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What Colin Reynolds could tell us about nutrient limitation, N:P ratios and eutrophication control
(2020)
Colin Reynolds exquisitely consolidated our understanding of driving forces shaping phytoplankton communities and those setting the upper limit to biomass yield, with limitation typically shifting from light in winter to phosphorus in spring. Nonetheless, co-limitation is frequently postulated from enhanced growth responses to enrichments with both N and P or from N:P ranging around the Redfield ratio, concluding a need to reduce both N and P in order to mitigate eutrophication. Here, we review the current understanding of limitation through N and P and of co-limitation. We conclude that Reynolds is still correct: (i) Liebig's law of the minimum holds and reducing P is sufficient, provided concentrations achieved are low enough; (ii) analyses of nutrient limitation need to exclude evidently non-limiting situations, i.e. where soluble P exceeds 3-10 mu g/l, dissolved N exceeds 100-130 mu g/l and total P and N support high biomass levels with self-shading causing light limitation; (iii) additionally decreasing N to limiting concentrations may be useful in specific situations (e.g. shallow waterbodies with high internal P and pronounced denitrification); (iv) management decisions require local, situation-specific assessments. The value of research on stoichiometry and co-limitation lies in promoting our understanding of phytoplankton ecophysiology and community ecology.
In the deep, cooler layers of clear, nutrient-poor, stratified water bodies, phytoplankton often accumulate to form a thin band or "deep chlorophyll maximum" (DCM) of ecological importance. Under such conditions, these photosynthetic microorganisms may be close to their physiological compensation points and to the boundaries of their ecological tolerance. To grow and survive any resulting energy limitation, DCM species are thought to exhibit highly specialised or flexible acclimation strategies. In this study, we investigated several of the adaptable ecophysiological strategies potentially employed by one such species, Chlamydomonas acidophila: a motile, unicellular, phytoplanktonic flagellate that often dominates the DCM in stratified, acidic lakes. Physiological and behavioural responses were measured in laboratory experiments and were subsequently related to field observations. Results showed moderate light compensation points for photosynthesis and growth at 22A degrees C, relatively low maintenance costs, a behavioural preference for low to moderate light, and a decreased compensation point for photosynthesis at 8A degrees C. Even though this flagellated alga exhibited a physiologically mediated diel vertical migration in the field, migrating upwards slightly during the day, the ambient light reaching the DCM was below compensation points, and so calculations of daily net photosynthetic gain showed that survival by purely autotrophic means was not possible. Results suggested that strategies such as low-light acclimation, small-scale directed movements towards light, a capacity for mixotrophic growth, acclimation to low temperature, in situ exposure to low O-2, high CO2 and high P concentrations, and an avoidance of predation, could combine to help overcome this energetic dilemma and explain the occurrence of the DCM. Therefore, corroborating the deceptive ecophysiological complexity of this and similar organisms, only a suite of complementary strategies can facilitate the survival of C. acidophila in this DCM.
Organisms often employ ecophysiological strategies to exploit environmental conditions and ensure bio-energetic success. However, the many complexities involved in the differential expression and flexibility of these strategies are rarely fully understood. Therefore, for the first time, using a three-part cross-disciplinary laboratory experimental analysis, we investigated the diversity and plasticity of photoresponsive traits employed by one family of environmentally contrasting, ecologically important phytoflagellates. The results demonstrated an extensive inter-species phenotypic diversity of behavioural, physiological, and compositional photoresponse across the Chlamydomonadaceae, and a multifaceted intra-species phenotypic plasticity, involving a broad range of beneficial photoacclimation strategies, often attributable to environmental predisposition and phylogenetic differentiation. Deceptively diverse and sophisticated strong (population and individual cell) behavioural photoresponses were observed, with divergence from a general preference for low light (and flexibility) dictated by intra-familial differences in typical habitat (salinity and trophy) and phylogeny. Notably, contrasting lower, narrow, and flexible compared with higher, broad, and stable preferences were observed in freshwater vs. brackish and marine species. Complex diversity and plasticity in physiological and compositional photoresponses were also discovered. Metabolic characteristics (such as growth rates, respiratory costs and photosynthetic capacity, efficiency, compensation and saturation points) varied elaborately with species, typical habitat (often varying more in eutrophic species, such as Chlamydomonas reinhardtii), and culture irradiance (adjusting to optimise energy acquisition and suggesting some propensity for low light). Considerable variations in intracellular pigment and biochemical composition were also recorded. Photosynthetic and accessory pigments (such as chlorophyll a, xanthophyll-cycle components, chlorophyll a:b and chlorophyll a:carotenoid ratios, fatty acid content and saturation ratios) varied with phylogeny and typical habitat (to attune photosystem ratios in different trophic conditions and to optimise shade adaptation, photoprotection, and thylakoid architecture, particularly in freshwater environments), and changed with irradiance (as reaction and harvesting centres adjusted to modulate absorption and quantum yield). The complex, concomitant nature of the results also advocated an integrative approach in future investigations. Overall, these nuanced, diverse, and flexible photoresponsive traits will greatly contribute to the functional ecology of these organisms, addressing environmental heterogeneity and potentially shaping individual fitness, spatial and temporal distribution, prevalence, and ecosystem dynamics.
Organisms often employ ecophysiological strategies to exploit environmental conditions and ensure bio-energetic success. However, the many complexities involved in the differential expression and flexibility of these strategies are rarely fully understood. Therefore, for the first time, using a three-part cross-disciplinary laboratory experimental analysis, we investigated the diversity and plasticity of photoresponsive traits employed by one family of environmentally contrasting, ecologically important phytoflagellates. The results demonstrated an extensive inter-species phenotypic diversity of behavioural, physiological, and compositional photoresponse across the Chlamydomonadaceae, and a multifaceted intra-species phenotypic plasticity, involving a broad range of beneficial photoacclimation strategies, often attributable to environmental predisposition and phylogenetic differentiation. Deceptively diverse and sophisticated strong (population and individual cell) behavioural photoresponses were observed, with divergence from a general preference for low light (and flexibility) dictated by intra-familial differences in typical habitat (salinity and trophy) and phylogeny. Notably, contrasting lower, narrow, and flexible compared with higher, broad, and stable preferences were observed in freshwater vs. brackish and marine species. Complex diversity and plasticity in physiological and compositional photoresponses were also discovered. Metabolic characteristics (such as growth rates, respiratory costs and photosynthetic capacity, efficiency, compensation and saturation points) varied elaborately with species, typical habitat (often varying more in eutrophic species, such as Chlamydomonas reinhardtii), and culture irradiance (adjusting to optimise energy acquisition and suggesting some propensity for low light). Considerable variations in intracellular pigment and biochemical composition were also recorded. Photosynthetic and accessory pigments (such as chlorophyll a, xanthophyll-cycle components, chlorophyll a:b and chlorophyll a:carotenoid ratios, fatty acid content and saturation ratios) varied with phylogeny and typical habitat (to attune photosystem ratios in different trophic conditions and to optimise shade adaptation, photoprotection, and thylakoid architecture, particularly in freshwater environments), and changed with irradiance (as reaction and harvesting centres adjusted to modulate absorption and quantum yield). The complex, concomitant nature of the results also advocated an integrative approach in future investigations. Overall, these nuanced, diverse, and flexible photoresponsive traits will greatly contribute to the functional ecology of these organisms, addressing environmental heterogeneity and potentially shaping individual fitness, spatial and temporal distribution, prevalence, and ecosystem dynamics.
Chlamydomonas acidophila, a unicellular green alga, is a dominant phytoplankton species in acidic water bodies, facing severe environmental conditions such as low pH and high heavy metal concentrations. We examined the pH-, and temperature-dependent accumulation of heat-shock proteins in this alga to determine whether heat-shock proteins play a role in adaptation to their environment. Our results show increased heat-shock proteins accumulation at suboptimal pHs, which were not connected with any change in intracellular pH. In comparison to the mesophilic Chlamydomonas reinhardtii, the acidophilic species exhibited significantly higher accumulations of heat-shock proteins under control conditions, indicating an environmental adaptation of increased basal levels of heat-shock proteins. The results suggest that heat- shock proteins might play a role in the adaptation of C. acidophila, and possibly other acidophilic algae, to their extreme environment
In extremely acidic lakes, low primary production rates have been measured. We assumed that proton stress might explain these observations and therefore investigated the photosynthetic behaviour of a Chlamydomonas species, a main primary producer in acidic lakes, over a range of pH values. Identified as C. acidophila using small subunit rDNA analysis, this species is identical to other isolates from acidic environments in Europe and South America, suggesting a worldwide distribution. Laboratory experiments with C. acidophila, revealed a broad pH-tolerance for growth and photosynthesis, the lower pH limit lying at pH 1.5 and the upper limit at pH 7. Growth rates at optimum pH conditions (pH 3 and 5) were equal to those of the mesophilic Chlamydomonas reinhardtii. In contrast, photosynthetic rates were significantly higher, suggesting that higher photosynthetic rates compensated for higher dark respiration rates, as confirmed experimentally. Electron transport capacities of PSI and PSII, P700(+) re-reduction times and measurements of PSII fluorescence revealed the induction of alternative electron transport mechanisms, such as chlororespiration, state transitions and cyclic electron transport, only at suboptimal pH values (pH 1.5; 4 and 6-7). The results indicate, that C. acidophila is well adapted to low pH and that the relatively low primary production rates are not a result of pH stress
1. The unicellular green alga Chlamydomonas acidophila accumulates in a thin phytoplankton layer in the hypolimnion (deep chlorophyll maximum, DCM) of an extremely acidic lake (Lake 111, pH 2.6, Lusatia, Germany), in which the underwater light spectrum is distorted and red-shifted. 2. Chlamydomonas acidophila exhibited a significantly higher absorption efficiency and a higher cellular chlorophyll b content when incubated in the red shifted underwater light of Lake 111 than in a typical, blue-green dominated, light spectrum. 3. Chlamydomonas acidophila has excellent low light acclimation properties (increased chlorophyll b content, increased oxygen yield and a low light saturation point for photosynthesis) that support survival of the species in the low light climate of the DCM. 4. In situ acclimation to the DCM under low light and temperature decreased maximum photosynthetic rate in autotrophic C. acidophila cultures, whereas the presence of glucose under these conditions enhanced photosynthetic efficiency and capacity. 5. The adaptive abilities of C. acidophila to light and temperature shown in this study, in combination with the absence of potent competitors because of low lake pH, most probably enable the unusual dominance of the green alga in the DCM of Lake 111
Pharmaceuticals are found in freshwater ecosystems where even low concentrations in the range of ng L−1 may affect aquatic organisms. In the current study, we investigated the effects of chronic exposure to three pharmaceuticals on two microalgae, a potential modulation of the effects by additional inorganic phosphorus (Pi) limitation, and a potential propagation of the pharmaceuticals’ effect across a trophic interaction. The latter considers that pharmaceuticals are bioaccumulated by algae, potentially metabolized into more (or less) toxic derivates and consequently consumed by zooplankton. We cultured Acutodesmus obliquus and Nannochloropsis limnetica in Pi-replete and Pi-limited medium contaminated with one of three commonly human used pharmaceuticals: fluoxetine, ibuprofen, and propranolol. Secondly, we tested to what extent first level consumers (Daphnia magna) were affected when fed with pharmaceutical-grown algae. Chronic exposure, covering 30 generations, led to (i) decreased cell numbers of A. obliquus in the presence of fluoxetine (under Pi-replete conditions) (ii) increased carotenoid to chlorophyll ratios in N. limnetica (under Pi-limited conditions), and (iii) increased photosynthetic yields in A. obliquus (in both Pi-conditions). In addition, ibuprofen affected both algae and their consumer: Feeding ibuprofen-contaminated algae to Pi-stressed D. magna improved their survival. We demonstrate, that even very low concentrations of pharmaceuticals present in freshwater ecosystems can significantly affect aquatic organisms when chronically exposed. Our study indicates that pharmaceutical effects can cross trophic levels and travel up the food chain.
Recently pharmaceuticals have become significant environmental pollutants in aquatic ecosystems, that could affect primary producers such as microalgae. Here we analyzed the effect of pharmaceuticals on the photosynthesis of microalgae commonly found in freshwater-two species of Chlorophyceae and a member of the Eustigmatophyceae, via PAM fluorometry. As pharmaceuticals, three medicines often consumed in households were chosen: (i) fluoxetine, an antidepressant, (ii) propranolol, a beta-blocker and (iii) ibuprofen, an anti-inflammatory and analgesic medicine. The EC50 for the quantum yield of photosystem II in phytoplankton acclimated to inorganic phosphorus (P-i)-replete and P-i-limited conditions was estimated. Acute toxicity experiments over a 5 h exposure revealed that Nannochloropsis limnetica was the least sensitive to pharmaceuticals in its photosynthetic yield out of all species tested. Although the estimation of sub-lethal effects can be vital in contrast to that of LC(50)s, the EC50 values in all species and for all medicines were orders of magnitude higher than concentrations found in polluted surface water. Chlamydomonas reinhardtii was the most sensitive to fluoxetine (EC50 of 1.6 mg L-1), and propranolol (EC50 of 3 mg L-1). Acutodesmus obliquus was most sensitive to ibuprofen (EC50 of 288 mg L-1). Additionally, the sensitivity to the pharmaceuticals changed under a P-i-limitation; the green algae became less sensitive to fluoxetine and propranolol. In contrast, P-i-limited algal species were more sensitive to ibuprofen. Our results suggest that the sensitivity of algae to pharmaceuticals is (i) highly compound- and species-specific and (ii) dependent on the cellular P status.
Inorganic phosphorus (P-i) is often the primary limiting nutrient in freshwater ecosystems. Since P(i-)limitation affects energy transduction, and inorganic carbon (C-i) acquisition can be energy demanding, C(i-)acquisition strategies were compared in four species of green algae grown under P-i-replete and P-i-limited conditions predominantly at low and partly at high CO2. Although P-i-limitation was evident by the 10-fold higher cellular C:P ratio and enhanced phosphatase activity, it only decreased C-i-acquisition to a small extent. Nonetheless, the effects of Pi-limitation on both CO2 and HCO3- acquisition were demonstrated. Decreased CO2 acquisition under conditions of Pi limitation was mainly visible in the maximum uptake rate (V-max) and, for the neutrophile Scenedesmus vacuolatus, in the affinity for CO2 acquisition. Discrimination against C-13 was higher under P-i-limited, high CO2 conditions, compared with P-i-replete, highCO(2) conditions, in Chlamydomonas acidophila and S. vacuolatus. In the pH-drift experiments, HCO3- acquisition was reduced in P-i-limited C. reinhardtii. In general, energy demanding bicarbonate uptake was indicated by the less strong discrimination against (13)Cunder lowCO(2) conditions in the neutrophiles (HCO3- users), separating them from the acidophilic or acidotolerant species (CO2 users). The high variability of the influence of Pi supply among different green algal species is linked to their species-specific C(i-)acquisition strategies.