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Growth of the Coccolithophore Emiliania Huxleyi in Light

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Growth of the Coccolithophore Emiliania Huxleyi in Light Growth of the coccolithophore Emiliania huxleyi in light- and nutrient-limited batch reactors: relevance for the BIOSOPE deep ecological niche of coccolithophores Laura Perrin, Ian Probert, Gerald Langer, Giovanni Aloisi To cite this version: Laura Perrin, Ian Probert, Gerald Langer, Giovanni Aloisi. Growth of the coccolithophore Emiliania huxleyi in light- and nutrient-limited batch reactors: relevance for the BIOSOPE deep ecological niche of coccolithophores. Biogeosciences, European Geosciences Union, 2016, 13 (21), pp.5983-6001. 10.5194/bg-13-5983-2016. hal-01497843 HAL Id: hal-01497843 https://hal.archives-ouvertes.fr/hal-01497843 Submitted on 31 Jul 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution - NoDerivatives| 4.0 International License Biogeosciences, 13, 5983–6001, 2016 www.biogeosciences.net/13/5983/2016/ doi:10.5194/bg-13-5983-2016 © Author(s) 2016. CC Attribution 3.0 License. Growth of the coccolithophore Emiliania huxleyi in light- and nutrient-limited batch reactors: relevance for the BIOSOPE deep ecological niche of coccolithophores Laura Perrin1, Ian Probert2, Gerald Langer3, and Giovanni Aloisi4 1Sorbonne Universités, UPMC Univ. Paris 06-CNRS-IRD-MNHN, LOCEAN-IPSL, 75252 Paris, France 2CNRS-UPMC Université, Paris 06 FR2424, Roscoff Culture Collection, Station Biologique de Roscoff, 29680 Roscoff, France 3The Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, Devon, PL1 2PB, UK 4LOCEAN, UMR 7159, CNRS-UPMC-IRD-MNHN, 75252 Paris, France Correspondence to: Laura Perrin ([email protected]) Received: 10 May 2016 – Published in Biogeosciences Discuss.: 14 June 2016 Revised: 30 September 2016 – Accepted: 12 October 2016 – Published: 2 November 2016 Abstract. Coccolithophores are unicellular calcifying ma- This study contributes more widely to the understanding of rine algae that play an important role in the oceanic carbon E. huxleyi physiology and behaviour in a low-light and olig- cycle via their cellular processes of photosynthesis (a CO2 otrophic environment of the ocean. sink) and calcification (a CO2 source). In contrast to the well- studied, surface-water coccolithophore blooms visible from satellites, the lower photic zone is a poorly known but po- tentially important ecological niche for coccolithophores in 1 Introduction terms of primary production and carbon export to the deep ocean. In this study, the physiological responses of an Emil- Coccolithophores are unicellular, photosynthetic and calcify- iania huxleyi strain to conditions simulating the deep niche ing algae that are very abundant in the marine environment in the oligotrophic gyres along the BIOSOPE transect in the and play key roles in the global carbon cycle (Paasche, 2002; South Pacific Gyre were investigated. We carried out batch Roth, 1994). Through photosynthesis they contribute to the culture experiments with an E. huxleyi strain isolated from upper ocean carbon pump (CO2 sink), while via calcification the BIOSOPE transect, reproducing the in situ conditions they contribute to the carbonate counter-pump (CO2 source) of light and nutrient (nitrate and phosphate) limitation. By (Paasche, 2002; Westbroek et al., 1993). The relative impor- simulating coccolithophore growth using an internal stores tance of calcification and photosynthesis is one of the fac- (Droop) model, we were able to constrain fundamental phys- tors that dictates the effect of coccolithophores on ocean– iological parameters for this E. huxleyi strain. We show that atmosphere CO2 fluxes (Shutler et al., 2013). Environmental simple batch experiments, in conjunction with physiologi- conditions such as temperature, irradiance, nutrient concen- cal modelling, can provide reliable estimates of fundamen- trations and pCO2 exert a primary control on the calcifica- tal physiological parameters for E. huxleyi that are usually tion/photosynthesis ratio in coccolithophores and also affect obtained experimentally in more time-consuming and costly cellular growth rates, which, together with grazing, mortality, chemostat experiments. The combination of culture exper- sinking of cells and oceanic transport, define the biogeogra- iments, physiological modelling and in situ data from the phy of coccolithophores. BIOSOPE cruise show that E. huxleyi growth in the deep Despite the fact that certain coccolithophores have been BIOSOPE niche is limited by availability of light and nitrate. fairly extensively studied in the laboratory (e.g. Daniels et al., 2014; Iglesias-Rodriguez et al., 2008; Krug et al., 2011; Published by Copernicus Publications on behalf of the European Geosciences Union. 5984 L. Perrin et al.: Growth of the coccolithophore Emiliania huxleyi Langer et al., 2012; Rouco et al., 2013), the factors control- periments with coccolithophores that combine both nutri- ling their biogeography in the global ocean are poorly under- ent and light limitation, however, are scarce. One reason is stood (Boyd et al., 2010). In controlled laboratory conditions, that investigating phytoplankton growth under nutrient limi- coccolithophore growth is monitored as given environmental tation in laboratory experiments is complicated. In batch cul- parameters are varied (e.g. Buitenhuis et al., 2008; Feng et tures the instantaneous growth rate decreases as nutrients be- al., 2008; Fritz, 1999; Langer et al., 2006; Leonardos and come limited, making it hard to extract the dependence of Geider, 2005; Paasche, 1999; Trimborn et al., 2007). In the growth rate on nutrient concentrations (Langer et al., 2013). ocean, geographical surveys of coccolithophore abundance This can be avoided by employing chemostat cultures, in and concomitant measurements of environmental variables which growth rates and nutrient concentrations are kept con- contribute to defining coccolithophore biogeography in rela- stant under nutrient-limited conditions (Engel et al., 2014; tion to the environment (Claustre et al., 2008; Henderiks et Leonardos and Geider, 2005; Müller et al., 2012). Physiolog- al., 2012). Although extrapolation of results from laboratory ical parameters obtained in chemostat experiments have been experiments to field distributions might not be straightfor- used in biogeochemical models to investigate environmen- ward, this approach has been widely used and continues to tal controls on phytoplankton biogeography (Follows and yield important insights into coccolithophore ecology and its Dutkiewicz, 2011; Gregg and Casey, 2007). Despite their rel- reaction to a rapidly changing environment. evance to nutrient-limited growth, chemostat cultures are rel- In this respect, one of the least well-understood but possi- atively rarely used because they are more expensive, time- bly globally relevant niches where coccolithophores can be consuming and complicated to set up and run than batch cul- relatively abundant is that occurring at the deep pycnocline tures (LaRoche et al., 2010). of oceanic gyres, probably the best studied example of which In this study, we investigated growth of the coccol- was observed during the BIOSOPE cruise in the South Pa- ithophore E. huxleyi under light and nutrient co-limitation cific Gyre (Beaufort et al., 2008; Claustre et al., 2008). This and applied the results of this culture study to investigate deep coccolithophore niche occurred at about 200 m depth, at the conditions controlling growth in the deep niche of the a very low irradiance level (< 20 µmol photons m−2 s−1/ and South Pacific Gyre. Using an E. huxleyi strain isolated dur- at a depth corresponding to the nitrate and phosphate nutri- ing the BIOSOPE cruise, we carried out batch culture ex- cline with dissolved nitrate (NO3/ and phosphate (PO4/ con- periments that reproduced the low- in situ light and nutrient centrations of about 1 and 0.2 µM respectively. The niche was conditions of the deep ecological niche. We monitored the dominated by coccolithophore species belonging to the fam- nitrogen and phosphorus content of particulate organic mat- ily Noëlaerhabdaceae, i.e. Emiliania huxleyi and species of ter, as well as cell, coccosphere and coccolith sizes, because Gephyrocapsa and Reticulofenestra (Beaufort et al., 2008). these parameters are known to vary with nutrient limitation Deep-dwelling coccolithophores have also been observed in (Fritz, 1999; Kaffes, 2010; Rouco et al., 2013). To overcome other geographic regions. Okada and McIntyre (1979) ob- the conceptual limitations inherent in nutrient-limited batch served coccolithophores in the North Atlantic Ocean down experiments (Langer et al., 2013), we modelled the transient to a depth of 100 m, where Florisphaera profunda domi- growth conditions in the batch reactor assuming that assim- nated assemblages in summer and E. huxleyi dominated as- ilation of nutrients and growth are either coupled (Monod, semblages for the rest of the year. Deep coccolithophore 1949) or decoupled (Droop, 1968) processes in the coccol- populations dominated by F. profunda in the lower photic ithophore E.
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