Description: The coccolithophore Emiliania huxleyi is a microalga with biogeochemical and biotechnological relevance, due to its high abundance in the ocean and its ability to form intricate calcium carbonate structures. Depletion of macronutrients in oceanic waters is very common and will likely enhance with advancing climate change. We present the first comprehensive metabolome study analyzing the effect of phosphorus (P) and nitrogen (N) starvation on the diploid and haploid life-cycle stage, applying various metabolome analysis methods to gain new insights in intracellular mechanisms to cope with nutrient starvation. P-starvation led to an accumulation of many generic and especially N-rich metabolites, including lipids, osmolytes, and pigments. This suggests that P-starvation primarily arrests cell-cycling due to lacking P for nucleic acid synthesis, but that enzymatic functionality is widely preserved. Also, the de-epoxidation ratio of the xanthophyll cycle was upregulated in the diploid stage under P-starvation, indicating increased nonphotochemical quenching, a response typically observed under high light stress. In contrast, N-starvation resulted in a decrease of most central metabolites, also P-containing ones, especially in the diploid stage, indicating that most enzymatic functionality ceased. The two investigated nutrient starvation conditions caused significantly different responses, contrary to previous assumptions derived from transcriptomic studies. Data highlight that instantaneous biochemical flux is a more dominant driver of the metabolome than the transcriptomically rearranged pathway patterns. Due to the fundamental nature of the observed responses it may be speculated that microalgae with similar nutrient requirements can cope better with P-starvation than with N-starvation.

Description: The potential for adaptation of phytoplankton to future climate is often extrapolated based on single strain responses of a representative species, ignoring variability within and between species. The aim of this study was to approximate the range of strain-specific reaction patterns within an Arctic diatom population, which selection can act upon. In a laboratory experiment, we first incubated natural communities from an Arctic fjord under present and future conditions. In a second step, single strains of the diatom Thalassiosira hyalina were isolated from these selection environments and exposed to a matrix of temperature (38C and 68C) and pCO 2 levels (180 latm, 370 latm, 1000 latm, 1400 latm) to establish reaction norms for growth, production rates, and elemental quotas. The results revealed interactive effects of temperature and pCO 2 as well as wide tolerance ranges. Between strains, however, sensitivities and optima differed greatly. These strain-specific responses corresponded well with their respective selection environments of the previous com- munity incubation. We therefore hypothesize that intraspecific variability and the selection between coexist- ing strains may pose an underestimated source of species’ plasticity. Thus, adaptation of phytoplankton assemblages may also occur by selection within rather than only between species, and species-wide inferences from single strain experiments should be treated with caution.

Description: Arctic phytoplankton and their response to future conditions shape one of the most rapidly changing ecosystems on the planet. We tested how much the phenotypic responses of strains from an Arctic diatom population diverge and whether the physiology and intraspecific composition of multi-strain populations differ from expectations based on single strain traits. To this end, we conducted incubation experiments with the diatom Thalassiosira hyalina under present-day and future temperature and pCO2 treatments. Six fresh isolates from the same Svalbard population were incubated as mono- and multi-strain cultures. For the first time, we were able to closely follow intraspecific selection within an artificial population using microsatellites and allele-specific quantitative PCR. Our results show not only that there is substantial variation in how strains of the same species cope with the tested environments, but also that changes in genotype composition, production rates and cellular quotas in the multi-strain cultures are not predictable from monoculture performance. Nevertheless, the physiological responses as well as strain composition of the artificial populations were highly reproducible within each environment. Interestingly, we only detected significant strain sorting in those populations exposed to the future treatment. This study illustrates that the genetic composition of populations can change on very short timescales through selection from the intraspecific standing stock, indicating the potential for rapid population level adaptation to climate change. We further show that individuals adjust their phenotype not only in response to their physico-chemical, but also to their biological surroundings. Such intraspecific interactions need to be understood in order to realistically predict ecosystem responses to global change.

Description: Enrichment of the oceans with CO2 may be beneficial for some marine phytoplankton, including harmful algae. Numerous laboratory experiments provided valuable insights into the effects of elevated pCO2 on the growth and physiology of harmful algal species, including the production of phycotoxins. Experiments close to natural conditions are the next step to improve predictions, as they consider the complex interplay between biotic and abiotic factors that can confound the direct effects of ocean acidification. We therefore investigated the effect of ocean acidification on the occurrence and abundance of phycotoxins in bulk plankton samples during a long-term mesocosm experiment in the Gullmar Fjord, Sweden, an area frequently experiencing harmful algal blooms. During the experimental period, a total of seven phycotoxin-producing harmful algal genera were identified in the fjord, and in accordance, six toxin classes were detected. However, within the mesocosms, only domoic acid and the corresponding producer Pseudo-nitzschia spp. was observed. Despite high variation within treatments, significantly higher particulate domoic acid contents were measured in the mesocosms with elevated pCO2. Higher particulate domoic acid contents were additionally associated with macronutrient limitation. The risks associated with potentially higher phycotoxin levels in the future ocean warrants attention and should be considered in prospective monitoring strategies for coastal marine waters.

Description: Primary productivity in the Arctic Ocean is vastly driven by single-celled phytoplankton. Within a comparably short growing season, they provide most of the carbon and energy for higher trophic levels and simultaneously influence biogeochemical cycles and the global climate. With the Arctic Ocean being one of the few regions that are expected to increase their productivity with future global change, it is especially important to understand how phytoplankton there is going to adapt. The potential for this adaptation to future climate change is often extrapolated from studies using single strains of a representative species that were cultured in laboratories for years. Since several decades, however, it is known that phytoplankton species and even local populations can exhibit large intraspecific diversity. During a field campaign on Svalbard, we isolated different strains of the Arctic diatom Thalassiosira hyalina from community incubations, which resembled present and future climate conditions. We then exposed these freshly isolated monocultures again to a matrix of CO and temperature. The results revealed that even within a single species, response patterns can differ greatly, comparable to variations seen between diatom species. Moreover, while only minor reactions of the communities were observed, the strain responses corresponded strongly with the previous selection environment. A strain isolated from future-like treatments, for instance, had its growth optimum at a higher temperature and pCO than another strain isolated from more present-like conditions. This suggests that intraspecific variability and the selection between coexisting ecotypes may be an underestimated source of species’ plasticity under changing environmental conditions and could ‘buffer’ functional species shifts. Adaptation of phytoplankton assemblages may therefore occur also by selection within rather than only between species, and species-wide inferences from single strain experiments should be handled with great care.

Description: Recent ocean acidification (OA) studies revealed that seawater [H+] rather than [CO2] or [HCO3-] regulate short-term responses in carbon fluxes of Emiliania huxleyi. Here, we investigated whether acclimation to altered carbonate chemistry modulates this regulation pattern and how the carbon supply for calcification is affected by carbonate chemistry. We acclimated E. huxleyi to present-day (ambient [CO2], [HCO3-], and pH) and OA conditions (high [CO2], ambient [HCO3-], low pH). To differentiate between the CO2 and pH/H+ effects, we also acclimated cells to carbonation (high [CO2] and [HCO3-], ambient pH) and acidification (ambient [CO2], low [HCO3-], and pH). Under these conditions, growth, production of particulate inorganic and organic carbon, as well as carbon and oxygen fluxes were measured. Under carbonation, photosynthesis and calcification were stimulated due to additional inline image uptake, whereas growth was unaffected. Such stimulatory effects are not apparent after short-term carbonation, indicating that cells adjusted their carbon acquisition during acclimation. Being driven by H+, these regulations can, however, not explain typical OA effects. Under acidification and OA, photosynthesis stayed constant, whereas calcification and growth decreased. Similar to the short-term responses toward high [H+], CO2 uptake significantly increased, but inline image uptake decreased. This antagonistic regulation in CO2 and inline image uptake can explain why photosynthesis, being able to use CO2 and inline image, often benefits from OA, whereas calcification, being mostly dependent on inline image, often decreases. We identified H+ as prime driver of coccolithophores' acclimation responses toward OA. Acidified conditions seem to put metabolic burdens on the cells that result in decreased growth.