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Simultaneous Shifts in Elemental Stoichiometry and Fatty Acids of Emiliania Huxleyi in Response to Environmental Changes

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Simultaneous Shifts in Elemental Stoichiometry and Fatty Acids of Emiliania Huxleyi in Response to Environmental Changes Biogeosciences, 15, 1029–1045, 2018 https://doi.org/10.5194/bg-15-1029-2018 © Author(s) 2018. This work is distributed under the Creative Commons Attribution 3.0 License. Simultaneous shifts in elemental stoichiometry and fatty acids of Emiliania huxleyi in response to environmental changes Rong Bi1,2,3, Stefanie M. H. Ismar3, Ulrich Sommer3, and Meixun Zhao1,2 1Key Laboratory of Marine Chemistry Theory and Technology (Ocean University of China), Ministry of Education, Qingdao, 266100, China 2Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China 3Marine Ecology, GEOMAR Helmholtz-Zentrum für Ozeanforschung, Kiel, 24105, Germany Correspondence: Meixun Zhao ([email protected]) Received: 30 April 2017 – Discussion started: 19 May 2017 Revised: 3 January 2018 – Accepted: 15 January 2018 – Published: 20 February 2018 Abstract. Climate-driven changes in environmental condi- Thus, simultaneous changes of elements and FAs should be tions have significant and complex effects on marine ecosys- considered when predicting future roles of E. huxleyi in the tems. Variability in phytoplankton elements and biochemi- biotic-mediated connection between biogeochemical cycles, cals can be important for global ocean biogeochemistry and ecological functions and climate change. ecological functions, while there is currently limited under- standing on how elements and biochemicals respond to the changing environments in key coccolithophore species such as Emiliania huxleyi. We investigated responses of elemen- 1 Introduction tal stoichiometry and fatty acids (FAs) in a strain of E. hux- leyi under three temperatures (12, 18 and 24 ◦C), three N : P Climate change and intensive anthropogenic pressures have supply ratios (molar ratios 10 V 1, 24 V 1 and 63 V 1) and two pronounced and diverse effects on marine ecosystems. Phys- pCO2 levels (560 and 2400 µatm). Overall, C : N : P stoi- ical and chemical properties in marine ecosystems are chang- chiometry showed the most pronounced response to N : P ing simultaneously such as the concurrent shifts in tempera- supply ratios, with high ratios of particulate organic car- ture, CO2 and oxygen concentrations, and nutrient availabil- bon vs. particulate organic nitrogen (POC : PON) and low ra- ity (Boyd et al., 2015). These changes have altered trophic tios of PON vs. particulate organic phosphorus (PON : POP) interactions in both bottom-up and top-down directions and in low-N media, and high POC : POP and PON : POP in thus resulted in changes in community structure of different low-P media. The ratio of particulate inorganic carbon vs. trophic levels and ecosystem functions (Doney et al., 2012). POC (PIC : POC) and polyunsaturated fatty acid proportions Phytoplankton are the base of marine food webs and major strongly responded to temperature and pCO2, both being drivers of ocean biogeochemical cycling, and thus quantify- lower under high pCO2 and higher with warming. We ob- ing their responses to changing oceanic conditions is a major served synergistic interactions between warming and nutrient challenge in studies of food web structure and ocean biogeo- deficiency (and high pCO2/ on elemental cellular contents chemistry. and docosahexaenoic acid (DHA) proportion in most cases, Coccolithophores are a key phytoplankton group in the indicating the enhanced effect of warming under nutrient de- ocean because of their production of calcified scales called ficiency (and high pCO2/. Our results suggest differential coccoliths. They are not only important photosynthetic pro- sensitivity of elements and FAs to the changes in tempera- ducers of organic matter (causing a drawdown of CO2 in the ture, nutrient availability and pCO2 in E. huxleyi, which is to surface layer) but also play predominant roles in the pro- some extent unique compared to non-calcifying algal classes. duction and export of calcium carbonate to deeper layers (causing a net release of CO2 into the atmosphere) (Rost Published by Copernicus Publications on behalf of the European Geosciences Union. 1030 R. Bi et al.: Elemental stoichiometry and fatty acids in Emiliania huxleyi and Riebesell, 2004). Owning to the determination of these fects of warming and nutrient deficiency, and modest effects two processes on ocean–atmosphere exchange of CO2, coc- of increased pCO2. However, for the key coccolithophore colithophores exhibit a complex and significant influence species E. huxleyi much less is known about the simultane- on the global carbon cycle (Rost and Riebesell, 2004). Of ous changes in elemental stoichiometry and biochemicals in all coccolithophores, Emiliania huxleyi is the most widely response to multiple environmental factor changes. distributed and the most abundant species (Winter et al., In the present study, we conducted semi-continuous cul- 2014), with the capacity to form spatially extensive blooms tures of E. huxleyi to disentangle potential effects of tem- in mid- to high latitudes (Raitsos et al., 2006; Tyrrell and perature, N : P supply ratios and pCO2 on E. huxleyi ele- Merico, 2004). Evidence from in situ and satellite observa- mental stoichiometry and FAs. The elevated levels of tem- tions indicates that E. huxleyi has been increasingly expand- perature and pCO2 in our study are within the predicted ing its range poleward in both hemispheres over the last two ranges of future ocean scenarios. The interannual average decades, and contributing factors to this poleward expansion temperature varied between 16 and 22 ◦C at the Azores may differ between regions and hemispheres (Winter et al., (http://dive.visitazores.com/en/when-dive), the source region 2014). For example, warming and freshening have promoted of our E. huxleyi strain, while annual mean sea surface tem- E. huxleyi blooms in the Bering Sea since the late 1970s perature across the North Atlantic (0–60◦ N) is projected to (Harada et al., 2012), while temperature and irradiance were reach 29.8 ◦C in 2100 according to the ocean general cir- best able to explain variability in E. huxleyi-dominated coc- culation model (Lewandowska et al., 2014). Considerable colithophore community composition and abundance across seasonal, depth and regional variations of pCO2 have been the Drake Passage (Southern Ocean) (Charalampopoulou et observed in the present-day ocean (Joint et al., 2011). In al., 2016). Hence, empirical data on the responses of E. plankton-rich waters, respiration plus atmospheric CO2 en- huxleyi to different environmental drivers would be critical richment can drive high regional pCO2 at times today, e.g., for fully understanding the roles of this prominent coccol- up to 900 µatm in August, with a minimum value of 192 µatm ithophore species in marine ecosystems. in April, in the Southern Bight of the North Sea (Schiettecatte Extensive experimental studies have shown highly vari- et al., 2007). In future oceans, pCO2 is projected to increase able responses of E. huxleyi to rising atmospheric CO2 (re- with rising atmospheric CO2, with 851–1370 µatm by 2100 viewed by Feng et al., 2017a; Meyer and Riebesell, 2015), and 1371–2900 µatm by 2150 (RCP8.5 scenario of the IPCC while other studies focused on the influence of other en- report 2014) (IPCC, 2014). We tested the following hypothe- vironmental factors such as temperature (Rosas-Navarro et ses in the present study: (i) elemental stoichiometry and FAs al., 2016; Sett et al., 2014; Sorrosa et al., 2005), light in- in E. huxleyi show different sensitivity to considerable vari- tensity (Nanninga and Tyrrell, 1996; Xing et al., 2015) and ations in temperature, N : P supply ratios and pCO2; (ii) the nutrient availability (Oviedo et al., 2014; Paasche, 1998). Re- ratios of particulate organic carbon vs. particulate organic ni- sponses of E. huxleyi to the interactions between these differ- trogen (POC : PON), POC vs. particulate organic phospho- ent factors have recently received more attention (De Bodt rus (POC : POP), and particulate inorganic carbon vs. POC et al., 2010; Feng et al., 2008; Milner et al., 2016; Perrin (PIC : POC) in E. huxleyi will reduce and the proportions of et al., 2016; Rokitta and Rost, 2012). Many of these studies unsaturated fatty acids will increase under projected future above focused on the physiological, calcification and photo- ocean scenarios; and (iii) there are synergetic interactions be- synthetic responses of E. huxleyi due to its considerable role tween warming, nutrient deficiency and rising pCO2 on E. in the global carbon cycle. However, biogeochemical cycles huxleyi elemental stoichiometry and FA composition. of the major nutrient elements (nitrogen and phosphorus) and carbon are tightly linked (Hutchins et al., 2009), and thus variability in E. huxleyi C : N : P stoichiometry (cellular quo- 2 Material and methods tas and ratios of C, N and P) can also be important in ocean biogeochemistry. Moreover, elemental budgets in organisms 2.1 Experimental setup are primarily determined by the physiology and biochemistry of biochemicals such as proteins and fatty acids (FAs) (An- To address our questions on how multiple environmental derson et al., 2004; Sterner and Elser, 2002). Thus, study- drivers influence elemental and FA composition in E. huxleyi, ing simultaneous changes of elements and biochemicals en- we performed a semi-continuous culture experiment cross- ables the connection between climate change and ecosystem ing three temperatures (12, 18 and 24 ◦C), three N : P supply functions such as elemental
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