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Abundance and Activity of Major Groups of Prokaryotic Plankton in the Coastal North Sea During Spring and Summer

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Abundance and Activity of Major Groups of Prokaryotic Plankton in the Coastal North Sea During Spring and Summer AQUATIC MICROBIAL ECOLOGY Vol. 45: 237–246, 2006 Published December 21 Aquat Microb Ecol Abundance and activity of major groups of prokaryotic plankton in the coastal North Sea during spring and summer Anne-Carlijn Alderkamp1, 3,*, Eva Sintes2, Gerhard J. Herndl2 1Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9759 AA Haren, The Netherlands 2Department of Biological Oceanography, Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB Den Burg, Texel, The Netherlands 3Present address: Department of Geophysics, Stanford University, 397 Panama Mall, Stanford, California 94305-2215, USA ABSTRACT: The dynamics of the abundance and activity of selected heterotrophic prokaryotic groups were determined in the coastal North Sea during a coastal spring bloom dominated by the prymnesiophyte Phaeocystis globosa and in the subsequent spring and summer season using cat- alyzed reporter deposition-fluorescence in situ hybridization combined with microautoradiography (MICRO-CARD-FISH). Both Crenarchea and Euryarchaea were detected throughout the study period, albeit never at levels that exceeded 2% of the total prokaryotic abundance, corresponding to a maximum abundance of 2.8 × 108 Archaea l–1. Euryarchaea were generally more abundant than Crenarchaea. On average, 21% of the Crenarchaea and 35% of the Euryarchaea were taking up leucine throughout the study period. Members of the Bacteroidetes were abundant during the P. glo- bosa bloom period. At the senescent stage of the bloom, Bacteroidetes comprised up to 63% of the prokaryotic community. The abundances of members of the Roseobacter clade as well as the SAR86 cluster were low during the phytoplankton spring bloom period (mean 2% each), but increased dur- ing August. On average, 51% of the Roseobacter, 38% of the Bacteroidetes and 39% of the SAR86 cluster were taking up leucine. The percentages of active Bacteria increased during the decline of the P. globosa spring bloom. The Bacteroidetes cluster showed the strongest increase, indicating that members of this cluster are likely to play a major role in the degradation of organic matter produced in the P. globosa spring bloom. KEY WORDS: Marine Archaea · Bacteroidetes · Roseobacter · North Sea · CARD-FISH · Microautoradiography · Bacterial succession · Phaeocystis Resale or republication not permitted without written consent of the publisher INTRODUCTION ate southern North Sea, Phaeocystis globosa (Prymne- siophyceae) typically dominates the phytoplankton Coastal areas cover only around 7% of the global community in spring and forms dense blooms with cell ocean’s surface, but contribute 30% to global marine abundances as high as 108 cells l–1 (Cadée & Hegeman primary production (Gattuso et al. 1998). In these 1986, Cadée 1992, Brussaard et al. 1996). These waters, a significant part of the annual primary pro- blooms may account for as much as 65% of the local duction is produced during phytoplankton spring annual primary production (Joiris et al. 1982). blooms initiated when high nutrient concentrations Phytoplankton produce labile dissolved organic coincide with increased solar radiation. In the temper- carbon (DOC) that is directly utilizable by heterotro- *Email: [email protected] © Inter-Research 2006 · www.int-res.com 238 Aquat Microb Ecol 45: 237–246, 2006 phic prokaryotes (Carlson et al. 1998). During growth, planktonic Archaea, their contribution to the marine phytoplankton release a fraction of their photo- biogeochemical cycles remains largely unknown. assimilated carbon as DOC (Teira et al. 2001). In addi- Specifically, the dynamics of the abundance and activ- tion, DOC is released by metazooplankton through ity of Archaea in response to phytoplankton blooms ‘sloppy feeding’ on phytoplankton (Møller et al. 2003). are unspecified. We used combined microautoradiog- With regard to Phaeocystis blooms, the collapse of the raphy with catalyzed reporter deposition fluorescence bloom can be sudden, with cell lysis potentially being in situ hybridization (MICRO-CARD-FISH) to deter- an important source of mortality (Brussaard et al. 1995, mine the dynamics in abundance and activity of 1996, 2005). Through cell lysis, phytoplankton biomass selected groups of Bacteria and Crenarchea and Eur- will be partly converted into dissolved and colloidal yarchaea in the coastal North Sea during a Phaeocys- matter, and subsequently recycled by heterotrophic tis-dominated phytoplankton bloom and the subse- prokaryotes rather than transferred to higher trophic quent spring and summer season. levels (Brussaard et al. 1996, Fuhrman 1999). Phyto- plankton blooms in general, and Phaeocystis blooms in particular, lead to an increase in the abundance and MATERIALS AND METHODS production of heterotrophic prokaryotes (Laanbroek et al. 1985, Blight et al. 1995, Brussaard et al. 1996, Bec- Sampling and analyses of phyto- and heterotrophic quevort et al. 1998). prokaryotic plankton. Surface water of the coastal Phytoplankton blooms impact the composition of the North Sea was collected with an acid-rinsed bucket heterotrophic bacterioplankton community (Arrieta & from the Royal Netherlands Institute for Sea Research Herndl 2002, Pinhassi et al. 2004); however, few data (NIOZ) jetty located at the southern entrance of the exist on the response of individual prokaryotic groups North Sea into the Dutch Wadden Sea (53° 00’ 18” N, to phytoplankton blooms. Studies of marine bacterio- 04° 47’ 42” E) between March and August 2004. Sam- plankton diversity have shown that essentially 3 ples from this tidal channel were collected at high tide clusters of Bacteria dominate marine bacterioplankton in order to sample water originating from the Dutch communities. Bacteria belonging to the polyphyletic coastal North Sea. Samples were taken from about group Cytophaga-Flavobacteria-Bacteroides, now 0.5 m depth, which was regarded as representative of termed Bacteroidetes, the Roseobacter clade of the the whole water column because the water of this tidal Alphaproteobacteria, and the SAR86 cluster of the channel is generally well-mixed. Samples were taken Gammaproteobacteria are not only present in neritic twice a week during the spring bloom and at weekly seas such as the North Sea (Eilers et al. 2000, Alonso & intervals during the summer. Pernthaler 2005) and the Mediterranean (Acinas et al. Phytoplankton abundance and species composition 1999), but also dominate open oceans such as the were determined on Lugol (non-acid)-preserved sam- Pacific and Atlantic (Mullins et al. 1995). Roseobacter ples under a Zeiss inverted microscope using 3 or 5 ml is closely associated with phytoplankton blooms, and counting chambers. Total and free-living prokaryotes members of this group utilize DMS(P) (Malmstrom et were enumerated in unfiltered and in 3 µm-filtered al. 2004). samples (Millipore, polycarbonate filter), respectively. Besides heterotrophic Bacteria, non-thermophilic Water samples (1 ml) were fixed with 2% formalde- pelagic Archaea are abundant throughout the marine hyde (final concentration), incubated at 4°C in the dark environment as well. The 2 major groups of Archaea, for 30 min, frozen in liquid nitrogen and stored at Crenarchaea and Euryarchaea, have been detected in –80°C until analysis. After thawing, the samples were the open ocean (Fuhrman et al. 1992, Karner et al. stained in the dark with SYBR Green I solution (Mole- 2001), coastal waters (DeLong 1992, Preston et al. cular Probes, 2.5 µmol l–1 final concentration) for 1996, Massana et al. 2001), and salt marshes (Munson 15 min and subsequently enumerated on a FACScal- et al. 1997). In the open ocean, Crenarchaea and Eur- ibur (Becton Dickinson) flow cytometer (FCM) with a yarchaea may account for more than half of the laser set at 488 nm wavelength (Brussaard 2004). Sam- prokaryotic abundance at the base of the euphotic ples were run at medium speed (40 µl min–1) and data zone and in the dark ocean, and play a significant role were acquired in log mode until a minimum of 10 000 in the oceanic carbon cycle because they are able to events had been recorded. The rate of particle passage utilize both dissolved organic and inorganic carbon in the capillary was always maintained below 1000 (Herndl et al. 2005, Teira et al. 2006a,b). In addition, events s–1. Cell concentrations were determined from Crenarchaea may play an important role as ammonia the flow rate and by using a known concentration of oxidizers (Könneke et al. 2005, Wuchter et al. 2006). 1 µm-diameter fluorescent latex beads (105 beads ml–1) Despite this recent progress in elucidating the poten- as an internal standard (Polyscience). Prokaryotes tial carbon and energy sources of non-thermophilic were detected by their signature of side scatter (SSC) Alderkamp et al.: Prokaryote dynamics in the North Sea 239 versus green fluorescence (FL1) as described else- 10% [w/v] dextran sulfate, 0.02% [w/v] sodium where (Gasol & del Giorgio 2000, Brussaard 2004). dodecyl sulfate, 1% [w/v] blocking reagent [Boeh- For MICRO-CARD-FISH analyses of the free-living ringer Mannheim], and 55% [v/v] formamide [for prokaryotes, water samples were filtered through Eub338, Non338, CF319, Ros537, Sar86] or 20% [v/v] polycarbonate filters (Millipore, 3 µm) in order to formamide [for Cren537, Eury806 and Non338]). remove most of the non-prokaryotic biota and the par- Hybridization was performed at 35°C for 12 to 15 h. ticle-attached prokaryotes. Two to 5 ml of the filtrate Thereafter, filter sections with probes targeting Bac- was spiked with 3H-leucine (specific activity160 Ci teria were washed in 50 ml pre-warmed washing mmol–1, 20 nM final concentration; Amersham). Con- buffer (5 mM EDTA [pH 8], 20 mM Tris-HCl [pH 7.4 trols were fixed with paraformaldehyde (2% final con- to 7.6], 0.01% [w/v] sodium dodecyl sulfate) contain- centration) 10 min prior to adding 3H-leucine. Samples ing 13 mM NaCl at 37°C for 15 min. Filter sections were incubated in the dark at in situ temperature for with probes targeting Archaea were washed in 50 ml 3 to 9 h depending on the in situ water temperature, pre-warmed washing buffer containing 145 mM subsequently fixed with paraformaldehyde (2% final NaCl.
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