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Negative effects of P-buffering and pH on photosynthetic activity of planktonic desmid species
(2004)
The photosynthetic activities of three planktonic desmid species (Staurastrum brachiatum, Staurodesmus cuspidatus var. curvatus, and Staurastrum chaetoceras) were compared after adaptation to medium enriched with either a 20 mM Na+- phosphate (P) or HEPES buffer. Incubations up to 2 d were carried out at pH 6 or 8 under normal air or air enriched with 5 % CO2. Gross maximum photosynthetic rate (Pmax) and growth rate were decreased in both S. brachiatum and Std. cuspidatus at higher pH when using the HEPES buffer and this effect was independent of CO2 concentration, indicating that pH had an inhibitory effect on photosynthesis and growth in these species. The P-buffer at pH 8 caused a large decrease in Pmax and quantum yield for charge separation in photosystem 2 (PS2), compared to HEPES-buffered algae. This effect was very large in both S. brachiatum and Std. cuspidatus, two species characteristic of soft water lakes, but also significant in S. chaetoceras, a species dominant in eutrophic, hard water lakes. The decreased Pmax in P- buffer could not be related to a significant increase in cellular P content known to be responsible for inhibition in isolated chloroplasts. Experiments at pH 6 and 8 showed that two conditions, high pH and high Na+ concentration, both contributed to the decreased Pmax and quantum yield in the desmids. Effects of a P-buffer were less pronounced by using K+-P buffer. The use of P-buffer at pH 8 possibly resulted in high irradiance stress in all species, indicated by damage in the PS2 core complex. In the soft water species pH 8 resulted in increased non-photochemical quenching together with a high de-epoxidation state of the xanthophyll cycle pigments.
Fatty acid profiles were used to characterize nutritional pathways in Chlamydomonas sp. isolated from an acidic mining lake (pH 2.7). Surprisingly, profiles of Chlamydomonas sp. grown in the lab under photoautotrophic, mixotrophic, and heterotrophic conditions at in situ deep strata lake water temperatures (8C) were very similar, polyunsaturated fatty acids including a-linolenic acid (18:3x3) and 16:4x3 along with palmitic acid (16:0) being most abundant. Therefore, heterotrophic growth of Chlamydomonas sp. at low temperatures can result in high concentrations of polyunsaturated fatty acids, as previously only described for some psychrophilic bacteria. By contrast, the cultivation of isolated Chlamydomonas sp. at 20C, reflecting surface water temperatures, provided fatty acid patterns characteristic of the nutrition strategy applied: the concentration of polyunsaturated fatty acids decreased when the growth pathway changed from photoautotrophic via mixotrophic to heterotrophic. Total fatty acid concentration also diminished in this order. Principal component analysis confirmed the significance of FA profiling to mirror nutritional pathways. Lake- water analysis revealed low concentrations of dissolved organic carbon, mainly consisting of polymeric fulvic acids that are unable to support heterotrophic growth of Chlamydomonas sp. Polymeric fulvic acids present in the deeper strata of the lake turned out to be formed in situ on the basis of organic monomers including reduced sulfur-containing ones, as revealed by thermochemolysis and pyrolysis. Growth of Chlamydomonas sp. in the deep chlorophyll maximum is therefore assumed to mainly result from photosynthesis, despite very low photon densities. Phytol-including metabolites proved to be significant biomarkers to indicate the nutritional pathway of Chlamydomonas sp. a, x-Dicarboxylic acidsùlight- induced degradation products of unsaturated fatty acidsùappeared to be good indicators of photooxidative alterations to the algal species under study.
Carbon acquisition mechanisms by planktonic desmids and their link to ecological distribution
(2005)
To test if different inorganic carbon (C-i) uptake mechanisms underlie the ecological distribution pattern of planktonic desmids, we performed pH-drift experiments with 12 strains, belonging to seven species, originating from lakes of different pH. Staurastrum brachiatum Ralfs and Staurodesmus cuspidatus (Ralfs) Teil. var. curvatus (W. West) Teil., species confined to acidic, soft water habitats, showed remarkably different behavior in the pH drift experiments: S. brachiatum appeared to use CO2 only, whereas Staurodesmus cuspidatus appeared to use HCO3- as well. Staurastrum chaetoceras (Schr.) Smith and Staurastrum planctonicum Teil, species well-known for their abundant occurrence in alkaline waters, were the most effective at using HCO3-. Other species, to be encountered in both slightly acidic and slightly alkaline waters, took an intermediate position. Experiments using specific inhibitors suggested that Cosmarium abbreviatum Rac. var. planctonicum W. & G.S. West and S. brachiatum use CO2 by an active CO2 uptake mechanism, whereas S. chaetoceras and Staurodesmus cuspidatus showed an active HCO3- uptake pattern. Most likely, these active uptake mechanisms make use of H+-ATPase, as none of the desmids expressed significant carbonic anhydrase activity. A series of strains of Staurastrum planctonicum isolated from different habitats, all clustered in between the species using HCO3-, but no further differentiation was observed. Therefore, desmids cannot be simply characterized as exclusive CO2 users, and the ecological distribution pattern of a desmid species does not unequivocally link to a certain C-i uptake mechanism. Nevertheless, there does appear to be a general ecological link between a species' C-i uptake mechanism and its ecological distribution
Chlamydomonas acidophila Negoro had a higher maximum growth rate upon aeration with 5% CO2 (v/v) than in nonaerated conditions at an external pH above 2. In medium with a pH of 1.0 or 2.0, a decrease in the maximum growth rate was observed upon CO2 aeration in comparison with nonaerated conditions. At both very low and very high external pH conditions, an induction of external carbonic anhydrase was detected; this being more pronounced in CO2-aerated cells than in nonaerated cells. It is therefore suggested that the induction of carbonic anhydrase is part of a stress response in Chlamydomonas acidophila. Comparison of some physiological characteristics of Chlamydomonas acidophila acclimated at pH 2.65 and at pH 6.0, revealed that CO2 aeration increased gross maximum photosynthesis at both pHs, whereas respiration, light acclimation, and photoinhibition were not effected. At pH 2.65, Chlamydomonas acidophila was found to have a carbon-concentrating mechanism under nonaerated conditions, whereas it did not under CO2-aerated conditions at pH 6. The affinity for CO2 use in O-2 production was not dependent on CO2 aeration, but it was much lower at pH 6 than it was at pH 2.65. CO2 kinetic characteristics indicate that the photosynthesis of Chlamydomonas acidophila in its natural environment is not limited by inorganic carbon
Inorganic phosphorus (P-i) and carbon (here, CO2) potentially limit the photosynthesis of phytoplankton simultaneously (colimitation). A single P-i limitation generally reduces photosynthesis, but the effect of a colimitation is not known. Therefore, photosynthesis was measured under P-i-limited conditions and high and low CO2, and osmo-mixotrophic (i.e., growth in the presence of glucose) conditions that result in colimiting conditions in some cases. The green alga Chlamydomonas acidophila Negoro was used as a model organism because low P-i and CO2 concentrations likely influence its photosynthetic rates in its natural environment. Results showed a decreasing maximum photosynthetic rate (P-max) and maximum quantum yield (Theta(II)) with increasing P-i limitation. In addition, a P-i limitation enhanced the relative contribution of dark respiration to P-max (R-d:P-max) but did not influence the compensation light intensity. P-max positively correlated with the cellular RUBISCO content. Osmo-mixotrophic conditions resulted in similar P-max, Theta(II), and RUBISCO content as in high-CO2 cultures. The low-CO2 cultures were colimited by P-i and CO2 and had the highest P-max, Theta(II), and RUBISCO content. Colimiting conditions for P-i and CO2 in C. acidophila resulted in an enhanced mismatch between photosynthesis and growth rates compared to the effect of a single P- i limitation. Primary productivity of colimited phytoplankton could thus be misinterpreted.
Chlamydomonas acidophila faces high heavy-metal concentrations in acidic mining lakes, where it is a dominant phytoplankton species. To investigate the importance of metals to C. acidophila in these lakes, we examined the response of growth, photosynthesis, cell structure, heat-shock protein (Hsp) accumulation, and metal adsorption after incubation in metal-rich lake water and artificial growth medium enriched with metals (Fe, Zn). Incubation in both metal-rich lake water and medium caused large decreases in photosystem II function (though no differences among lakes), but no decrease in growth rate (except for medium + Fe). Concentrations of small Hsps were higher in algae incubated in metal-rich lake- water than in metal-enriched medium, whereas Hsp60 and Hsp70A were either less or equally expressed. Cellular Zn and Fe contents were lower, and metals adsorbed to the cell surface were higher, in lake-water-incubated algae than in medium- grown cells. The results indicate that high Zn or Fe levels are likely not the main or only contributor to the low primary production in mining lakes, and multiple adaptations of C. acidophila (e.g., high Hsp levels, decreased metal accumulation) increase its tolerance to metals and permit survival under such adverse environmental conditions. Supposedly, the main stress factor present in the lake water is an interaction between low P and high Fe concentrations.
Chlamydomonas acidophila, a dominant phytoplankton species in the very acidic Lake 111 (pH 2.7) situated in Germany, faces low concentrations of inorganic phosphorus (P-i), inorganic carbon (C-i) and potassium (K+) in its environment, which may lead to a complex colimitation by these nutrients. We performed laboratory and field investigations to test for P-i limitation and its dependence on C-i and K+ concentrations. The minimum cell quota for phosphorus (Q(0)) and phosphatase enzyme activity were similar to those for neutrophilic algae, despite the low pH and high concentrations of iron and aluminium, indicating no extra metabolic costs or inhibition of enzymes by the extreme environment. The threshold concentration of soluble reactive phosphorus for growth (SRPt), the algal C:P ratio and the alkaline phosphatase enzyme activity all suggested a moderate P-i limitation of C. acidophila in Lake 111. SRPt and Q(0) were higher at low CO2 and K+ concentrations in culture, showing a relationship between C-i and P-i acquisition. Furthermore, SRPt and Q(0) were higher under K+/P-i-colimiting conditions than under P-i-limiting conditions alone, suggesting that K+ concentrations influence P-i limitation in C. acidophila as well. Our results show that a limitation by one macronutrient requires consideration of the availability of the others as their uptake mechanisms depend on each other. Notwithstanding these interactions, C-i or K+ concentrations had no clear influence on the P-i limitation of C. acidophila in Lake 111.
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.
Red, orange or green snow is the macroscopic phenomenon comprising different eukaryotic algae. Little is known about the ecology and nutrient regimes in these algal communities. Therefore, eight snow algal communities from five intensively tinted snow fields in western Spitsbergen were analysed for nutrient concentrations and fatty acid (FA) composition. To evaluate the importance of a shift from green to red forms on the FA-variability of the field samples, four snow algal strains were grown under nitrogen replete and moderate light (+N+ML) or N-limited and high light (-N+HL) conditions. All eight field algal communities were dominated by red and orange cysts. Dissolved nutrient concentration of the snow revealed a broad range of NH4+ (<0.005-1.2 mg NI-1) and only low PO43- (< 18 mu g P I-1) levels. The external nutrient concentration did not reflect cellular nutrient ratios as C:N and C:P ratios of the communities were highest at locations containing relatively high concentrations of NH4- and PO43-. Molar N:P ratios ranged from 11 to 21 and did not suggest clear limitation of a single nutrient. On a per carbon basis, we found a 6-fold difference in total FA content between the eight snow algal communities, ranging from 50 to 300 mg FA g C-1. In multivariate analyses total FA content opposed the cellular N:C quota and a large part of the FA variability among field locations originated from the abundant FAs C181n-9, C18 2n-6, and C183n-3. Both field samples and snow algal strains grown under -N+HL conditions had high concentrations of C181n-9. FAs possibly accumulated due to the cessation of growth. Differences in color and nutritional composition between patches of snow algal communities within one snow field were not directly related to nutrient conditions. We propose that the highly patchy distribution of snow algae within and between snow fields may also result from differences in topographical and geological parameters such as slope, melting water rivulets, and rock formation.
The extremophilic green microalga Chlamydomonas acidophila grows in very acidic waters (pH 2.3-3.4), where CO2 is the sole inorganic carbon source. Previous work has revealed that the species can accumulate inorganic carbon (Ci) and exhibits high affinity CO2 utilization under low-CO2 (air-equilibrium) conditions, similar to organisms with an active CO2 concentrating mechanism (CCM), whereas both processes are down-regulated under high CO2 (4.5 % CO2) conditions. Responses of this species to phosphorus (Pi)-limited conditions suggested a contrasting regulation of the CCM characteristics. Therefore, we measured external carbonic anhydrase (CA(ext)) activities and protein expression (CAH1), the internal pH, Ci accumulation, and CO2-utilization in cells adapted to high or low CO2 under Pi-replete and Pi-limited conditions. Results reveal that C. acidophila expressed CA(ext) activity and expressed a protein cross-reacting with CAH1 (the CA(ext) from Chlamydomonas reinhardtii). Although the function of this CA remains unclear, CA(ext) activity and high affinity CO2 utilization were the highest under low CO2 conditions. C. acidophila accumulated Ci and expressed the CAH1 protein under all conditions tested, and C. reinhardtii also contained substantial amounts of CAH1 protein under Pi-limitation. In conclusion, Ci utilization is optimized in C. acidophila under ecologically relevant conditions, which may enable optimal survival in its extreme Ci- and Pi-limited habitat. The exact physiological and biochemical acclimation remains to be further studied.
The CO2 acquisition was analyzed in Chlamydomonas acidophila at pH 2.4 in a range of medium P and Fe concentrations and at high and low CO2 condition. The inorganic carbon concentrating factor (CCF) was related to cellular P quota (Q(p)), maximum CO2-uptake rate by photosynthesis (V-max; O-2), half saturation constant for CO2 uptake (K-0.5), and medium Fe concentration. There was no effect of the medium Fe concentration on the CCF. The CCF increased with increasing Q(p) in both high and low CO2 grown algae, but maximum Q(p) was 6-fold higher in the low CO2 cells. In high CO2 conditions, the CCF was low, ranging between 0.8 and 3.5. High CCF values up to 9.1 were only observed in CO2-limited cells, but P- and CO2-colimited cells had a low CCF. High CCF did not relate with a low K-0.5 as all CO2-limited cells had a low K-0.5 (<4 mu M CO2). High Ci-pools in cells with high Qp suggested the presence of an active CO2-uptake mechanism. The CCF also increased with increasing V-max; O-2 which reflect an adaptation to the nutrient in highest demand (CO2) under balanced growth conditions. It is proposed that the size of the CCF in C. acidophila is more strongly related to porter density for CO2 uptake (reflected in V-max; O-2) and less- to high-affinity CO2 uptake (low K-0.5) at balanced growth. In addition, high CCF can only be realized with high Q(p).
The extremophilic microalga Chlamydomonas acidophila inhabits very acidic waters (pH 2-3.5), where its growth is often limited by phosphorus (P) or colimited by P and inorganic carbon (CO(2)). Because this alga is a major food source for predators in acidic habitats, we studied its fatty acid content, which reflects their quality as food, grown under a combination of P-limited and different carbon conditions (either mixotrophically with light + glucose or at high or low CO(2), both without glucose). The fatty acid composition largely depended on the cellular P content: stringent P-limited cells had a higher total fatty acid concentration and had a lower percentage of polyunsaturated fatty acids. An additional limitation for CO(2) inhibited this decrease, especially reflected in enhanced concentrations of 18:3(9,12,15) and 16:4(3,7,10,13), resulting in cells relatively rich in polyunsaturated fatty acids under colimiting growth conditions. The percentage of polyunsaturated to total fatty acid content was positively related with maximum photosynthesis under all conditions applied. The two factors, P and CO(2), thus interact in their effect on the fatty acid composition in C. acidophila, and colimited cells P-limited algae can be considered a superior food source for herbivores because of the high total fatty acid content and relative richness in polyunsaturated fatty acids.
Photosynthetic acclimation of phytoplankton to lower irradiation can be met by several strategies such as increasing the affinity for light or increasing antenna size and stacking of the thylakoids. The latter is reflected by a higher proportion of polyunsaturated fatty acids (PUFAs). Additionally, photosynthetic capacity (P-max), respiratory losses, and proton leakage can be reduced under low light. Here we consider the effect of light intensity and phosphorus availability simultaneously on the photosynthetic acclimation and fatty acid composition of four phytoplankters. We studied representatives of the Chlorophyceae, Cryptophyceae and Mediophyceae, all of which are important components of plankton communities in temperate lakes. In our analysis, excluding fatty acid composition, we found different acclimation strategies in the chlorophytes Scenedesmus quadricauda, Chlamydomonas globosa, cryptophyte Cryptomonas ovata and ochrophyte Cyclotella meneghiniana. We observed interactive effects of light and phosphorus conditions on photosynthetic capacity in S. quadricauda and Cry. ovata. Cry. ovata can be characterized as a low light-acclimated species, whereas S. quadricauda and Cyc. meneghiniana can cope best with a combination of high light intensities and low phosphorus supply. Principal component analyses (PCA), including fatty acid composition, showed further species-specific patterns in their regulation of P-max with PUFAs and light. In S. quadricauda and Cyc. meneghiniana, PUFAs negatively affected the relationship between P-max and light. In Chl. globosa, lower light coincided with higher PUFAs and lower P-max, but PCA also indicated that PUFAs had no direct influence on P-max. PUFAs and P-max were unaffected by light in Cry. ovata. We did not observe a general trend in the four species tested and concluded that, in particular, the interactive effects highlight the importance of taking into account more than one environmental factor when assessing photosynthetic acclimation to lower irradiation.
The underlying mechanisms and consequences of competition and diversity are central themes in ecology. A higher diversity of primary producers often results in higher resource use efficiency in aquatic and terrestrial ecosystems. This may result in more food for consumers on one hand, while, on the other hand, it can also result in a decreased food quality for consumers; higher biomass combined with the same availability of the limiting compound directly reduces the dietary proportion of the limiting compound. Here we tested whether and how interspecific competition in phytoplankton communities leads to changes in resource use efficiency and cellular concentrations of nutrients and fatty acids. The measured particulate carbon : phosphorus ratios (C:P) and fatty acid concentrations in the communities were compared to the theoretically expected ratios and concentrations of measurements on simultaneously running monocultures. With interspecific competition, phytoplankton communities had higher concentrations of the monounsaturated fatty acid oleic acid and also much higher concentrations of the ecologically and physiologically relevant long-chain polyunsaturated fatty acid eicosapentaenoic acid than expected concentrations based on monocultures. Such higher availability of essential fatty acids may contribute to the positive relationship between phytoplankton diversity and zooplankton growth, and may compensate limitations by mineral nutrients in higher trophic levels.