Vertical partitioning of phosphate uptake among picoplankton groups in the low Pi Mediterranean Sea

Biogeosciences, 12, 1237–1247, 2015 www.biogeosciences.net/12/1237/2015/ doi:10.5194/bg-12-1237-2015 © Author(s) 2015. CC Attribution 3.0 License. Vertical partitioning of phosphate uptake among picoplankton groups in the low Pi Mediterranean Sea A. Talarmin1,2,* , F. Van Wambeke1,2 , P. Lebaron3,4 , and T. Moutin1,2 1 Aix Marseille Université, Mediterranean Institute of Oceanography (MIO), 13288, Marseille, CEDEX 9, France 2 Université de Toulon, 83957, CNRS-INSU/IRD, France 3 Sorbonne Universités, UPMC Univ. Paris 06, USR 3579, LBBM, Observatoire Océanologique, 66650, Banyuls-sur-Mer, France 4 CNRS, USR 3579, LBBM, Observatoire Océanologique, 66650 Banyuls-sur-Mer, France * now at: Red Sea Research Center, 4700 King Abdullah University of Science and Technology, Thuwal, 23955-6900, Saudi Arabia Correspondence to: A. Talarmin () Received: 15 September 2014 – Published in Biogeosciences Discuss.: 13 October 2014 Revised: 2 February 2015 – Accepted: 4 February 2015 – Published: 26 February 2015 Abstract. Microbial transformations are key processes in marine phosphorus cycling. In this study, we investigated the contribution of phototrophic and heterotrophic groups to phosphate (Pi) uptake fluxes in the euphotic zone of the lowPi Mediterranean Sea and estimated Pi uptake kinetic characteristics. Surface soluble reactive phosphorus (SRP) concentrations were in the range of 6–80 nmol L−1 across the transect, and the community Pi turnover times, assessed using radiolabeled orthophosphate incubations, were longer in the western basin, where the highest bulk and cellular rates were measured. Using live cell sorting, four vertical profiles of Pi uptake rates were established for heterotrophic prokaryotes (Hprok), phototrophic picoeukaryotes (Pic) and Prochlorococcus (Proc) and Synechococcus (Syn) cyanobacteria. Hprok cells contributed up to 82 % of total Pi uptake fluxes in the superficial euphotic zone, through constantly high abundances (2.7–10.2 × 105 cells mL−1 ) but variable cellular rates (6.6 ± 9.3 amol P cell−1 h−1 ). Cyanobacteria achieved most of the Pi uptake (up to 62 %) around the deep chlorophyll maximum depth, through high abundances (up to 1.4 × 105 Proc cells mL−1 ) and high cellular uptake rates (up to 40 and 402 amol P cell−1 h−1 , respectively for Proc and Syn cells). At saturating concentrations, maximum cellular rates up to 132 amol P cell−1 h−1 were measured for Syn at station (St.) C, which was 5 and 60 times higher than Proc and Hprok, respectively. Pi uptake capabilities of the different groups likely contribute to their vertical distribution in the low Pi Mediterranean Sea, possibly along with other energy limitations. 1 Introduction Understanding nutrient uptake strategies in microorganisms is a necessity to predict their biogeochemical response to environmental changes. Heterotrophic (Hprok) and phototrophic prokaryotes (cyanobacteria) dominate the planktonic biomass in oligotrophic areas of the surface ocean and account for most of the carbon fluxes through the microbial loop (Azam et al., 1983). Nanomolar concentrations of orthophosphate (Pi) and Pi turnover times as low as minutes or hours are seasonally observed in the Sargasso and Mediterranean seas (e.g., McLaughlin et al., 2013; Moutin et al., 2002; Sebastián et al., 2012; Thingstad et al., 1998; Wu et al., 2000). Pi is the preferred form of phosphorus for most osmotrophs, but recent studies show that dissolved organic phosphorus (DOP) can be a significant source of P as well, particularly in its most labile forms like ATP (e.g., Björkman and Karl, 1994; Björkman et al., 2012; Casey et al., 2009; Duhamel et al., 2012; Fu et al., 2006; Lomas et al., 2010; Sebastián et al., 2012). It is now well established that concentrations of Pi in the environment impact uptake processes by microbes, who rely on high affinity systems via active transport at low concentrations and high capacity systems and diffu- Published by Copernicus Publications on behalf of the European Geosciences Union. 1238 A. Talarmin et al.: Vertical partitioning of phosphate uptake among picoplankton groups sion at higher environmental Pi concentrations (e.g., Knauss and Porter, 1954; Nyholm, 1977). Along with an increased stratification and oligotrophication of the surface ocean, a widely spread size-shift in the structure of phytoplankton communities is expected, from nano- and micro- eukaryotes to pico-sized cells, as observed in the North Pacific Subtropical Gyre (Church et al., 2002; Karl et al., 2001). How phytoplankton and bacteria share P resources when they are poorly available has been debated for over 30 years. The existence of different Pi acquisition systems in microorganisms was highlighted in studies where Hprok systems were found to be saturating at much lower Pi concentrations than phototrophic eukaryotes (> 3 µm: Currie and Kalff, 1984; Currie et al., 1986). Some eukaryotes possess mixotrophic capabilities: grazing on P-richer prokaryotes (Christaki et al., 1999; Hartmann et al., 2011) as well as DOP hydrolysis induced by ectoenzymes (ATPases, alkaline phosphatases, e.g., Webb, 1992) can fill most of their requirements of P. Eukaryotic phytoplankton may compensate for their low affinity for the substrate at low concentrations (high Km) with high Pi storage capacity (Cotner and Biddanda, 2002) compared to prokaryotes and a more efficient growth mechanism, i.e., a low half-saturation constant for growth (Ks, Rhee, 1973). Pi uptake by microbes in natural environments has largely been assessed using size fractionation. Studies concur on the high contribution of the small size fractions (< 0.8, < 1, < 2 or < 3 µm) to Pi uptake fluxes (Björkman and Karl, 1994; Currie et al., 1986; Moutin et al., 2002; Tanaka et al., 2003; Thingstad et al., 1993, 1998). This contribution generally increases in aquatic systems with short Pi turnover times and also in low Pi systems after P amendments, emphasizing the idea that heterotrophic prokaryotes are high competitors in P-deficient areas (e.g., Björkman et al., 2012; Currie et al., 1986; Drakare, 2002; Labry et al., 2002). However, size fractionation offers a limited resolution of microbial processes, especially in oligotrophic environments where osmotrophs are small and where taxonomic and functional types overlap in size. The development of combined radiolabeling techniques and cell sorting by flow cytometry has improved the level of resolution for studying Pi uptake strategies in heterotrophic and phototrophic microbes (e.g., Björkman et al., 2012; Casey et al., 2009; Duhamel et al., 2012; Lomas et al., 2014; Talarmin et al., 2011b; Zubkov et al., 2007). When looking into the contribution of picoplanktonic groups to total Pi uptake, prokaryotes are better competitors than eukaryotes. Among prokaryotes, measured cellular uptake rates of Pi were higher for Synechococcus (Syn) compared to Hprok and Prochlorococcus (Proc) in the Sargasso Sea (Michelou et al., 2011), an (...truncated)