Coccolithophores do not increase particulate carbon production under nutrient limitation: A case study using Emiliania huxleyi (PML B92/11)
Introduction
It is generally held that the recent, putatively man-made, increase in sea surface temperature will lead to an enhanced stratification in the oceans. The latter in turn will reduce the input of nutrients into phytoplankton rich surface waters, which will increase the probability of phytoplankton nutrient limitation (Behrenfeld et al., 2006). The response of the biogeochemically important coccolithophores to nutrient (nitrogen, N, and phosphorus, P) limitation is a matter of interest in that context, with special emphasis being put on these algae's production of particulate organic (POC) and inorganic (PIC) carbon (Rost and Riebesell, 2004). By producing POC as well as PIC, coccolithophores, as opposed to e.g., diatoms, contribute to the organic carbon pump as well as the carbonate counter pump (Rost and Riebesell, 2004). The term carbon pump refers to particulate carbon which sinks to depth, thereby transporting carbon from sea surface waters to the deep ocean. The PIC/POC ratio of the material that sinks to depth is an important parameter in the global carbon cycle. A number of recent studies have addressed the question of particulate carbon production in coccolithophores by means of laboratory experiments (Borchard et al., 2011, Kaffes et al., 2010, Langer et al., 2012, Matthiessen et al., 2012). It was suggested that coccolithophores increase PIC production in response to nutrient limitation (McConnaughey and Whelan, 1997). Such a response was indeed shown for Calcidiscus leptoporus (Langer et al., 2012), but not for Emiliania huxleyi (Borchard et al., 2011, Kaffes et al., 2010, Paasche, 1998, Riegman et al., 2000). The responses of the latter species moreover varied between different studies, which might hint at strain-specific differences, because a different strain was used in each study (except Borchard et al., 2011, Kaffes et al., 2010, who used the same strain). Species- and strain-specific responses of coccolithophores were shown with respect to e.g., salinity (Brand, 1984) and carbonate chemistry (Langer et al., 2006, Langer et al., 2009, Langer et al., 2011) changes.
Nevertheless, it was argued that coccolithophores do not increase particulate carbon production in response to macro-nutrient limitation, and that the increase in production observed in C. leptoporus is a methodological artefact (Langer et al., 2012). The response of coccolithophores to nutrient limitation was studied in batch and (semi)-continuous culture (Benner, 2008, Borchard et al., 2011, Kaffes et al., 2010, Paasche, 1998, Riegman et al., 2000). Langer et al. (2012) argued that there are methodological limitations in determining particulate carbon production in the batch approach, which can lead to apparently increased production under limitation. Briefly, production is the product of growth rate and carbon quota. Both factors are integrated values over the course of the experiment. In batch culture the cells undergo a transition from exponential to stationary growth, entailing a non-constant growth rate. A constant growth rate, by contrast, is a prerequisite for an accurate determination of production by means of this method. The latter is the reason why Langer et al. (2012) hypothesised that production as determined in the batch approach contains a methodological artefact, i.e., a wrong growth rate, which in turn can result in apparently increased production under limitation. This hypothesis can only be tested by comparing the response patterns of a particular culture strain grown in batch as well as (semi)-continuous culture. Here we test this hypothesis in a case study using E. huxleyi (PML B92/11). The latter strain was recently grown in nitrogen-limited semi-continuous culture (Kaffes et al., 2010) and phosphorus-limited continuous culture (Borchard et al., 2011). In this study we grew E. huxleyi (PML B92/11) in nitrogen as well as phosphorus limited batch culture.
Section snippets
Material and methods
Clonal cultures of E. huxleyi (strain PML B92/11), were grown in sterile filtered (0.2 μm) seawater enriched with trace metals and vitamins according to f/2, a common recipe for culture media additives (Guillard and Ryther, 1962). Initial nitrate and phosphate concentrations varied in dependence of treatment (Table 1). The N-limited treatment featured an initial nitrate concentration of ca. 3 μM and an initial phosphate concentration of ca. 35 μM. The P-limited treatment was characterized by an
Results
E. huxleyi (strain PML B92/11) was grown in both N-limited and P-limited dilute batch cultures. The evolution of seawater phosphate concentrations in the P-limited treatment and seawater nitrate concentrations in the N-limited treatment in relation to cell density is depicted in Fig. 1. It can be seen that phosphate and nitrate concentrations in the P- and N-limited treatments respectively fell below the detection limit on day 5. By that time ca. 50% of the final cell density had been produced.
Discussion
Phosphorus limitation did apparently not affect PIC production of E. huxleyi (PML B92/11), whereas POC production increased by a factor of 3.3 under P-limitation (Table 3, Fig. 2). While the former observation tallies with data of Borchard et al. (2011), the latter observation is in stark contrast to the results of Borchard et al. (2011). The latter authors performed a chemostat (i.e., continuous culture) experiment on that very same strain including two different levels of P-limitation
Acknowledgements
We thank Ina Benner for insightful comments and Angela M. Oviedo and Patrizia Ziveri for stimulating discussions. This work was supported by the European Commission through grant 211384 (EU FP7 “EPOCA”). Financial support for BIOACID was provided by the German Federal Ministry of Education and Research (BMBF) (FKZ 03F0608). The research leading to these results has received funding from the European Community’s Seventh Framework Programme under grant agreement 265103 (Project MedSeA). This work
References (27)
- et al.
Biogeochemical response of Emiliania huxleyi (PML B92/11) to elevated CO2 and temperature under phosphorous limitation: a chemostat study
J. Exp. Mar. Biol. Ecol.
(2011) The salinity tolerance of forty-six marine phytoplankton isolates
Estuarine Coastal Shelf Sci.
(1984)- et al.
A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media
Deep-Sea Res.
(1987) - et al.
Carbon and nitrogen fluxes in the marine coccolithophore Emiliania huxleyi grown under different nitrate concentrations
J. Exp. Mar. Biol. Ecol.
(2010) - et al.
Calcification of Calcidiscus leptoporus under nitrogen and phosphorus limitation
J. Exp. Mar. Biol. Ecol.
(2012) - et al.
Calcification generates protons for nutrient and bicarbonate uptake
Earth Sci. Rev.
(1997) - et al.
Relationship between coccolith Sr/Ca ratios and coccolithophore production and export in the Arabian Sea and Sargasso Sea
Deep-Sea Res. II Top. Stud. Oceanogr.
(2007) - et al.
Climate-driven trends in contemporary ocean productivity
Nature
(2006) - Benner I., 2008. The utilization of organic nutrients in marine phytoplankton with emphasis on coccolithophores, PhD...
- et al.
Measurement of total carbon dioxide and alkalinity in the North Atlantic ocean in 1981
The carbon dioxide system in sea water: equilibrium chemistry and measurements
Carbon fixation and coccolith detachment in the coccolithophore Emiliania huxleyi in nitrate-limited cyclostats
Mar. Biol.
Determination of the equivalence point in potentiometric titrations of seawater with hydrochloric acid
Oceanol Acta.
Cited by (24)
Local hydrodynamic in coastal system affects the coccolithophore community at a short spatial scale
2023, Marine MicropaleontologyRefining the alkenone-pCO<inf>2</inf> method II: Towards resolving the physiological parameter ‘b’
2020, Geochimica et Cosmochimica ActaLipid biomarker production by marine phytoplankton under different nutrient and temperature regimes
2019, Organic GeochemistryCitation Excerpt :For diatoms, increasing temperature caused an overall increase in cellular POC contents in Thalassiosira pseudonana (Berges et al., 2002) and Phaeodactylum tricornutum (Bi et al., 2017), a decrease in Thalassiosira weissflogii, and a U-shaped response in Chaetoceros sp. (Lomas and Glibert, 1999). Similarly, differential responses of cellular POC contents to changes in environmental conditions were also found in other phytoplankton groups, such as dinoflagellates (Fu et al., 2008; Nielsen, 1996; Vidyarathna and Graneli, 2013) and coccolithophores (Bi et al., 2018b; Langer et al., 2013; Leonardos and Geider, 2005). Such diverse responses of cellular POC contents can be attributed to the interactions between different environmental factors (Bi et al., 2017; Li et al., 2012), which often makes it difficult for direct comparisons between studies using differing experimental conditions.
Phosphorus availability modifies carbon production in Coccolithus pelagicus (Haptophyta)
2015, Journal of Experimental Marine Biology and EcologyCitation Excerpt :The cellular POC and PIC contents have been measured only at the end of experiments once the growth rate is reduced to zero (Benner, 2008; Gerecht et al., 2014; Langer et al., 2012, 2013). The cellular content is therefore uncoupled from the overall growth rate used to calculate production, which is not constant over the course of the experiment (Langer et al., 2012, 2013). To calculate production in nutrient-limited batch cultures, a different approach is necessary e.g. using a radioactive tracer (Paasche, 1964).
Alkenone δD as an ecological indicator: A culture and field study of physiologically-controlled chemical and hydrogen-isotopic variation in C<inf>37</inf> alkenones
2015, Geochimica et Cosmochimica ActaCitation Excerpt :Samples (300 ml filtered onto pre-combusted glass fiber filters) were oven-dried and stored at room temperature until analysis. These cultures are described in more detail, along with discussion of their calcification behavior, in Langer et al. (2013; for B92/11) and Oviedo et al. (2014; for RCC1812–1833). In situ large volume filters (LVFs) were collected during ‘GoCal4’, a 2008 cruise to the Gulf of California and adjacent eastern tropical north Pacific (ETNP).