Tight Coupling of Glaciecola Spp. and Diatoms During Cold-Water Phytoplankton Spring Blooms
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fmicb-08-00027 January 17, 2017 Time: 16:47 # 1 View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Frontiers - Publisher Connector ORIGINAL RESEARCH published: 19 January 2017 doi: 10.3389/fmicb.2017.00027 Tight Coupling of Glaciecola spp. and Diatoms during Cold-Water Phytoplankton Spring Blooms Markus von Scheibner1, Ulrich Sommer2 and Klaus Jürgens1* 1 Leibniz Institute for Baltic Sea Research Warnemünde, Rostock, Germany, 2 Helmholtz Centre for Ocean Research, Kiel, Germany Early spring phytoplankton blooms can occur at very low water temperatures but they are often decoupled from bacterial growth, which is assumed to be often temperature controlled. In a previous mesocosm study with Baltic Sea plankton communities, an early diatom bloom was associated with a high relative abundance of Glaciecola sequences (Gammaproteobacteria), at both low (2◦C) and elevated (8◦C) temperatures, suggesting an important role for this genus in phytoplankton-bacteria coupling. In this study, the temperature-dependent dynamics of free-living Glaciecola spp. during the bloom were analyzed by catalyzed reporter deposition fluorescence in situ hybridization using a newly developed probe. The analysis revealed the appearance of Glaciecola spp. in this and in previous spring mesocosm experiments as the dominating bacterial clade during diatom blooms, with a close coupling between the population dynamics Edited by: of Glaciecola and phytoplankton development. Although elevated temperature resulted Jakob Pernthaler, in a higher abundance and a higher net growth rate of Glaciecola spp. (Q10 ∼ 2.2), University of Zurich, Switzerland their growth was, in contrast to that of the bulk bacterial assemblages, not suppressed Reviewed by: at 2◦C and showed a similar pattern at 8◦C. Independent of temperature, the highest Robert (Mike) McKay, Bowling Green State University, USA abundance of Glaciecola spp. (24.0 ± 10.0% of total cell number) occurred during the Ludwig Jardillier, peak of the phytoplankton bloom. Together with the slightly larger cell size of Glaciecola, University of Paris-Sud, France this resulted in a ∼30% contribution of Glaciecola to total bacterial biomass. Overall, *Correspondence: Klaus Jürgens the results of this and previous studies suggest that Glaciecola has an ecological [email protected] niche during early diatom blooms at low temperatures, when it becomes a dominant consumer of phytoplankton-derived dissolved organic matter. Specialty section: This article was submitted to Keywords: Glaciecola, phytoplankton, spring bloom, marine bacteria, temperature, Baltic Sea, CARD-FISH Aquatic Microbiology, a section of the journal Frontiers in Microbiology INTRODUCTION Received: 02 August 2016 Accepted: 05 January 2017 The predicted increase in surface temperatures of 2–5◦ by the end of this century (IPCC, 2013) will Published: 19 January 2017 lead to warmer oceans (Levitus, 2000), with important implications for pelagic communities and Citation: biotic interactions (Petchey et al., 1999; Burrows et al., 2011). For example, the differential impact von Scheibner M, Sommer U and of warming on autotrophic production and the consumption of dissolved organic matter (DOM) Jürgens K (2017) Tight Coupling of by heterotrophs induces a higher rate of bacterial degradation of phytoplankton-derived organic Glaciecola spp. and Diatoms during Cold-Water Phytoplankton Spring matter (Wohlers et al., 2009). At low temperatures, phytoplankton spring blooms can be temporally Blooms. Front. Microbiol. 8:27. decoupled from bacterial degradation (Pomeroy and Deibel, 1986; Lignell et al., 1993; Bird and doi: 10.3389/fmicb.2017.00027 Karl, 1999), whereas rising water temperatures intensify phytoplankton-bacteria coupling and Frontiers in Microbiology | www.frontiersin.org 1 January 2017 | Volume 8 | Article 27 fmicb-08-00027 January 17, 2017 Time: 16:47 # 2 von Scheibner et al. Glaciecola Dominance during Early Phytoplankton Blooms thereby enhance carbon flow into the microbial food web in the mesocosms, despite intense grazing pressure, and thus (Müren et al., 2005; Morán et al., 2006; Hoppe et al., 2008; presumably play an important role in carbon processing during Degerman et al., 2013). The mechanisms underlying these diatom blooms, both at low and at elevated temperatures. processes are poorly understood, although they probably depend on the ability of the bacterial assemblage to respond rapidly to the input of labile dissolved organic carbon (DOC) supplied MATERIALS AND METHODS by blooming phytoplankton (Pinhassi et al., 2004; Grossart et al., 2005; Sapp et al., 2007; Teeling et al., 2012). This has Experimental Design and Sampling indeed been observed for bacteria belonging to Alteromonadales The experiment was performed within the priority program (Gammaproteobacteria), in which both cell abundance and AQUASHIFT (Sommer et al., 2007), using 12 indoor mesocosms transcriptional activities increase rapidly in response to DOC, maintained in four climate chambers at the GEOMAR particularly phytoplankton-derived organic carbon (Eilers et al., (Kiel, Germany) from 6 February to 26 March 2008, as 2000; McCarren et al., 2010; Sarmento and Gasol, 2012; Beier previously described in detail with respect to the phytoplankton et al., 2015). Although Alteromonadales are strongly grazed development and experimental setup (Lewandowska and by bacterivorous protists (e.g., Beardsley et al., 2003), high Sommer, 2010), biogeochemistry (Biermann et al., 2014), and proportional abundances have nonetheless been detected during microbial response (von Scheibner et al., 2014). Briefly, the marine phytoplankton spring blooms (Tada et al., 2011; Teeling 12 mesocosms, each with a volume of 1400 L, were filled et al., 2012), indicating the central role of these bacteria in the simultaneously with unfiltered brackish seawater from the Kiel utilization of phytoplankton-derived DOC (Pedler et al., 2014). Fjord (Baltic Sea) and thus contained the natural winter/spring The succession of dominant, free-living bacterial lineages community (in situ temperature of 4.1◦C). They were then during the proliferation of a phytoplankton spring bloom has incubated at either ∼2.0◦C(D 10◦C; low temperature) or not been well-studied at high taxonomic resolution, with a few ∼8.0◦C(D 16◦C; high temperature). The experiment also cross- exceptions (Teeling et al., 2012). Most studies quantitatively linked the two temperature scenarios with three different light examined the bacterial succession during the phytoplankton conditions. However, since the latter had no significant effect blooms, using relatively broad phylogenetic probes such as on either phytoplankton or bacterial parameters, the respective those for Bacteroidetes, Gammaproteobacteria, and Roseobacter mesocosms were pooled such that six replicate mesocosms were in marine environments (Alderkamp et al., 2006; Tada et al., available for each temperature (Lewandowska and Sommer, 2011; Sintes et al., 2013) and for Actinobacteria, Bacteroidetes, 2010; von Scheibner et al., 2014). and Betaproteobacteria in limnic systems (Zeder et al., 2009; Samples used to determine bacterial abundance were fixed Eckert et al., 2012). To our knowledge, no study has quantified with 2% (final concentration) formaldehyde, filtered onto the species- or genus-level dynamics of the dominant bacteria 0.2-mm polycarbonate filters (Whatman), stained with 40,6- during the development of a phytoplankton spring bloom. The diamidino-2-phenylindole (DAPI), and then counted on a Zeiss identification of these bacterial taxa would enable a more detailed Axioplan epifluorescence microscope at 1000× magnification. investigation of their role during early phytoplankton spring For bacterial biomass estimations, the area of the DAPI- blooms, when low water temperatures are thought to otherwise stained bacterial cells was measured with the program Cell- suppress most bacterial activities (Pomeroy and Deibel, 1986). IP (Olympus). The results were projected to cell volume Mesocosm studies have shown that warming results in by assuming a cylindrical shape for the cells and then a tighter phytoplankton-bacterial coupling and an enhanced transforming that value into biomass using the equation: fg C carbon flow into the microbial food web (Hoppe et al., 2008; cell−1 D 133.754 × V0:438, according to Romanova and Sazhin Wohlers et al., 2009; Wohlers-Zöllner et al., 2012; von Scheibner (2010). et al., 2014). Reduced bacterial development in the colder For the enumeration of heterotrophic nanoflagellates (HNFs), treatments is due to a combination of lower growth rates and the samples were filtered onto 0.8-mm black polycarbonate relatively temperature-insensitive protist grazing pressure (von filters (Whatman), stained with DAPI, and counted using Scheibner et al., 2014). In this study, we were particularly an epifluorescence microscope (Axioskop2 mote plus, Zeiss). interested in following the growth dynamics of Glaciecola Biovolumes were calculated from the mean cell diameter and spp. (Alteromonadaceae, Gammaproteobacteria), identified as converted to carbon using a conversion factor of 220 fg C cm3 a dominant taxa in a previous mesocosm study carried out (for details, see von Scheibner et al., 2014). during early phytoplankton bloom conditions. We also examined The Glaciecola probe was also used to examine samples from a how the growth of these bacteria is affected by an increase AQUASHIFT mesocosm experiment performed at the GEOMAR in temperature. The population