Seasonal and spatial variability of virio-, bacterio-, and picophytoplanktonic abundances in three peri-alpine lakes
- 331 Downloads
- 30 Citations
Abstract
Flow cytometry (FCM) was used to assess microbial community abundances and patterns in three natural, large and deep peri-alpine hydrosystems, i.e., lakes Annecy (oligotrophic), Bourget, and Geneva (mesotrophic). Picocyanobacteria, small eukaryotic autotrophs, heterotrophic prokaryotes, and viruses were studied in the 0–50 m surface layers to highlight the impact of both physical and chemical parameters as well as possible biotic interactions on the functioning of microbial communities. Some specificities were recorded according to the trophic status of each ecosystem such as the higher number of viruses and heterotrophic bacteria in mesotrophic environments (i.e., Lakes Geneva and Bourget) or the higher abundance of picocyanobacteria in the oligotrophic Lake Annecy. However, both seasonal (temperature) and spatial (depth) variations were comparatively more important than the trophic status in driving the microbial communities’ abundances in these three lakes, as revealed by principal component analysis (PCA). A strong viral termination of the heterotrophic bacterial blooms could be observed in autumn for each lake, in parallel to the mixing of the upper lit layers. As virus to bacteria ratio (VBR) was indeed very high at this period with values varying between 87 and 114, such important relationships between viruses and bacteria were likely. The magnitudes of seasonal variations in VBR, with the highest values ever reported so far, were largely greater than the magnitude of theoretical variations due to the trophic status, suggesting also a strong seasonality in virioplankton production associated to prokaryotic dynamics. FCM analyses allowed discriminating several viral groups. Virus-Like Particles group 1 (VLP1) and group 2 (VLP2) were always observed and significantly correlated to bacteria for the former and chlorophyll a and picocyanobacteria for the latter, suggesting that most of VLP1 and VLP2 could be bacteriophages and cyanophages, respectively. On the basis of these results, new ways of investigation emerge concerning the study of relationships between specific picoplanktonic groups; and overall these results provide new evidence of the necessity to consider further viruses for a better understanding of lake plankton ecology.
Keywords
Viruses Bacteria Flow cytometry Lake Trophic statusNotes
Acknowledgments
Monika Ghosh is acknowledged for improving the English. SP was funded by a grant from the French Research and Technology Ministry. This is a contribution to the French ANR project AQUAPHAGE.
References
- Abedon, S. T., 2006. Phage ecology. In Abedon, C. S. T. (ed.), The Bacteriophages. Oxford University Press, Oxford: 37–46.Google Scholar
- Anesio, A. M., C. Hollas, W. Granéli & J. Laybourn-Parry, 2004. Influence of humic substances on bacterial and viral dynamics in freshwaters. Applied and Environmental Microbiology 70: 4848–4854.PubMedCrossRefGoogle Scholar
- Azam, F., T. Fenchel, J. G. Field, J. S. Gray, M. A. Meyer Reil & T. F. Thingstad, 1983. The ecological role of water column microbes in the sea. Marine Ecology Progress Series 10: 257–263.CrossRefGoogle Scholar
- Bergh, O., K. Y. Borsheim, G. Bratbak & M. Heldal, 1989. High abundance of viruses found in aquatic environments. Nature 340: 467–468.PubMedCrossRefGoogle Scholar
- Bouvy, M., R. Arfi, P. Cecchi, D. Corbin, D. Pagano, L. Saint Jean & S. Thomas, 1998. Trophic coupling between bacterial and phytoplanktonic compartments in shallow tropical reservoirs (Ivory Coast, West Africa). Aquatic Microbial Ecology 15: 25–37.CrossRefGoogle Scholar
- Bratbak, G., M. Heldal, S. Norland & T. F. Thingstad, 1990. Viruses as partners in spring bloom microbial trophodynamics. Applied and Environmental Microbiology 56: 1400–1405.PubMedGoogle Scholar
- Bratbak, G., O. H. Haslund, I. M. Head, A. Naess & T. Roeggen, 1992. Giant marine viruses. Marine Ecology Progress Series 85: 201–202.CrossRefGoogle Scholar
- Bratbak, G., M. Heldal, T. F. Thingstad & P. I. Tuomi, 1996. Dynamics of virus abundance in coastal sea water. FEMS Microbiology Ecology 19: 263–269.CrossRefGoogle Scholar
- Breitbart, M., L. R. Thompson, C. A. Suttle & M. B. Sullivan, 2007. Exploring the vast diversity of marine viruses. Oceanography 20: 135–139.Google Scholar
- Brum, J. R., G. F. Stewart, S. C. Jiang & R. Jellison, 2005. Spatial and temporal variability of prokaryotes, viruses, and viral infections of prokaryotes in an alkaline, hypersaline lake. Aquatic Microbial Ecology 41: 247–260.CrossRefGoogle Scholar
- Brussaard, C. P. D., 2004. Optimization of procedures for counting viruses by flow cytometry. Applied and Environmental Microbiology 70: 1506–1513.PubMedCrossRefGoogle Scholar
- Brussaard, C. P. D., S. W. Wilhelm, F. T. Thingstad, M. G. Weinbauer, G. Bratbak, M. Heldal, S. A. Kimmance, M. Middelboe, K. Nagasaki, J. H. Paul, D. C. Schroeder, C. A. Suttle, D. Vaqué & K. E. Wommack, 2008. Global-scale processes with a nanoscale drive: the role of marine viruses. The ISME Journal 2: 575–578.PubMedCrossRefGoogle Scholar
- Callieri, C., 2007. Picocphytoplankton in freshwater ecosystems: the importance of small-sized phototrophs. Freshwater Reviews 1: 1–28.Google Scholar
- Callieri, C. & M. L. Pinolini, 1995. Picoplankton in Lake Maggiore, Italy. Internationale Revue der Gesamten Hydrobiologie 80: 491–501.CrossRefGoogle Scholar
- Callieri, C. & J. G. Stockner, 2000. Picocyanobacteria success in oligotrophic lakes: fact or fiction? Journal of Limnology 59: 72–76.Google Scholar
- Castberg, T., A. Larsen, R. A. Sandaa, C. P. D. Brussaard, J. K. Egge, M. Heldal, R. Thyrhaug, E. J. van Hannen & G. Bratbak, 2001. Microbial population dynamics and diversity during a bloom of the marine coccolithophorid Emiliania huxleyi (Haptophyta). Marine Ecology Progress Series 221: 39–46.CrossRefGoogle Scholar
- Chen, F., J. R. Lu, B. J. Binder, Y. C. Liu & R. E. Hodson, 2001. Application of digital image analysis and flow cytometry to enumerate marine viruses stained with SYBR gold. Applied and Environmental Microbiology 67: 539–545.PubMedCrossRefGoogle Scholar
- Clasen, J. L., S. N. Brigden, J. P. Payet & C. A. Suttle, 2008. Evidence that viral abundance across oceans and lakes is driven by different biological factors. Freshwater Biology 53(6): 1090–1100.CrossRefGoogle Scholar
- Cochlan, W. P., J. Wilkner, G. F. Steward, D. C. Smith & F. Azam, 1993. Spatial distribution of viruses, bacteria, chorophyll a in neritic, oceanic and estuarine environments. Marine Ecology Progress Series 92: 77–87.CrossRefGoogle Scholar
- Cole, J. J., S. Findlay & M. L. Pace, 1988. Bacterial production in fresh and seawater ecosystem: a cross-system overview. Marine Ecology Progress Series 43: 1–10.CrossRefGoogle Scholar
- Colombet, J., T. Sime-Ngando, H. M. Cauchie, G. Fonty, L. Hoffmann & G. Demeure, 2006. Depth-related gradients of viral activity in Lake Pavin. Applied and Environmental Microbiology 72: 4440–4445.PubMedCrossRefGoogle Scholar
- Courties, C., A. Vaquer, M. Trousselier, M. J. Chrétiennot-Dinet, J. Neveux, C. Machado & H. Claustre, 1994. Smallest eukaryotic organism. Nature 370: 255.CrossRefGoogle Scholar
- Crosbie, N. D., K. Teubner & T. Weisse, 2003. Flow cytometric mapping provides novel insights into the seasonal and vertical distributions of freshwater autotrophic picoplankton. Aquatic Microbial Ecology 33: 53–66.CrossRefGoogle Scholar
- Culley, A. I. & N. A. Welschmeyer, 2002. The abundance, distribution and correlation of viruses, phytoplankton and prokaryotes along a Pacific Ocean transect. Limnology and Oceanography 47: 1508–1513.Google Scholar
- Currie, D. J., 1990. Large scale variability and interactions among phytoplankton, bacterioplankton and phosphorous. Limnology and Oceanography 35: 1437–1455.CrossRefGoogle Scholar
- Danovaro, R., A. Dell’Anno, A. Trucco, M. Serresi & S. Vanucci, 2001. Determination of virus abundance in marine sediments. Applied and Environmental Microbiology 67: 1384–1387.PubMedCrossRefGoogle Scholar
- Del Giorgio, P. A. & R. H. Peters, 1993. Balance between phytoplankton production and plankton respiration in lakes. Canadian Journal of Fisheries and Aquatic Sciences 50: 282–289.CrossRefGoogle Scholar
- Del Giorgio, P. A. & G. Scarborough, 1995. Increase in the proportion of metabolically active bacteria along gradients of enrichment in freshwater and marine plankton: implications for estimates of bacterial growth and production rates. Journal of Plankton Research 17: 1879–1903.CrossRefGoogle Scholar
- Duhamel, S. & S. Jacquet, 2006. Flow cytometric analysis of bacteria- and virus-like particles in lake sediments. Journal of Microbiological Methods 64: 316–332.PubMedCrossRefGoogle Scholar
- Duhamel, S., I. Domaizon, S. Personnic & S. Jacquet, 2006. Assessing the microbial community dynamics and the role of bacteriophages as mortality agents in Lake Geneva. Journal of Water Science 19: 115–126.Google Scholar
- Gasol, J. M. & C. M. Duarte, 2000. Comparative analyses in aquatic microbial ecology: how far do they go? FEMS Microbiology Ecology 31: 99–106.PubMedCrossRefGoogle Scholar
- Gasol, J. M., A. M. Simons & J. Kalff, 1995. Patterns in the top-down versus bottom-up regulation of heterotrophic nanoflagellates in temperate lakes. Journal of Plankton Research 17: 1879–1903.CrossRefGoogle Scholar
- Gobler, C. J., T. W. Davis, S. N. Deonarine, M. A. Saxton, P. J. Lavrentyev, F. J. Jochem & S. W. Wilhelm, 2008. Grazing and virus-induced mortality of microbial populations before and during the onset of annual hypoxia in Lake Erie. Aquatic Microbial Ecology 51: 117–128.CrossRefGoogle Scholar
- Goddard, V., A. C. Baker, J. E. Davy, D. G. Adams, S. J. Thackeray, S. C. Maberly & W. H. Wilson, 2005. Temporal distribution of viruses, bacteria and phytoplankton throughout the water column in a freshwater hypereutrophic lake. Aquatic Microbial Ecology 39: 211–223.CrossRefGoogle Scholar
- Guixa-Boixereu, N., D. Vaqué, J. M. Gasol & C. Pedros-Alio, 1999. Distribution of viruses and their potential effect on bacterioplankton in an oligotrophic marine system. Aquatic Microbial Ecology 19: 205–213.CrossRefGoogle Scholar
- Hambly, E. & C. A. Suttle, 2005. The viriosphere, diversity, and genetic exchange within phage communities. Current Opinion in Microbiology 8: 444–450.PubMedCrossRefGoogle Scholar
- Jacquet, S., J. F. Lennon & D. Vaulot, 1998. Application of a compact and automatic sea water sampler to high frequency picoplankton studies. Aquatic Microbial Ecology 14: 309–314.CrossRefGoogle Scholar
- Jacquet, S., M. Heldal, D. Iglesias-Rodriguez, A. Larsen, W. H. Wilson & G. Bratbak, 2002. Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aquatic Microbial Ecology 27: 111–124.CrossRefGoogle Scholar
- Jacquet, S., I. Domaizon, S. Personnic, S. Duhamel, M. Heldal, A. S. Pradeep Ram & T. Sime-Ngando, 2005. Estimates of protozoan and virus-mediated mortality of bacterioplankton in Lake Bourget (France). Freshwater Biology 50: 627–645.CrossRefGoogle Scholar
- Jeppesen, E., M. Erlandsen & M. Sondergaard, 1997. Can simple empirical equations describe the seasonal dynamics of bacterioplankton in lakes: an eight-year study in shallow hypertrophic and biologically highly dynamic lake Sobygard, Denmark. Microbial Ecology 34: 11–26.PubMedCrossRefGoogle Scholar
- Jiang, C. S., & J. H. Paul, 1995. Viral contribution to dissolved DNA in the marine environment: differential centrifugation and kingdom probing. Applied and Environmental Microbiology 61: 2235–2241.PubMedGoogle Scholar
- Larsen, A., T. Castberg, R. A. Sandaa, C. P. D. Brussaard, J. Egge, M. Heldal, A. Paulino, R. Thyrhaug, E. J. van Hannen & G. Bratbak, 2001. Population dynamics and diversity of phytoplankton, bacteria and viruses in a seawater enclosure. Marine Ecology Progress Series 221: 47–57.CrossRefGoogle Scholar
- Larsen, A., G. A. F. Flaten, R. A. Sandaa, T. Castberg, R. Thyrhaug, S. R. Erga, S. Jacquet & G. Bratbak, 2004. Spring phytoplankton bloom dynamics in Norwegian coastal waters: microbial community succession and diversity. Limnology and Oceanography 49: 180–190.Google Scholar
- Li, W. K. W. & P. M. Dickie, 2001. Monitoring phytoplankton, bacterioplankton, and virioplankton in a coastal Inlet (Belford bassin) by flow cytometry. Cytometry 44: 236–246.PubMedCrossRefGoogle Scholar
- Maranger, R. & D. F. Bird, 1995. Viral abundance in aquatic systems: a comparison between marine and fresh waters. Marine Ecology Progress Series 121: 217–226.CrossRefGoogle Scholar
- Marie, D., C. P. D. Brussaard, R. Thyrhaug, G. Bratbak & D. Vaulot, 1999. Enumeration of marine viruses in culture and natural samples by flow cytometry. Applied and Environmental Microbiology 65: 45–52.PubMedGoogle Scholar
- Marie D., F. Partensky, N. Simon, L. Guillou & D. Vaulot D., 2000. Flow cytometry analysis of marine picoplankton. In DeMaggio, S. (ed), Living Colors: Protocols in Flow Cytometry and Cell sorting. Springer, Berlin: 421–454.Google Scholar
- Mathias, C. B., A. K. T. Kirchner & B. Velimirov, 1995. Seasonal variations of virus abundance and viral control of the bacterial production in a backwater system of the Danube River. Applied and Environmental Microbiology 61: 3734–3740.PubMedGoogle Scholar
- Miki, T. & S. Jacquet, 2008. Complex interactions in the microbial world: under-explored key links between viruses, bacteria and protozoan grazers in aquatic environments. Aquatic Microbial Ecology 51: 195–208.CrossRefGoogle Scholar
- Murray, A. G. & G. A. Jackson, 1992. Viral dynamics: a model of the effects of size, shape, motion and abundance of single-celled planktonic organisms and other particles. Marine Ecology Progress Series 89: 103–116.CrossRefGoogle Scholar
- Noble, R. T. & J. A. Fuhrman, 1998. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquatic Microbial Ecology 14: 113–118.CrossRefGoogle Scholar
- Padisak, J., L. Krienitz, R. Koschel & J. Nedoma, 1997. Deep-layer autotrophic picoplankton maximum in the oligotrophic Lake Stechlin, Germany: origin, activity, development and erosion. European Journal of Phycology 32: 403–416.CrossRefGoogle Scholar
- Paul J. H. & S. C. Jiang, 2001. Lysogeny and transduction. In Paul, J. H. (ed), Methods in Microbiology: Marine Microbiology, Vol. 30. Academic Press, London: 105–125.Google Scholar
- Payet, J. P. & C. A. Suttle, 2008. Physical and biological correlates of virus dynamics in the southern Beaufort Sea and Amundsen Gulf. Journal of Marine Systems 74: 933–945.CrossRefGoogle Scholar
- Raven, J. A., 1986. Physiological consequences of extremely small size for autotrophic organisms in the sea. Canadian Bulletin of Fisheries and Aquatic Sciences 241: 1–70.Google Scholar
- Rodriguez, F., E. Fernandez, R. N. Head, D. S. Harbour, G. Bratbak, M. Heldal & R. P. Harris, 2000. Temporal variability of viruses, bacteria, phytoplankton and zooplankton in the western English Channel off Plymouth. Journal of the Marine Biological Association of the United Kingdom 80: 575–586.CrossRefGoogle Scholar
- Rose, J. M., D. A. Caron, M. E. Sieracki & N. Poulton, 2004. Counting heterotrophic nanoplanktonic protists in cultures and aquatic communities by flow cytometry. Aquatic Microbial Ecology 34: 263–277.CrossRefGoogle Scholar
- Shortreed, K. S. & J. G. Stockner, 1986. Trophic status of 19 subarctic lakes in the Yukon Territory. Canadian Journal of Fisheries and Aquatic Sciences 43: 797–805.Google Scholar
- Sime-Ngando, T., J. Colombet, S. Personnic, I. Domaizon, U. Dorigo, P. Perney, J.-C. Hustache, E. Viollier & S. Jacquet, 2008. Short-term variations in abundances and potential activities of viruses, bacteria and nanoprotists in Lake Bourget (France). Ecological Research 23: 851–861.CrossRefGoogle Scholar
- Suttle, C. A., 2005. Viruses in the sea. Nature 437: 356–361.PubMedCrossRefGoogle Scholar
- Suttle, C. A., 2007. Marine viruses—major players in the global ecosystem. Nature Reviews Microbiology 5: 801–812.PubMedCrossRefGoogle Scholar
- Tzaras, A. & F. R. Pick, 1994. The relationships between bacterial and heterotrophic nanoflagellates for controlling bacterial abundance in oligotrophic and mesotrophic temperate lakes. Marine Microbial Food Webs 8: 347–355.Google Scholar
- Vaulot, D., 1989. CYTOPC: processing software for flow cytometric data. Signal and Noise 2: 8.Google Scholar
- Vaulot, D., C. Courties & F. Partensky, 1989. A simple method to preserve oceanic phytoplankton for flow cytometry. Cytometry 10: 629–635.PubMedCrossRefGoogle Scholar
- Vrede, K., U. Stensdotter & E. S. Lindström, 2003. Viral and bacterioplankton dynamics in two lakes with different humic contents. Microbial Ecology 46: 406–415.PubMedCrossRefGoogle Scholar
- Weinbauer, M. G., 2004. Ecology of prokaryotic viruses. FEMS Microbiology Reviews 28: 127–181.PubMedCrossRefGoogle Scholar
- Weinbauer, M. G. & M. G. Hofle, 1998. Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Applied and Environmental Microbiology 64: 431–438.PubMedGoogle Scholar
- Weinbauer, M. G. & P. Peduzzi, 1995. Effect of virus-rich high molecular weight concentrates of seawater on the dynamics of dissolved amino acids and carbohydrates. Marine Ecology Progress Series 127: 245–253.CrossRefGoogle Scholar
- Weinbauer, M. G. & F. Rassoulzadegan, 2004. Are viruses driving microbial diversification and diversity. Environmental Microbiology 6: 1–11.PubMedCrossRefGoogle Scholar
- Weisse, T. & U. Kenter, 1991. Ecological characteristics of autotrophic picoplankton in a prealpine lake. Internationale Revue der gesamten Hydrobiologie 76: 493–504.CrossRefGoogle Scholar
- Wilhelm, S. W. & C. A. Suttle, 1999. Viruses and nutrient cycles in the sea—viruses play critical roles in the structure and function of aquatic food webs. Bioscience 49: 781–788.CrossRefGoogle Scholar
- Wilson, W. H. & N. H. Mann, 1997. Lysogenic and lytic viral production in marine microbial communities. Aquatic Microbial Ecology 13: 95–100.CrossRefGoogle Scholar
- Wommack, K. E. & R. R. Colwell, 2000. Virioplankton: viruses in aquatic ecosystems. Microbiology and Molecular Biology Reviews 64: 69–114.PubMedCrossRefGoogle Scholar
- Wommack, K., R. T. Hill, M. Kessel, E. Russek-Cohen & R. R. Colwell, 1992. Distribution of viruses in the Chesapeake Bay. Applied and Environmental Microbiology 58: 2965–2970.PubMedGoogle Scholar
- Xenopoulos, M. A. & D. F. Bird, 1997. Virus à la sauce Yo-Pro: microwave-enhanced staining for counting viruses by epifluorescence microscopy. Limnology and Oceanography 42: 1648–1650.CrossRefGoogle Scholar
- Zinabu, G. M. & W. D. Taylor, 1997. Bacteria–chlorophyll relationships in Ethiopian lakes of varying salinity: are soda lakes different? Journal of Plankton Research 19: 647–654.CrossRefGoogle Scholar