Abstract
In order to study interactions between microorganisms at different nutrient conditions in an arctic environment, a mesocosm experiment was performed in Kongsfjorden, Svalbard (79°N). A phytoplankton bloom was initiated by daily additions of mineral nutrients (ammonium and phosphate) to all mesocosm units. The addition of silicate and glucose, forming a factorial design (+Si/+C, +Si/−C, −Si/+C, −Si/−C), was intended to produce different types of growth rate limitation for the bacterial community. We here focus on the response in bacterial community composition to different nutrient situations. Phytoplankton, bacteria and viruses were enumerated by flow cytometry, while denaturing gradient gel electrophoresis (DGGE) was used to track changes in the bacterial community composition. Our results showed that both glucose and silicate addition affected the bacterial community composition, with the largest effect from glucose. The initial increase in bacterial abundance was most pronounced in the glucose units. After silicate addition, highest bacterial abundance was observed in the silicate treatments where mineral nutrient competition by diatoms was expected to be highest. The major effect of glucose was expressed by the significant separation of the +C and the −C samples at the end of the experiment, while silicate addition resulted in a more stable bacterial community structure. In the unit, given both silicate and glucose, the diatoms were totally outcompeted by the bacterial community. The competitive success of the heterotrophic bacteria in C-replete situations allows the conclusion that the bacteria were not more negatively affected by low temperatures than phytoplankton.
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References
Allers E, Gomez-Consarnau L, Pinhassi J, Gasol JM, Simek K, Pernthaler J (2007) Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ Microbiol 9:2417–2429
Baas-Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. van Stockkum’s Gravenhange, The Hague
Bailey MJ, Lilley AK, Thompson IP, Rainey PB, Ellis RJ (1995) Site directed chromosomal marking of a fluorescent pseudomonad isolated from the phytosphere of sugar beet; Stability and potential for marker gene transfer. Mol Ecol 4:755–763
Bell W, Mitchell R (1972) Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull 143:265–277
Bell WH, Lang JM, Mitchell R (1974) Selective stimulation of marine bacteria by algal extracellular products. Limnol Oceanogr 19:833–839
Bratbak G, Thingstad TF (1985) Phytoplankton-bacteria interactions—an apparent paradox—analysis of a model system with both competition and commensalism. Mar Ecol Prog Ser 25:23–30
Bratbak G, Jacobsen A, Heldal M (1998) Viral lysis of Phaeocystis pouchetii and bacterial secondary production. Aquat Microb Ecol 16:11–16
Caron DA (1987) Grazing of attached bacteria by heterotrophic microflagellates. Microb Ecol 13:203–218
Castberg T, Larsen A, Sandaa RA, Brussaard CPD, Egge JK, Heldal M, Thyrhaug R, van Hannen EJ, Bratbak G (2001) Microbial population dynamics and diversity during a bloom of the marine coccolithophorid Emiliania huxleyi (Haptophyta). Mar Ecol Prog Ser 221:39–46
Chen WH, Wangersky PJ (1996) Production of dissolved organic carbon in phytoplankton cultures as measured by high-temperature catalytic oxidation and ultraviolet photo-oxidation methods. J Plankton Res 18:1201–1211
Currie DJ, Kalff J (1984a) Can bacteria outcompete phytoplankton for phosphorus—a chemostat test. Microb Ecol 10:205–216
Currie DJ, Kalff J (1984b) A comparison of the abilities of fresh-water algae and bacteria to acquire and retain phosphorus. Limnol Oceanogr 29:298–310
Currie DJ, Kalff J (1984c) The relative importance of bacterioplankton and phytoplankton in phosphorus uptake in fresh-water. Limnol Oceanogr 29:311–321
Ducklow HW (1983) Production and fate of bacteria in the oceans. Bioscience 33:494–501
Egge JK, Jacobsen A (1997) Influence of silicate on particulate carbon production in phytoplankton. Mar Ecol Prog Ser 147:219–230
Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548
Fukami K, Simidu U, Taga N (1985) Microbial decomposition of phytoplankton and zooplankton in seawater. 2. Changes in the bacterial community. Mar Ecol Prog Ser 21:7–13
Giovannoni SJ, Britschgi TB, Moyer CL, Field KG (1990) Genetic diversity in Sargasso Sea bacterioplankton. Nature 345:60–63
Gonzalez JM, Sherr EB, Sherr BF (1990) Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl Environ Microbiol 56:583–589
Grossart HP (1999) Interactions between marine bacteria and axenic diatoms (Cylindrotheca fusiformis, Nitzschia laevis, and Thalassiosira weissflogii) incubated under various conditions in the lab. Aquat Microb Ecol 19:1–11
Havskum H, Thingstad TF, Scharek R, Peters F, Berdalet E, Sala MM, Alcaraz M, Bangsholt JC, Zweifel UL, Hagstrom A, Perez M, Dolan JR (2003) Silicate and labile DOC interfere in structuring the microbial food web via algal-bacterial competition for mineral nutrients: results of a mesocosm experiment. Limnol Oceanogr 48:129–140
Juergens K, Arndt H, Rothhaupt KO (1994) Zooplankton-mediated changes of bacterial community structure. Microb Ecol 27:27–42
Kirchman DL, Malmstrom RR, Cottrell MT (2005) Control of bacterial growth by temperature and organic matter in the Western Arctic. Deep Sea Res (II Top Stud Oceanogr) 52:3386–3395
Kirchman DL, Moran XAG, Ducklow H (2009) Microbial growth in the polar oceans—role of temperature and potential impact of climate change. Nat Rev Microbiol 7:451–459
Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid-determination of 16S ribosomal-RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82:6955–6959
Mague TH, Friberg E, Hughes DJ, Morris I (1980) Extracellular release of carbon by marine-phytoplankton—a physiological approach. Limnol Oceanogr 25:262–279
Manabe S, Stouffer RJ (1994) Multiple-century response of a coupled ocean-atmosphere model to an increase of atmospheric carbon-dioxide. J Clim 7:5–23
Marie D, Brussaard CPD, Thyrhaug R, Bratbak G, Vaulot D (1999) Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl Environ Microbiol 65:45–52
Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112
Matz C, Jurgens K (2003) Interaction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community. Microb Ecol 45:384–398
Moran XAG, Calvo-Diaz A, Ducklow HW (2010) Total and phytoplankton mediated bottom-up control of bacterioplankton change with temperature in NE Atlantic shelf waters. Aquat Microb Ecol 58:229–239
Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16S ribosomal-RNA. Appl Environ Microbiol 59:695–700
Myklestad SM (1995) Release of extracellular products by phytoplankton with special emphasis on polysaccharides. Sci Total Environ 165:155–164
Nagata T, Kirchman DL (1991) Release of dissolved free and combined amino-acids by bacterivorous marine flagellates. Limnol Oceanogr 36:433–443
Øvreås L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373
Pengerud B, Skjoldal EF, Thingstad TF (1987) The reciprocal interaction between degradation of glucose and ecosystem structure—studies in mixed chemostat cultures of marine bacteria, algae and bacterivorous nanoflagellates. Mar Ecol Prog Ser 35:111–117
Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A, Marrase C (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70:6753–6766
Pomeroy LR, Deibel D (1986) Temperature regulation of bacterial-activity during the spring bloom in Newfoundland coastals waters. Science 233:359–361
Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23:187–204
Riemann L, Steward GF, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66:578–587
Rose J, Caron D (2007) Does low temperature constrain the growth rates of heterotrophic protists? evidence and implications for algal blooms in cold waters. Limnol Oceanogr 52:886–895
Sandaa RA (2008) Burden or benefit? virus-host interactions in the marine environment. Res Microbiol 159:374–381
Sandaa RA, Gomez-Consarnau L, Pinhassi J, Riemann L, Malits A, Weinbauer MG, Gasol JM, Thingstad TF (2009) Viral control of bacterial biodiversity—evidence from a nutrient-enriched marine mesocosm experiment. Environ Microbiol 11:2585–2597
Sapp M, Schwaderer AS, Wiltshire KH, Hoppe HG, Gerdts G, Wichels A (2007) Species-specific bacterial communities in the phycosphere of microalgae? Microb Ecol 53:683–699
Sharp JH (1977) Excretion of organic-matter by marine-phytoplankton—healthy cells do it. Limnol Oceanogr 22:381–399
Simek K, Chrzanowski TH (1992) Direct and indirect evidence of size-selective grazing on pelagic bacteria by fresh-water nanoflagellates. Appl Environ Microbiol 58:3715–3720
Simek K, Vrba J, Pernthaler J, Posch T, Hartman P, Nedoma J, Psenner R (1997) Morphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Appl Environ Microbiol 63:587–595
Thingstad TF (2000) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45:1320–1328
Thingstad TF, Skjoldal EF, Bohne RA (1993) Phosphorus cycling and algal-bacterial competition in Sandsfjord, western Norway. Mar Ecol Prog Ser 99:239–259
Thingstad TF, Bellerby RG, Bratbak G, Borsheim KY, Egge JK, Heldal M, Larsen A, Neill C, Nejstgaard J, Norland S, Sandaa RA, Skjoldal EF, Tanaka T, Thyrhaug R, Topper B (2008) Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455:387–390
Wohlers J, Engel A, Zollner E, Breithaupt P, Jurgens K, Hoppe HG, Sommer U, Riebesell U (2009) Changes in biogenic carbon flow in response to sea surface warming. Proc Natl Acad Sci USA 106:7067–7072
Acknowledgments
This work was financed by the Research Council of Norway through the International Polar Year project 175939/S30 ‘PAME-Nor’ (IPY activity ID no. 71), with additional support from the strategic institution project 158936/I10 ‘Patterns in microbial diversity’, Bjerknes Centre of Climate Research, Centre of Excellence Project 146003/V30, project 178441/S40 ‘Interact’ and project 184860/S30 ‘MERCLIM’. Support was also received from Norsk Hydro Produksjon AS project number 5404889 and from the Svalbard Science Forum as ‘Aktisstipend’. We thank Kings Bay A/S and the staff at Ny Ålesund for help with logistics. Many thanks also to J. L. Ray for her helpful comments to the manuscript and Joachim Paul Spindelböck for statistical assistance.
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Töpper, B., Larsen, A., Thingstad, T.F. et al. Bacterial community composition in an Arctic phytoplankton mesocosm bloom: the impact of silicate and glucose. Polar Biol 33, 1557–1565 (2010). https://doi.org/10.1007/s00300-010-0846-4
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DOI: https://doi.org/10.1007/s00300-010-0846-4