duhamel, S. and Jacquet, S.: Flow cytometric analysis of bacteria- and virus-like particles in lake sediments, J. Microbiol. Meth., 64, 316–322, 2006. Duhamel, S., Zeman, F., and Thierry, M.: A dual-labeling method for the simultaneous measurement of dissolved inorganic carbon and phosphate uptake by marine planktonic species, Limnol. Oceanogr. Meth., 4, 416–425, 2005. Duhamel, S., Domaizon, I., Personnic, S., and Jacquet, S.: Assessing the microbial community dynamics and the role of viruses as bacterial mortality agents in Lake Geneva, J. Water Sci., 19, 115–126, 2006. Evans, C., Archer, S. D., Jacquet, S., and Wilson, W. H.: Direct estimates of the contribution of viral lysis and microzooplankton grazing to the decline of a <i>Micromonas</i> spp. population, Aquat. Microb. Ecol., 30, 207–219, 2003. Fuhrman, J. A. and Noble, R. T.: Viruses and protists cause similar bacterial mortality in coastal seawater, Limnol. Oceanogr., 40, 1236–1242, 1995. Gasol, J. M. and Duarte, C. M.: Comparative analyses in aquatic microbial ecology: how far do they go?, FEMS Microbiol. Ecol., 31, 99–106, 2000. Glover, H. E., Phinney, D. A., and Yentsch, C. S.: Photosynthetic characteristics of picoplankton compared with those of higher phytoplankton populations in various water masses in the Gulf of Maine, Biol. Oceanogr., 3, 223–248, 1985. Goldman, J. C.: Temperature effects on phytoplankton growth in continuous culture, Limnol. Ocean., 22, 932–935, 1977. Harris, G. P.: Phytoplankton ecology: Structure, function, and fluctuationm Chapman and Hall, London, UK, 1986. Hutchinson, G. E.: A treatise on limnology, Vol. 2, Wiley, New York, 1967. Ishiguro, N. and Balvay, G.: L'écoulement des eaux du Rhône dans le lac Léman, Archs Sci. Genève, 56, 117–126, 2003. Jacquet, S., Havskum, H., Thingstad, F. T., and Vaulot, D.: Effect of inorganic and organic nutrient addition on a coastal microbial community (Isefjord, Denmark), Mar. Ecol.-Prog. Ser., 228, 3–14, 2002. Jacquet, S., Miki, T., Noble, R., Peduzzi, P., and Wilhelm, S.: 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, 71–101, 2010. Jacquet, S., Barbet, D., Cachera, S., Caudron, A., Colon, M., Girel, C., Guillard, J., Hébert, A., Kerrien, F., Laine, L., Lazzarotto, J., Moille, J.-P., Paolini, G., Perga, M.-E., Perney, P., and Rimet, F.: Suivi environnemental des eaux du lac du Bourget pour l'année 2011, Rapport INRA-CISALB-CALB, p. 220, 2012. Jacquet, S., Dorigo, U., and Personnic, S.: A few tests prior to flow cytometry and epifluorescence analyses of freshwater bacterio- and virioplankton communities, in: Flow Cytometry: Principles, Methodology and Applications, Chapter 1, Related Nova publication, Nova Publishers Inc., New York, 1–30, 2013. Jugnia, L. B., Tadonléké, R. D., Sime-Ngando, T., Devaux, J., and Andrivon, C.: Bacterial population dynamics, production, and heterotrophic activity in a recently formed reservoir, Can. J. Microbiol., 45, 747–753, 1999. Kimmance, S. A., Wilson, W. H., and Archer, S. D.: Modified dilution technique to estimate viral versus grazing mortality of phytoplankton: limitations associated with method sensitivity in natural waters, Aquat. Microb. Ecol., 49, 207–222, 2007. Lazzarotto, J. and Klein, A.: Evolution physico-chimique des eaux du Léman, rapport CIPEL pour l'année 2011, 26–50, 2012. Lemmin, U., Fer, I., and Perrinjaquet, C.: Courantologie lémanique: le refroidissement hivernal, in: Découvrir le Léman 100 ans après François-Alphonse Forel, Actes du colloque pluridisciplinaire, Editions Slatkine, Nyon-Genève, 53–67, 1999. Li, W. K. W., Subba-Rao, D. V., Harrison, W. G., Smith, J. C., Cullen, J. J., Irwin, B., and Platt, T.: Autotrophic picoplankton in the tropical ocean, Science, 219, 292–295, 1983. Maranger, R. and Bird, D. F.: Viral abundance in aquatic systems: a comparison between marine and fresh waters, Mar. Ecol.-Prog. Ser., 121, 217–226, 1995. Olson, R. J., Chisholm, S. W., Zettler, E. R., Altabet, M., and Dusenberry, J.: Spatial and temporal distributions of prochlorophyte picoplankton in the North Atlantic ocean, Deep-Sea Res., 37, 1033–1051, 1990. Parvathi, A., Zhong, X., and Jacquet, S.: Dynamics of various viral groups infecting autotrophic plankton in Lake Geneva, Adv. Ocean. Limnol., 3, 171–191, 2012. Pelletier, J. P. and Orand, A.: Appareil de prelevement d'un echantillon dans un fluide, INRA Patent number 1978 76.08579, 1978. Personnic, S., Domaizon, I., Dorigo, U., Berdjeb, L., and Jacquet, S.: Seasonal and spatial variability of virio-, bacterio, and picophytoplanktonic abundances in three peri-alpine lakes, Hydrobiologia, 627, 99–116, 2009a. Personnic, S., Domaizon, I., Sime-Ngando, T., and Jacquet, S.: Seasonal variations of microbial abundances and of virus- vs. flagellate- induced mortality of picophytoplankton in some peri-alpine lakes, J. Plankton Res., 31, 1161–1177, 2009b. Platt, T., Subba-Rao, D. V., and Irwin, B.: Photosynthesis of picoplankton in the oligotrophic ocean, Nature, 300, 701–704, 1983. Pradeep Ram, A. S., Boucher, D., Sime-Ngando, T., Debroas, D., and Romagoux, J. C.: Phage bacteriolysis, protistan bacterivory, and bacterial production in a freshwater reservoir: coupling with temperature, Microb. Ecol., 50, 64–72, 2005. Pradeep Ram, A. S., Arnous, B., Danger, M., Carrias, J. F., Lacroix, G., and Sime-Ngando, T.: High and differential viral infection rates within bacterial 'morphopopulations' in a shallow sand pit lake (Lac de Creteil, France), FEMS Microbiol. Ecol., 74, 83–92, 2010. Raven, J. A.: The twelfth Tansley Lecture: Small is beautiful: The picophytoplankton, Funct. Ecol., 12, 503–513, 1998. Rushansky, N. M., Berman, T., Berner T., Yacobi, Y. Z., and Dubinsky, A. Z.: Physiological characteristics of picophytoplankton, isolated from Lake Kinneret: responses to light and temperature, J. Plankton Res., 24, 1173–1183, 2002. Sarmiento, J. L. and Gruber, N.: Ocean Biogeochemical Dynamics, Princeton University Press, Princeton, New Jersey, USA, 2006. Shapiro, J: Current beliefs regarding dominance by blue-greens: the case for the importance of CO<sub>2</sub> and pH, Verhand. Int. Ver. Theor. Angew. Limnol., 24, 38–54, 1990. Sime-Ngando, T., Mignot, J. P., Amblard, C., Bourdier, G., Desvilettes, C., and Quiblier-Lloberas, C.: Charactérisation des particules virales planctoniques dans un lac du Massif Central Français: Aspects méthodologiques et premiers résultats, Annales de Limnology – International Journal of Limnology, 32, 259–263, 1996. Stockner, J. G. and Porter, K. G.: Microbial food webs in fresh water planktonic ecosystems, in: Complex interactions in lake communities, edited by: Carpenter, S. R., Springer-Verlag, New York, 69–83, 1988. Suttle, C. A.: Viruses in the sea, Nature, 437, 356–361, 2005. Tadonléké, D. R.: Evidence of warming effects on phytoplankton productivity rates and their dependence on eutrophication status, Limnol. Oceanogr., 55, 973–982, 2010. Tadonléké, D. R., Planas, D., and Lucotte, M.: Microbial food web in boreal humic lakes and reservoirs: ciliates as a major factor related to the dynamics of the most active bacteria, Microb. Ecol., 49, 325–341, 2005. Tadonléké, D. R., Lazzarotto, J., Anneville, O., and Druart, J.-C.: Phytoplankton productivity increased in Lake Geneva despite phosphorus loading reduction, J. Plankton Res., 31, 1179–1194, 2009. Thomas, R., Berdjeb, L., Sime Ngando, T., and Jacquet, S.: Viral abundance, production, decay rates and life strategies (lysogeny versus lysis) in Lake Bourget (France), Environ. Microbiol., 13, 616–630, 2011. Utermöhl, H.: Neue Wege in der quantitativen Erfassung des Planktons (mit besonderer Berücksichtigung des Ultraplanktons), Verh. Int. Ver. Theor. Angew. Limnol., 5, 567–596, 1931. Vincon-Leite, B., Mouchel, J. M., and Tassin, B.: Modelisation de l'evolution thermique saisonniere du lac du Bourget (Savoie, France), Rev. Des. Sci., 2, 483–510, 1989. Weinbauer, M. G.: Ecology of prokaryotic viruses, FEMS Microbiol. Rev., 28, 127–181, 2004. Weinbauer, M. G. and HÖfle, M. G.: Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake, Appl. Environ. Microbiol., 64, 431–438, 1998. Weinbauer, M. G. and Suttle, C. A.: Comparison of epi-fluorescence and transmission electron microscopy for counting viruses in natural marine waters, Aquat. Microb. Ecol., 13, 225–232, 1997. Weinbauer, M. G., Winter, C., and Hofle, M.: Reconsidering transmission electron microscopy based estimates of viral infection of bacterioplankton using conversion factors derived from natural communities, Aquat. Microb. Ecol., 27, 103–110, 2002. Wetzel, R. G.: Limnology, lake and river ecosystems, Academic Press, 3rd Edn., London, UK, p. 1006, 2000. Whitman, W. B., Coleman, D. C., and Wiebe, W. J.: Prokaryotes: the unseen majority, P. Natl. Acad. Sci., 95, 6578–6583, 1998. Wilhelm, S. W., Brigden, S. M., and Suttle, C. A.: A dilution technique for the direct measurement of viral production: a comparison in stratified and tidally mixed coastal waters, Microb. Ecol., 43, 168–173, 2002. Worden, A. Z. and Not, F.: Ecology and Diversity of Picoeukaryotes, in: Book Chapter in: Microbial Ecology of the Ocean, 2nd Edn., edited by: Kirchman, D., Wiley, San Francisco, 2008. Worden, A. Z., Nolan, J. K., and Palenik, B.: Assessing the dynamics and ecology of marine picophytoplankton: the importance of the eukaryotic component, Limnol. Oceanogr., 49, 168–179, 2004. Zhong, X., Berdjeb, L., and Jacquet, S.: Temporal dynamics and structure of picocyanobacteria and cyanomyoviruses in two large and deep peri-alpine lakes, FEMS Microbiol. Ecol., 86, 312–326, 2013.