AMUST - Arctic phytoplankton under multiple stressors
Ecological stability under environmental change is determined by both interspecific and intraspecific processes. Particularly for planktonic microorganisms it is challenging to follow intraspecific dynamics over space and time. We propose a new method, Microsatellite PoolSeq Barcoding (MPB), for tracing allele frequency changes in protist populations. We successfully applied this method to experimental community incubations and field samples of the diatom Thalassiosira hyalina from the Arctic, a rapidly changing ecosystem. Validation of the method found compelling accuracy in comparison with established genotyping approaches within different diversity contexts. In experimental and environmental samples, we show that MPB can detect meaningful patterns of population dynamics, resolving allelic stability and shifts within a key diatom species in response to experimental treatments as well as different bloom phases and years. Through our novel MPB approach, we produced a large dataset of populations at different time-points and locations with comparably little effort. Results like this can add insights into the roles of selection and plasticity in natural protist populations under stable experimental but also variable field conditions. Especially for organisms where genotype sampling remains challenging, MPB holds great potential to efficiently resolve eco-evolutionary dynamics and to assess the mechanisms and limits of resilience to environmental stressors. This article is protected by copyright. All rights reserved.
Thalassiosira hyalina and Nitzschia frigida are important members of Arctic pelagic and sympagic (sea‐ice associated) diatom communities. We investigated the effects of light stress (shift from 20 to 380 µmol photons m‐2 s‐1, resembling upwelling or ice break‐up) under contemporary and future pCO2 (400 vs. 1000 µatm). The responses in growth, elemental composition, pigmentation and photophysiology were followed over 120 h and are discussed together with underlying gene expression patterns. Stress response and subsequent re‐acclimation were efficiently facilitated by T. hyalina, which showed only moderate changes in photophysiology and elemental composition, and thrived under high‐light after 120 h. In N. frigida, photochemical damage and oxidative stress appeared to outweigh cellular defenses, causing dysfunctional photophysiology and reduced growth. pCO2 alone did not specifically influence gene expression, but amplified the transcriptomic reactions to light stress, indicating that pCO2 affects metabolic equilibria rather than sensitive genes. Large differences in acclimation capacities towards high‐light and high pCO2 between T. hyalina and N. frigida indicate species‐specific mechanisms in coping with the two stressors, which may reflect their respective ecological niches. This could potentially alter the balance between sympagic vs. pelagic primary production in a future Arctic.
Compared to the rest of the globe, the Arctic Ocean is affected disproportionately by climate change. Despite these fast environmental changes, we currently know little about the effects of ocean acidification (OA) on marine key species in this area. Moreover, the existing studies typically test the effects of OA under constant, hence artificial light fields. In this study, the abundant Arctic picoeukaryote Micromonas pusilla was acclimated to current (400 μatm) and future (1000 μatm) pCO2 levels under a constant as well as dynamic light, simulating natural light fields as experienced in the upper mixed layer. To describe and understand the responses to these drivers, growth, particulate organic carbon (POC) production, elemental composition, photophysiology and reactive oxygen species (ROS) production were analysed. M. pusilla was able to benefit from OA on various scales, ranging from an increase in growth rates to enhanced photosynthetic capacity, irrespective of the light regime. These beneficial effects were, however, not reflected in the POC production rates, which can be explained by energy partitioning towards cell division rather than biomass build-up. In the dynamic light regime, M. pusilla was able to optimise its photophysiology for effective light usage during both low and high light periods. This effective photoacclimation, which was achieved by modifications to photosystem II (PSII), imposed high metabolic costs leading to a reduction in growth and POC production rates when compared to constant light. There were no significant interactions observed between dynamic light and OA, indicating that M. pusilla was able maintain effective photoacclimation without increased photoinactivation under high pCO2. Based on these findings, physiologically plastic M. pusilla may exhibit a robust positive response to future Arctic Ocean conditions.
In the Arctic Ocean, climate change effects such as warming and ocean acidification (OA) are manifesting faster than in other regions. Yet, we are lacking a mechanistic understanding of the interactive effects of these drivers on Arctic primary producers. In the current study, one of the most abundant species of the Arctic Ocean, the prasinophyte Micromonas pusilla, was exposed to a range of different pCO2 levels at two temperatures representing realistic current and future scenarios for nutrient-replete conditions. We observed that warming and OA synergistically increased growth rates at intermediate to high pCO2 levels. Furthermore, elevated temperatures shifted the pCO2 optimum of biomass production to higher levels. Based on changes in cellular composition and photophysiology, we hypothesise that the observed synergies can be explained by beneficial effects of warming on carbon fixation in combination with facilitated carbon acquisition under OA. Our findings help to understand the higher abundances of picoeukaryotes such as M. pusilla under OA, as has been observed in many mesocosm studies.
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. This article is protected by copyright. All rights reserved.
The Arctic and subarctic shelf seas, which sustain large fisheries and contribute to global biogeochemical cycling, are particularly sensitive to ongoing ocean acidification (that is, decreasing seawater pH due to anthropogenic CO2 emissions). Yet, little information is available on the effects of ocean acidification on natural phytoplankton assemblages, which are the main primary producers in high-latitude waters. Here we show that coastal Arctic and subarctic primary production is largely insensitive to ocean acidification over a large range of light and temperature levels in different experimental designs. Out of ten CO2-manipulation treatments, significant ocean acidification effects on primary productivity were observed only once (at temperatures below 2 °C), and shifts in the species composition occurred only three times (without correlation to specific experimental conditions). These results imply a high capacity to compensate for environmental variability, which can be understood in light of the environmental history, tolerance ranges and intraspecific diversity of the dominant phytoplankton species.
In the Arctic Ocean, climate change effects such as warming and ocean acidification (OA) are manifesting faster than in other regions. Yet, we are lacking a mechanistic understanding of the interactive effects of these drivers on Arctic primary producers. In the current study, one of the most abundant species of the Arctic Ocean, the prasinophyte Micromonas pusilla, was exposed to a range of different pCO2 levels at two temperatures representing realistic scenarios for current and future conditions. We observed that warming and OA synergistically increased growth rates at intermediate to high pCO2 levels. Furthermore, elevated temperatures shifted the pCO2-optimum of biomass production to higher levels. Based on changes in cellular composition and photophysiology, we hypothesise that the observed synergies can be explained by beneficial effects of warming on carbon fixation in combination with facilitated carbon acquisition under OA. Our findings help to understand the higher abundances of picoeukaryotes such as M. pusilla under OA, as has been observed in many mesocosm studies.
The authors regret an error in the published article, where incorrect data was used to produce Figure 2, showing the temporal development of pH over the duration of the experiment. The corrected Fig. 2 shows that the error did not affect the interpretation of nor the conclusions drawn from the present dataset. The original article has been corrected.
The Arctic Ocean is a region particularly prone to ongoing ocean acidification (OA) and climate-driven changes. The influence of these changes on Arctic phytoplankton assemblages, however, remains poorly understood. In order to understand how OA and enhanced irradiances (e.g., resulting from sea–ice retreat) will alter the species composition, primary production, and eco-physiology of Arctic phytoplankton, we conducted an incubation experiment with an assemblage from Baffin Bay (71°N, 68°W) under different carbonate chemistry and irradiance regimes. Seawater was collected from just below the deep Chl a maximum, and the resident phytoplankton were exposed to 380 and 1000 µatm pCO2 at both 15 and 35% incident irradiance. On-deck incubations, in which temperatures were 6 °C above in situ conditions, were monitored for phytoplankton growth, biomass stoichiometry, net primary production, photo-physiology, and taxonomic composition. During the 8-day experiment, taxonomic diversity decreased and the diatom Chaetoceros socialis became increasingly dominant irrespective of light or CO2 levels. We found no statistically significant effects from either higher CO2 or light on physiological properties of phytoplankton during the experiment. We did, however, observe an initial 2-day stress response in all treatments, and slight photo-physiological responses to higher CO2 and light during the first five days of the incubation. Our results thus indicate high resistance of Arctic phytoplankton to OA and enhanced irradiance levels, challenging the commonly predicted stimulatory effects of enhanced CO2 and light availability for primary production.
In order to understand how ocean acidification (OA) and enhanced irradiance levels might alter phytoplankton eco-physiology, productivity and species composition, we conducted an incubation experiment with a natural plankton assemblage from sub-surface Subarctic waters (Davis Strait, 63 • N). The phytoplankton assemblage was exposed to 380 and 1,000 µatm pCO 2 at both 15 and 35% surface irradiance over 2 weeks. The incubations were monitored and characterized in terms of their photo-physiology, biomass stoichiometry, primary production and dominant phytoplankton species. We found that the phytoplankton assemblage exhibited pronounced highlight stress in the first days of the experiment (20–30% reduction in photosynthetic efficiency, F v /F m). This stress signal was more pronounced when grown under OA and high light, indicating interactive effects of these environmental variables. Primary production in the high light treatments was reduced by 20% under OA compared to ambient pCO 2 levels. Over the course of the experiment, the assemblage fully acclimated to the applied treatments, achieving similar bulk characteristics (e.g., net primary production and elemental stoichiometry) under all conditions. We did, however, observe a pCO 2-dependent shift in the dominant diatom species, with Pseudonitzschia sp. dominating under low and Fragilariopsis sp. under high pCO 2 levels. Our results indicate an unexpectedly high level of resilience of Subarctic phytoplankton to OA and enhanced irradiance levels. The co-occurring shift in dominant species suggests functional redundancy to be an important, but so-far largely overlooked mechanism for resilience toward climate change.
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 community 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.