Ocean-Related Global Change Alters Lipid Biomarker Production in Common Marine Phytoplankton
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Biogeosciences, 17, 6287–6307, 2020 https://doi.org/10.5194/bg-17-6287-2020 © Author(s) 2020. This work is distributed under the Creative Commons Attribution 4.0 License. Ocean-related global change alters lipid biomarker production in common marine phytoplankton Rong Bi1,2,3, Stefanie M. H. Ismar-Rebitz3, Ulrich Sommer3, Hailong Zhang1,2, and Meixun Zhao1,2 1Frontiers Science Center for Deep Ocean Multispheres and Earth System, and Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Ocean University of China, Qingdao 266100, China 2Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China 3Marine Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, 24105, Germany Correspondence: Meixun Zhao ([email protected], [email protected]) Received: 22 May 2020 – Discussion started: 8 June 2020 Revised: 19 October 2020 – Accepted: 28 October 2020 – Published: 14 December 2020 Abstract. Lipids, in their function as trophic markers in food 1 Introduction webs and organic matter source indicators in the water col- umn and sediments, provide a tool for reconstructing the Ocean phytoplankton has profoundly responded to and complexity of global change effects on aquatic ecosystems. driven natural climatic variability throughout Earth’s his- It remains unclear how ongoing changes in multiple environ- tory (Riding, 1992; Falkowski and Oliver, 2007; Falkowski, mental drivers affect the production of key lipid biomarkers 2015). In the contemporary ocean, human-induced physi- in marine phytoplankton. Here, we tested the responses of cal and chemical modifications are complex and concur- sterols, alkenones and fatty acids (FAs) in the diatom Phaeo- rent, including warming, acidification, deoxygenation and dactylum tricornutum, the cryptophyte Rhodomonas sp. and changes in nutrient availability (Doney et al., 2012; Moore the haptophyte Emiliania huxleyi under a full-factorial com- et al., 2013; DeVries et al., 2017). The ocean-related global bination of three temperatures (12, 18 and 24 ◦C), three N : P change fundamentally affects marine ecosystems (Hoegh- supply ratios (molar ratios 10 : 1, 24 : 1 and 63 : 1) and two Guldberg and Bruno, 2010). These include especially global pCO2 levels (560 and 2400 µatm) in semicontinuous cultur- phytoplankton biomass decreases (Boyce et al., 2010; Moore ing experiments. Overall, N and P deficiency had a stronger et al., 2018; Lotze et al., 2019) and plankton community effect on per-cell contents of sterols, alkenones and FAs changes (Richardson and Schoeman, 2004; Jonkers et al., than warming and enhanced pCO2. Specifically, P deficiency 2019), which consequently alters food-web dynamics (Ko- caused an overall increase in biomarker production in most rtsch et al., 2015; du Pontavice et al., 2020) and biogeo- cases, while N deficiency, warming and high pCO2 caused chemical cycles (Hofmann and Schellnhuber, 2009; Gruber, nonsystematic changes. Under future ocean scenarios, we 2011; Doney et al., 2012). A major challenge is the lack predict an overall decrease in carbon-normalized contents of of understanding of the complexity of biological impacts of sterols and polyunsaturated fatty acids (PUFAs) in E. hux- global change, which has hindered the prediction of poten- leyi and P. tricornutum and a decrease in sterols but an in- tial feedbacks between marine ecosystems and projected en- crease in PUFAs in Rhodomonas sp. Variable contents of vironmental changes. Some of the phytoplankton-produced lipid biomarkers indicate a diverse carbon allocation between biomolecules (biomarkers), functioning as indicators of nu- marine phytoplankton species in response to changing envi- tritional food quality (Müller-Navarra, 2008) and tracers of ronments. Thus, it is necessary to consider the changes in organic matter sources (Volkman et al., 1998), have provided key lipids and their consequences for food-web dynamics crucial insight into the trajectory of ecological responses to and biogeochemical cycles, when predicting the influence of changing environment along food webs in the present-day global change on marine ecosystems. ocean (Ruess and Müller-Navarra, 2019), as well as over ge- ological time (Brocks et al., 2017). Published by Copernicus Publications on behalf of the European Geosciences Union. 6288 R. Bi et al.: Ocean-related global change alters lipid biomarker production Lipids are amongst the most important and widely used al. (1996) found a dramatic decrease in total sterol contents biomarkers, because they have far-reaching biochemical and (per dry weight) in Phaeodactylum tricornutum as tempera- physiological roles in cells and are sensitive to environmental ture increased. In contrast, a significant increase in carbon- changes (Arts et al., 2009); they are also important because of normalized sterol contents with increasing temperature was their dominance in the geological record as fossil molecules found in other algal species (Piepho et al., 2012; Ding et al., to reveal life’s signatures on Earth (Falkowski and Freeman, 2019). Enhanced pCO2 caused an increase in the percentage 2014). There are also growing applications of lipids as prox- of sterols (% of total lipids) in Dunaliella viridis (Gordillo et ies for global climate and marine ecosystem change. Of all al., 1998) but no clear change in per-cell contents of sterols biomarkers, fatty acids (FAs), the basic constituents of most in Emiliania huxleyi (Riebesell et al., 2000). Although sig- algal lipids, have received the most intense attention. Polyun- nificant interactions between two environmental factors have saturated fatty acids (PUFAs) are essential for many ani- been observed on carbon-normalized or per-cell sterol con- mals and have been applied as nutritional components to tents in certain phytoplankton species (Piepho et al., 2010, study trophic interactions (Brett and Müller-Navarra, 1997; 2012; Ding et al., 2019), the impacts of multiple environmen- Müller-Navarra et al., 2000; Dalsgaard et al., 2003; Kelly tal drivers on phytoplankton sterol contents have not been and Scheibling, 2012; Ruess and Müller-Navarra, 2019). The thoroughly investigated. impact of environmental changes on phytoplankton FAs has Long-chain alkenones are major lipids produced only by been well studied, mostly with a focus on the effects of tem- certain species of haptophytes, e.g., oceanic species E. hux- perature and nutrient changes (reviewed by Guschina and leyi and Gephyrocapsa oceanica (Volkman et al., 1980c; Harwood, 2009; Galloway and Winder, 2015; Hixson and Conte et al., 1995) and coastal species Isochrysis galbana Arts, 2016), while the interplay between different environ- (reviewed by Conte et al., 1994). Alkenones in E. huxleyi mental drivers has been recently tested (Bermúdez et al., are believed to be used for energy storage (Epstein et al., 2015; Bi et al., 2017, 2018). However, determining how phy- 2001; Eltgroth et al., 2005), while little is known about the toplankton lipids respond to global change still faces substan- entire biosynthetic pathway of alkenones and their evolution- tial challenges, partly because data on other important lipid ary and ecological functions (Rontani et al., 2006; Kitamura classes such as sterols and alkenones are scarce. Understand- et al., 2018). Alkenones may have fitness and trophic bene- ing the impact of environmental change on these lipid classes fit for their producers, because these unusual lipids are not is critical to achieve a better application of lipid biomark- only more photostable than other neutral lipids such as tria- ers to contemporary issues and to the past record of marine cylglycerols but are also resistant to digestion, perhaps mak- ecosystems. ing alkenone producers less suitable for grazers (Eltgroth et Sterols are tetracyclic triterpenoids present in all eukary- al., 2005). Moreover, alkenones are well preserved in sedi- otes (Volkman, 2003, 2016). Sterols function primarily as ments over millions of years and thus their unsaturation ratios K0 D C structural components of plasma membranes but also play (e.g., the U37 index ( C37 V 2 = (C37 V 2 C37 V 3)); Brassell et key roles in cellular defense against toxic compounds and al., 1986; Prahl and Wakeham, 1987) are widely applied signal transduction, and they serve as precursors to sev- for reconstructing sea surface temperatures (Rosell-Melé and eral important compounds (e.g., steroid hormones in an- Prahl, 2013; Herbert et al., 2016). A long-standing issue for imals) involved in cellular and developmental processes the use of alkenones to infer paleo-ocean surface tempera- (Hartmann, 1998; Guschina and Harwood, 2009; Fabris ture is how the production of these compounds is influenced et al., 2012). In ecology, sterols have been used as in- by other environmental factors such as nutrients. Thus, cul- dicators of dietary nutritional quality, because some in- ture studies have been conducted to test alkenone contents vertebrates are incapable of synthesizing sterols de novo (mostly per-cell contents) in several species of haptophytes and thus must obtain sterols from their diets (reviewed by such as E. huxleyi under different growth phases (Wolhowe Martin-Creuzburg and von Elert, 2009b). In geochemistry, et al., 2009; Pan and Sun, 2011; Wolhowe et al., 2015), salin- sterols such as 24-methylcholesta-5,22E-dien-3β-ol (brassi- ity (Sachs et al., 2016), temperature (Ding et al., 2019) and casterol = epi-brassicasterol) and 4α,23,24-trimethylcholest-