skip to main content

Title: Effects of Temperature and Nutrient Supply on Resource Allocation, Photosynthetic Strategy, and Metabolic Rates of Synechococcus sp.

Temperature and nutrient supply are key factors that control phytoplankton ecophysiology, but their role is commonly investigated in isolation. Their combined effect on resource allocation, photosynthetic strategy, and metabolism remains poorly understood. To characterize the photosynthetic strategy and resource allocation under different conditions, we analyzed the responses of a marine cyanobacterium (SynechococcusPCC7002) to multiple combinations of temperature and nutrient supply. We measured the abundance of proteins involved in the dark (RuBisCO,rbcL) and light (PhotosystemII, psbA) photosynthetic reactions, the content of chlorophylla, carbon and nitrogen, and the rates of photosynthesis, respiration, and growth. We found thatrbcL and psbA abundance increased with nutrient supply, whereas a temperature‐induced increase in psbA occurred only in nutrient‐replete treatments. Low temperature and abundant nutrients caused increased RuBisCOabundance, a pattern we observed also in natural phytoplankton assemblages across a wide latitudinal range. Photosynthesis and respiration increased with temperature only under nutrient‐sufficient conditions. These results suggest that nutrient supply exerts a stronger effect than temperature upon both photosynthetic protein abundance and metabolic rates inSynechococcussp. and that the temperature effect on photosynthetic physiology and metabolism is nutrient dependent. The preferential resource allocation into the light instead of the dark reactions of photosynthesis as temperature rises is likely related to the different temperature dependence of dark‐reaction enzymatic rates versus photochemistry. These findings contribute to our understanding of the strategies for photosynthetic energy allocation in phytoplankton inhabiting contrasting environments.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;
Publisher / Repository:
Date Published:
Journal Name:
Journal of Phycology
Page Range / eLocation ID:
p. 818-829
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary

    The widespread coccolithophoreEmiliania huxleyiis an abundant oceanic phytoplankton, impacting the global cycling of carbon through both photosynthesis and calcification. Here, we examined the transcriptional responses of populations ofE. huxleyiin the North Pacific Subtropical Gyre to shifts in the nutrient environment. Using a metatranscriptomic approach, nutrient‐amended microcosm studies were used to track the global metabolism ofE. huxleyi. The addition of nitrate led to significant changes in transcript abundance for gene pathways involved in nitrogen and phosphorus metabolism, with a decrease in the abundance of genes involved in the acquisition of nitrogen (e.g. N‐transporters) and an increase in the abundance of genes associated with phosphate acquisition (e.g. phosphatases). Simultaneously, after the addition of nitrate, genes associated with calcification and genes unique to the diploid life stages ofE. huxleyisignificantly increased. These results suggest that nitrogen is a major driver of the physiological ecology ofE. huxleyiin this system and further suggest that the addition of nitrate drives shifts in the dominant life‐stage of the population. Together, these results underscore the importance of phenotypic plasticity to the success ofE. huxleyi, a characteristic that likely underpins its ability to thrive across a variety of marine environments.

    more » « less
  2. Summary

    Food chain efficiency (FCE), the proportion of primary production converted to production of the top trophic level, can influence several ecosystem services as well as the biodiversity and productivity of each trophic level. AquaticFCEis affected by light and nutrient supply, largely via effects on primary producer stoichiometry that propagate to herbivores and then carnivores. Here, we test the hypothesis that the identity of the top carnivore mediatesFCEresponses to changes in light and nutrient supply.

    We conducted a large‐scale, 6‐week mesocosm experiment in which we manipulated light and nutrient (nitrogen and phosphorus) supply and the identity of the carnivore in a 2 × 2 × 2 factorial design. We quantified the response ofFCEand the biomass and productivity of each trophic level (phytoplankton, zooplankton, and carnivore). We used an invertebrate,Chaoborus americanus, and a vertebrate, bluegill sunfish (Lepomis macrochirus), as the two carnivores in this study because of the large difference in phosphorus requirements between these taxa.

    We predicted that bluegill would be more likely to experience P‐limitation due to higher P requirements, and hence thatFCEwould be lower in the bluegill treatments than in theChaoborustreatments. We also expected the interactive effect of light and nutrients to be stronger in the bluegill treatments. Within a carnivore treatment, we predicted highestFCEunder low light and high nutrient supply, as these conditions would produce high‐quality (low C:nutrient) algal resources. In contrast, if food quantity had a stronger effect on carnivore production than food quality, carnivore production would increase proportionally with primary production, thusFCEwould be similar across light and nutrient treatments.

    Carnivore identity mediated the effects of light and nutrients onFCE, and as predictedFCEwas higher in food chains withChaoborusthan with bluegill. Also as predicted,FCEinChaoborustreatments was higher under low light. However,FCEin bluegill treatments was higher at high light supply, opposite to our predictions. In addition, bluegill production increased proportionally with primary production, whileChaoborusproduction was not correlated with primary production, suggesting that bluegill responded more strongly to food quantity than to food quality. These carnivore taxa differ in traits other than body stoichiometry, for example, feeding selectivity, which may have contributed to the observed differences inFCEbetween carnivores.

    Comparison of our results with those from previous experiments showed thatFCEresponds similarly to light and nutrients in food chains withChaoborusand larval fish (gizzard shad: Clupeidae), but very differently in food chains with bluegill. These findings warrant further investigation into the mechanisms related to carnivore identity (e.g., developmental stage, feeding selectivity) underlying these responses, and highlight the importance of considering both top‐down and bottom‐up effects when evaluating food chain responses to changing light and nutrient conditions.

    more » « less
  3. Summary

    Steady‐state photosyntheticCO2responses (A/Cicurves) are used to assess environmental responses of photosynthetic traits and to predict future vegetative carbon uptake through modeling. The recent development of rapidA/Cicurves (RACiRs) permits faster assessment of these traits by continuously changing [CO2] around the leaf, and may reveal additional photosynthetic properties beyond what is practical or possible with steady‐state methods.

    Gas exchange necessarily incorporates photosynthesis and (photo)respiration. Each process was expected to respond on different timescales due to differences in metabolite compartmentation, biochemistry and diffusive pathways. We hypothesized that metabolic lags in photorespiration relative to photosynthesis/respiration andCO2diffusional limitations can be detected by varying the rate of change in [CO2] duringRACiR assays. We tested these hypotheses through modeling and experiments at ambient and 2% oxygen.

    Our data show that photorespiratory delays cause offsets in predictedCO2compensation points that are dependent on the rate of change in [CO2]. Diffusional limitations may reduce the rate of change in chloroplastic [CO2], causing a reduction in apparentRACiR slopes under highCO2ramp rates.

    MultirateRACiRs may prove useful in assessing diffusional limitations to gas exchange and photorespiratory rates.

    more » « less
  4. Summary

    Seed development largely depends on the long‐distance transport of sucrose from photosynthetically active source leaves to seed sinks. This source‐to‐sink carbon allocation occurs in the phloem and requires the loading of sucrose into the leaf phloem and, at the sink end, its import into the growing embryo. Both tasks are achieved through the function ofSUTsucrose transporters. In this study, we used vegetable peas (Pisum sativumL.), harvested for human consumption as immature seeds, as our model crop and simultaneously overexpressed the endogenousSUT1transporter in the leaf phloem and in cotyledon epidermal cells where import into the embryo occurs. Using this ‘Push‐and‐Pull’ approach, the transgenicSUT1plants displayed increased sucrose phloem loading and carbon movement from source to sink causing higher sucrose levels in developing pea seeds. The enhanced sucrose partitioning further led to improved photosynthesis rates, increased leaf nitrogen assimilation, and enhanced source‐to‐sink transport of amino acids. Embryo loading with amino acids was also increased inSUT1‐overexpressors resulting in higher protein levels in immature seeds. Further, transgenic plants grown until desiccation produced more seed protein and starch, as well as higher seed yields than the wild‐type plants. Together, the results demonstrate that theSUT1‐overexpressing plants with enhanced sucrose allocation to sinks adjust leaf carbon and nitrogen metabolism, and amino acid partitioning in order to accommodate the increased assimilate demand of growing seeds. We further provide evidence that the combined Pushand‐Pull approach for enhancing carbon transport is a successful strategy for improving seed yields and nutritional quality in legumes.

    more » « less
  5. Abstract

    Climate warming is affecting the structure and function of river ecosystems, including their role in transforming and transporting carbon (C), nitrogen (N), and phosphorus (P). Predicting how river ecosystems respond to warming has been hindered by a dearth of information about how otherwise well‐studied physiological responses to temperature scale from organismal to ecosystem levels. We conducted an ecosystem‐level temperature manipulation to quantify how coupling of stream ecosystem metabolism and nutrient uptake responded to a realistic warming scenario. A ~3.3°C increase in mean water temperature altered coupling of C, N, and P fluxes in ways inconsistent with single‐species laboratory experiments. Net primary production tripled during the year of experimental warming, while whole‐stream N and P uptake rates did not change, resulting in 289% and 281% increases in autotrophic dissolved inorganic N and P use efficiency (UE), respectively. Increased ecosystem production was a product of unexpectedly large increases in mass‐specific net primary production and autotroph biomass, supported by (i) combined increases in resource availability (via N mineralization and N2fixation) and (ii) elevated resource use efficiency, the latter associated with changes in community structure. These large changes in C and nutrient cycling could not have been predicted from the physiological effects of temperature alone. Our experiment provides clear ecosystem‐level evidence that warming can shift the balance between C and nutrient cycling in rivers, demonstrating that warming will alter the important role of in‐stream processes in C, N, and P transformations. Moreover, our results reveal a key role for nutrient supply and use efficiency in mediating responses of primary producers to climate warming.

    more » « less