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CO2 and Vitamin B12 Interactions Determine Bioactive Trace Metal Requirements of a Subarctic Pacific Diatom

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CO2 and Vitamin B12 Interactions Determine Bioactive Trace Metal Requirements of a Subarctic Pacific Diatom The ISME Journal (2011) 5, 1388–1396 & 2011 International Society for Microbial Ecology All rights reserved 1751-7362/11 www.nature.com/ismej ORIGINAL ARTICLE CO2 and vitamin B12 interactions determine bioactive trace metal requirements of a subarctic Pacific diatom Andrew L King1, Sergio A San˜ udo-Wilhelmy2, Karine Leblanc3, David A Hutchins1 and Feixue Fu1 1Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA; 2Department of Biological Sciences and Department of Earth Sciences, University of Southern California, Los Angeles, CA, USA and 3Centre National de la Recherche Scientifique; Universite´ de la Me´diterrane´e; Laboratoire d’Oce´anographie Physique et Bioge´ochimique, Marseille, France Phytoplankton growth can be limited by numerous inorganic nutrients and organic growth factors. Using the subarctic diatom Attheya sp. in culture studies, we examined how the availability of vitamin B12 and carbon dioxide partial pressure (pCO2) influences growth rate, primary productivity, cellular iron (Fe), cobalt (Co), zinc (Zn) and cadmium (Cd) quotas, and the net use efficiencies (NUEs) of these bioactive trace metals (mol C fixed per mol cellular trace metal per day). Under B12-replete conditions, cells grown at high pCO2 had lower Fe, Zn and Cd quotas, and used those trace metals more efficiently in comparison with cells grown at low pCO2. At high pCO2,B12-limited cells had B50% lower specific growth and carbon fixation rates, and used Fe B15-fold less efficiently, and Zn and Cd B3-fold less efficiently, in comparison with B12-replete cells. The observed higher Fe, Zn and Cd NUE under high pCO2/B12-replete conditions are consistent with predicted downregulation of carbon-concentrating mechanisms. Co quotas of B12-replete cells were B5- to 14-fold higher in comparison with B12-limited cells, suggesting that 480% of cellular Co of B12- limited cells was likely from B12. Our results demonstrate that CO2 and vitamin B12 interactively influence growth, carbon fixation, trace metal requirements and trace metal NUE of this diatom. This suggests the need to consider complex feedback interactions between multiple environmental factors for this biogeochemically critical group of phytoplankton in the last glacial maximum as well as the current and future changing ocean. The ISME Journal (2011) 5, 1388–1396; doi:10.1038/ismej.2010.211; published online 20 January 2011 Subject Category: microbial ecosystem impacts Keywords: phytoplankton; iron; vitamin B12; carbon dioxide; ocean acidification; trace metals Introduction archaea (Rodionov et al., 2003). About half of cultured eukaryotic phytoplankton species, includ- Marine phytoplankton account for about half ing many harmful algal bloom dinoflagellates, are of global primary production (Behrenfeld and unable to synthesize B12 and thus require an Falkowski, 1997), and depend on the availability exogenous supply (Provasoli and Carlucci, 1974; of dissolved inorganic carbon, major nutrients and Croft et al., 2005; Tang et al., 2010). The renewed trace elements. Many eukaryotic phytoplankton attention to B12 over the past decade has led to also require a number of organic growth cofactors numerous field studies that have demonstrated that including cobalamin—vitamin B12 (Provasoli and vitamin B12 is a limiting factor in a variety of marine Carlucci, 1974)—a cobalt (Co)-containing molecule ecosystems, including temperate and polar coastal synthesized by many, but not all, bacteria and waters (San˜ udo-Wilhelmy et al., 2006; Gobler et al., 2007), iron (Fe)-limited/high-nutrient regimes of the Southern Ocean (Bertrand et al., 2007) and the high- Correspondence: AL King, Department of Biological Sciences, nitrate, low-chlorophyll (HNLC) Gulf of Alaska University of Southern California, 3616 Trousdale Pkwy, Los Angeles, CA 90089, USA. (Koch et al., submitted). E-mail: [email protected] or SA San˜ udo-Wilhelmy, Department Another factor potentially affecting phytoplank- of Biological Sciences and Department of Earth Sciences, ton growth that has recently received attention is the University of Southern California, 3616 Trousdale Pkwy, availability of dissolved inorganic carbon in the Los Angeles, CA 90089, USA. E-mail: [email protected] context of ocean acidification (reviewed by Hutchins Received 14 October 2010; revised 10 December 2010; accepted et al., 2009). Past glacial–interglacial variability in 12 December 2010; published online 20 January 2011 carbon dioxide partial pressure (pCO2)basedon Diatom CO2,B12 and trace metal interactions AL King et al 1389 paleoclimate proxies (Petit et al., 1999) and the them through a column packed with Chelex-100 future predicted anthropogenic rise in pCO2 (Bio-Rad, Hercules, CA, USA; Price et al., 1988/89). (Solomon et al., 2007) could influence phytoplank- For both B12 conditions, triplicate acid-washed ton physiology and elemental requirements. For polycarbonate bottles were equilibrated with com- instance, a higher CO2 availability could alleviate mercially prepared air:CO2 mixtures at three differ- high metabolic energy and trace metal requirements ent CO2 concentrations: 200, 370 and 670 p.p.m. of the carbon-concentrating mechanisms that supply pCO2 (see below). In-line HEPA filters were used to CO2 for photosynthesis (Raven, 1991; Morel et al., avoid trace metal and bacterial contamination from 1994). the gas tanks or lines. Despite the global importance of both vitamin B12 Trace metal clean semi-continuous culturing meth- and pCO2 to phytoplankton metabolic pathways, ods were used during acclimation periods and virtually nothing is known about the possible steady-state growth. Final sampling was carried interactions between these two critical factors. We out following 4–8 weeks of semi-continuous incuba- tested the effects of B12 and CO2 availability on tion after statistically invariant growth rates were specific growth rates, primary productivity and the recorded for at least three consecutive transfers. requirements of major nutrients (C, N and P) and Fe, Cultures were grown semi-continuously to maintain as well as other trace metals (zinc (Zn), Co and cells in the exponential growth phase to avoid bias cadmium (Cd)) in steady-state semi-continuous resulting from sampling during different growth cultures of Attheya sp., a centric diatom isolated phases in different experimental treatments. All from the Bering Sea (an Fe-limited HNLC region; medium handling, culturing and manipulation used Leblanc et al., 2005). Attheya sp. belongs to the careful trace metal clean methods under class 100 family Chaetocerotaceae, and was previously classi- conditions. fied in the genus Chaetoceros (Crawford et al., Seawater medium pCO2 in the experimental 2000), a biogeochemically important algal group that bottles was calculated throughout the experiment dominates blooms in coastal upwelling regions and using measurements of pH and total dissolved in mesoscale and bottle Fe addition experiments inorganic carbon according to Dickson and Goyet (Hutchins and Bruland, 1998; de Baar et al., 2005). (1994). To ensure that CO2 levels remained constant during growth, the pH in each bottle was monitored daily using a microprocessor pH meter, calibrated Materials and methods with pH 4, 7 and 10 buffer solutions. Total dissolved inorganic carbon was measured via coulometry Unialgal axenic Attheya sp. (CCMP207) stock cul- (model CM 140, UIC, Joliet, IL, USA). The calculated tures, isolated from the Bering Sea, were obtained pCO2 values (using CO2SYS; http://www.cdiac. from the Provasoli-Guillard Culture Collection of ornl.gov/ftp/co2sys/CO2SYS_calc_XLS) from the Marine Phytoplankton (West Boothbay Harbor, final day of the experiment were 201±13, 367±21 Maine, USA) and grown in microwave-sterilized and 671±31 p.p.m. (Table 1); these treatments are media prepared from 0.2 mm-filtered natural sea- referred to using rounded-off values of 200, 370 and water (collected using trace metal clean techniques). 670 p.p.m. pCO2. Media had Aquil concentrations of nitrate, phos- Primary production was measured in triplicate À1 14 phate and silicic acid with additions of 5 mM EDTA, using 24 h incubations with 3.7 kBq ml H CO3 451 nM Fe, 80 nM Zn, 50 nM Co and no added Cd under the appropriate experimental growth condi- (Price et al., 1988/89). Stock cultures were incubated tions of light and temperature for each treatment, at 3 1C with a 12 h:12 h light–dark cycle and an followed by filtration and scintillation counting. incident photon flux density of 80 mmol photons Aliquots for analysis of particulate organic C and N À2 À1 m s . Although B12 auxotrophy has not been were filtered onto pre-combusted 25 mm GF/F filters evaluated for Attheya sp., various centric diatoms (Whatman, Maidstone, UK) and analyzed using a including species from the same family, Chaeto- 4010 CHNS Elemental Combustion System (Costech, cerotaceae, have been found to require vitamin B12 Valencia, CA, USA). Samples for particulate organic (Provasoli and Carlucci, 1974). Cultures were ver- phosphorous were processed and analyzed spectro- ified to be axenic by staining subsamples with photometrically. Details for these methods can be 40,6-diamidino-2-phenolindole, followed by bacter- foundinFuet al. (2005, 2007; and references therein). ial counts using epifluorescence microscopy Particulate samples for trace metal analysis were directly before the final sampling. filtered onto acid-washed 3-mm-pore-size polycarbo- Experimental treatments included trace metal nate filters (Millipore, Billerica,
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