Occurrence of mixotrophic flagellates in relation to bacterioplankton production, light regime and availability of inorganic nutrients in unproductive lakes with differing humic contents

1. Field data from five unproductive Swedish lakes were used to investigate the occurrence of mixotrophic flagellates in relation to bacterioplankton, autotrophic phytoplankton, heterotrophic flagellates and abiotic environmental factors. Three different sources of data were used: (i) a 3‐year study (1995–97) of the humic Lake Örträsket, (ii) seasonal measurements from five lakes with widely varying dissolved organic carbon (DOC) concentrations, and (iii) whole lake enrichment experiments with inorganic nutrients and organic carbon. 2. Mixotrophic flagellates usually dominated over autotrophic phytoplankton in Lake Örträsket in early summer, when both bacterial production and light levels were high. Comparative data from the five lakes demonstrated that the ratio between the biomasses of mixotrophic flagellates and autotrophic phytoplankton (the M/A‐ratio) was positively correlated to bacterioplankton production, but not to the light regime. Whole lake carbon addition (white sugar) increased bacterial biomass, and production, reduced the biomass of autotrophs by a factor of 16, and increased the M/A‐ratio from 0.03 to 3.4. Collectively, the results indicate that the dominance of mixotrophs among phytoplankton was positively related to bacterioplankton production. 3. Whole lake fertilisation with nitrogen (N) and phosphorus (P) demonstrated that the obligate autotrophic phytoplankton was limited by N. N‐addition increased the biomass of the autotrophic phytoplankton but had no effect on mixotrophic flagellates or bacteria, and the M/A‐ratio decreased from 1.2 to 0.6 after N‐enrichment. Therefore, we suggest that bacteria under natural conditions, by utilising allochthonous DOC as an energy and carbon source, are able to outcompete autotrophs for available inorganic nutrients. Consequently, mixotrophic flagellates can become the dominant phytoplankters when phagotrophy permits them to use nutrients stored in bacterial biomass. 4. In Lake Örträsket, the biomass of mixotrophs was usually higher than the biomass of heterotrophs during the summer. This dominance could not be explained by higher grazing rates among the mixotrophs. Instead, ratios between mixotrophic and heterotrophic biomass (the M/H‐ratio) were positively related to light availability. Therefore, we suggest that photosynthesis can enable mixotrophic flagellates to outcompete heterotrophic flagellates.     

Establishment of Microbial Eukaryotic Enrichment Cultures from a Chemically Stratified Antarctic Lake and Assessment of Carbon Fixation Potential

Lake Bonney is one of numerous permanently ice-covered lakes located in the McMurdo Dry Valleys, Antarctica. The perennial ice cover maintains a chemically stratified water column and unlike other inland bodies of water, largely prevents external input of carbon and nutrients from streams. Biota are exposed to numerous environmental stresses, including year-round severe nutrient deficiency, low temperatures, extreme shade, hypersalinity, and 24-hour darkness during the winter ¹. These extreme environmental conditions limit the biota in Lake Bonney almost exclusively to microorganisms ².Single-celled microbial eukaryotes (called "protists") are important players in global biogeochemical cycling ³ and play important ecological roles in the cycling of carbon in the dry valley lakes, occupying both primary and tertiary roles in the aquatic food web. In the dry valley aquatic food web, protists that fix inorganic carbon (autotrophy) are the major producers of organic carbon for organotrophic organisms ^{4, 2}. Phagotrophic or heterotrophic protists capable of ingesting bacteria and smaller protists act as the top predators in the food web ⁵. Last, an unknown proportion of the protist population is capable of combined mixotrophic metabolism ^{6, 7}. Mixotrophy in protists involves the ability to combine photosynthetic capability with phagotrophic ingestion of prey microorganisms. This form of mixotrophy differs from mixotrophic metabolism in bacterial species, which generally involves uptake dissolved carbon molecules. There are currently very few protist isolates from permanently ice-capped polar lakes, and studies of protist diversity and ecology in this extreme environment have been limited ^{8, 4, 9, 10, 5}. A better understanding of protist metabolic versatility in the simple dry valley lake food web will aid in the development of models for the role of protists in the global carbon cycle.We employed an enrichment culture approach to isolate potentially phototrophic and mixotrophic protists from Lake Bonney. Sampling depths in the water column were chosen based on the location of primary production maxima and protist phylogenetic diversity ^{4, 11}, as well as variability in major abiotic factors affecting protist trophic modes: shallow sampling depths are limited for major nutrients, while deeper sampling depths are limited by light availability. In addition, lake water samples were supplemented with multiple types of growth media to promote the growth of a variety of phototrophic organisms.RubisCO catalyzes the rate limiting step in the Calvin Benson Bassham (CBB) cycle, the major pathway by which autotrophic organisms fix inorganic carbon and provide organic carbon for higher trophic levels in aquatic and terrestrial food webs ¹². In this study, we applied a radioisotope assay modified for filtered samples ¹³ to monitor maximum carboxylase activity as a proxy for carbon fixation potential and metabolic versatility in the Lake Bonney enrichment cultures.     

Growth engineering of Synechococcus elongatus PCC 7942 for mixotrophy under natural light conditions for improved feedstock production

Synechococcus elongatus PCC 7942 has been widely explored as cyanobacterial cell factory through genetic modifications for production of various value‐added compounds. However, successful industrial scale‐ups have not been reported for the system predominantly due to its obligate photoautotrophic metabolism and use of artificial light in photobioreactors. Hence, engineering the organism to perform mixotrophy under natural light could serve as an effective solution. Thus, we applied a genetically engineered strain of Synechococcus elongatus PCC 7942 expressing heterologous hexose transporter gene (galP) to perform mixotrophy under natural light in a temperature controlled environmental chamber (EC). We systematically studied the comparative performances of these transformants using autotrophy and mixotrophy, which showed 3.4 times increase in biomass productivity of mixotrophically grown transformants over autotrophs in EC. Chlorophyll a yield was found to have decreased in mixotrophic conditions, possibly indicating reduced dependency on light for energy metabolism. Although pigment yield decreases under mixotrophy, titer was found to have improved due to increased biomass productivity. Carotenoid analysis showed that zeaxanthin is the major carotenoid produced by the species which is essential for photoprotection. Our work thus demonstrates that mixotrophy under temperature controlled natural light can serve as the viable solution to improve biomass productivity of Synechococcus elongatus PCC 7942 and for commercial production of natural or engineered value added compounds from the system. © 2017 American Institute of Chemical Engineers Biotechnol. Prog., 33:1182–1192, 2017     

Light and dissolved phosphorus interactively affect microbial metabolism,stoichiometry and decomposition of leaf litter

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The role of C, N and P in dissolved and particulate organic matter as a nutrient source for phytoplankton growth, including toxic species

Phytoplankton have traditionally been regarded as strictly phototrophic, with a well defined position at the base of pelagic food webs. However, recently we have learned that the nutritional demands of a growing number of phytoplankton species can be met, at least partially, or under specific environmental conditions, through heterotrophy. Mixotrophy is the ability of an organism to be both phototrophic and heterotrophic, in the latter case utilizing either organic particles (phagotrophy) or dissolved organic substances (osmotrophy). This finding has direct implications for our view on algal survival strategies, particularly for harmful species, and energy- and nutrient flow in pelagic food webs. Mixotrophic species may outcompete strict autotrophs, e.g. in waters poor in inorganic nutrients or under low light. In the traditional view of the ‘microbial loop’ DOC is thought to be channeled from algal photosynthesis to bacteria and then up the food chain through heterotrophic flagellates, ciliates and mesozooplankton. Are mixotrophic phytoplankton that feed on bacteria also significantly contributing to this transport of photosynthetic carbon up the food chain? How can we estimate the fluxes of carbon and nutrients between different trophic levels in the plankton food web involving phagotrophic algae? These questions largely remain unanswered. In this review we treat evidence for both osmotrophy and phagotrophy in phytoplankton, especially toxic marine species, and some ecological implications of mixotrophy.     

Beaver activity increases aquatic subsidies to terrestrial consumers

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Interactive effects of N:P ratios and light on nitrogen‐fixer abundance

Nitrogen‐fixers can contribute significant amounts of nitrogen (N) and impact ecosystem functioning in diverse aquatic and terrestrial ecosystems. What determines N‐fixer abundance still remains poorly understood. Here we experimentally investigate major environmental controls on the abundance of N‐fixers: nitrogen to phosphorus (N:P) ratio and light. We grew a N‐fixer, cyanobacterium Anabaena flos‐aquae, in a multispecies community of freshwater phytoplankton in replicated factorial design treatments with two N:P ratios and two light levels. We show that low N:P ratios promote the dominance of the N‐fixer in the community, but only under high light. Under low light, N:P ratio did not have a significant effect on the abundance of the N‐fixer. N fixation occurred at low N:P only and increased with increasing light. In contrast, the density of non N‐fixing cyanobacteria did not depend on N:P ratios. Green algae dominated under high N:P and high light only, exhibiting the opposite pattern of dominance to N‐fixers. These results are consistent with patterns observed in nature and help explain the N‐fixer distribution along the environmental gradients of nutrients and light.     

Discrepancies between net particulate carbon production and 13C‐labelled bicarbonate uptake by Alexandrium catenella (Dinophyceae): grazing controls the balance between autotrophic and non autotrophic carbon acquisition1

Inorganic carbon uptake by Alexandrium catenella estimated from incorporation of ¹³C labelled bicarbonate (an estimate of carbon gain by autotrophy) was compared to increases in particulate carbon (PC) that integrate all processes leading to carbon gain by cells (autotrophy, heterotrophy, mixotrophy). During blooms of A. catenella in the field, the ¹³C tracer technique could account for only 47% (range 29%–59%) of the increase in PC in conventional 24 h incubations. From dilution experiments, the ratio of PC increases to bicarbonate uptake was related significantly and positively to the grazing rate, indicating that dissolved organic carbon contributes to growth as a direct function of grazing activity. In addition, as grazing rate increases, the contribution of dissolved inorganic carbon uptake to carbon‐based growth decreases in a linear way (from 56% to 33% of total C acquisition) and the contribution of non autotrophic processes increases (from 54% to 67%). Thus, grazing appears to closely control the balance between autotrophic and non autotrophic processes leading to carbon acquisition by natural populations of A. catenella.     

To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs

Homeostasis of element composition is one of the central concepts of ecological stoichiometry. In this context, homeostasis is the resistance to change of consumer body composition in response to the chemical composition of consumer's food. To simplify theoretical analysis, it has generally been assumed that autotrophs exhibit flexibility in their composition, while heterotrophs are confined to a constant (strictly homeostatic) body composition. Yet, recent studies suggest that heterotrophs are not universally strictly homeostatic. We examined the degree to which autotrophs and heterotrophs regulate stoichiometric homeostasis (P:C, N:C, N:P, or %P and %N). We conducted a quantitative review and meta‐analysis using 132 datasets extracted from 57 literature sources which examined the dependence of organismal stoichiometry on resource stoichiometry. Among individual datasets, there was a wide range of responses from strictly homeostatic to non‐homeostatic. Even within heterotrophic organisms, varying levels of homeostasis were observed. Comparing the degree of homeostasis between organisms based on large‐scale habitat types using meta‐analysis indicated some significant differences between groups. For example, aquatic macroinvertebrates were significantly more homeostatic in terms of P:C than terrestrial invertebrates. Our meta‐analysis also confirmed that, with regard to N:P, heterotrophs are significantly more homeostatic than autotrophs. Furthermore, our analysis indicated that the homeostasis parameter 1/H, despite being a potentially useful predictive metric, has to be utilized with caution since it oversimplifies some important aspects of the responses of organisms to elemental imbalances. This critical evaluation of stoichiometric homeostasis contributes to a better understanding of many food‐web interactions, which are commonly driven by elemental imbalances between consumers and their resources.     

Interactions between metazoans,autotrophs, mixotrophs and bacterioplankton in nutrient‐depleted high DOC environments: a long‐term experiment

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Disentangling the role of light and nutrient limitation on bacterivory by mixotrophic nanoflagellates

Many phytoplankton taxa function on multiple trophic levels by combining photosynthesis and ingestion of bacteria, termed mixotrophy. Despite the recognition of mixotrophy as a universal functional trait, we have yet to fully resolve how environmental conditions influence community grazing rates in situ. A microcosm study was used to assess bacterivory by mixotrophic nanoflagellates following nutrient enrichment and light attenuation in a temperate lake. We found contrasting results based on assessment of mixotroph abundance or bacterivory. Despite an interactive effect of nutrient enrichment and light attenuation on mixotroph abundance, significant differences within light treatments were observed only after enrichment with P or N + P. The greatest abundance of mixotrophs across treatments occurred under co-nutrient enrichment with full exposure to irradiance. However, bacterivory by mixotrophic nanoflagellates was greatest under shaded conditions after either N or P enrichment. We suggest that PAR availability dampened the stimulatory effect of nutrient limitation, and bacterivory supplemented a suboptimal photosynthetic environment. In a saturating light regime, the mixotrophic community was less driven to ingest bacteria because photosynthesis was able to satisfy energetic demands. These findings quantify community bacterivory in response to environmental drivers that may characterize future ecosystem conditions and highlight the importance of considering grazing rates in conjunction with abundance of mixotrophic protists.     

Mixotrophic trade‐off under warming and UVR in a marine and a freshwater alga

Mixotrophic protists combine phagotrophy and phototrophy within a single cell. Greater phagotrophic activity could reinforce the bypass of carbon (C) flux through the bacteria‐mixotroph link and thus lead to a more efficient transfer of C and other nutrients to the top of the trophic web. Determining how foreseeable changes in temperature and UVR affect mixotrophic trade‐offs in favor of one or the other nutritional strategy, along the mixotrophic gradient, is key to understanding the fate of carbon and mineral nutrients in the aquatic ecosystem. Our two main hypotheses were: (i) that increased warming and UVR will divert metabolism toward phagotrophy, and (ii) that the magnitude of this shift will vary according to the organism's position along the mixotrophic gradient. To test these hypotheses, we used two protists (Isochrysis galbana and Chromulina sp.) located in different positions on the mixotrophic gradient, subjecting them to the action of temperature and of UVR and their interaction. Our results showed that the joint action of these two factors increased the primary production:bacterivory ratio and stoichiometric values (N:P ratio) close to Redfield's ratio. Therefore, temperature and UVR shifted the metabolism of both organisms toward greater phototrophy regardless of the original position of the organism on the mixotrophic gradient. Weaker phagotrophic activity could cause a less efficient transfer of C to the top of trophic webs.     

How light and nutrients affect the relationship between autotrophic and heterotrophic biomass in a tropical black water periphyton community

This study examines how nutrients and light affect the relationship between autotrophic biomass and non-autotrophic periphyton organic matter in a tropical black water lake biofilm community. We hypothesized that there is no positive correlation between autotrophic and non-autotrophic organic matter in the periphytic community of a black water humic lake, where non-algal components of periphyton can rely on carbon sources external to the periphyton matrix and where nutrient availability is low. Second, we sought to test our hypothesis that non-autotrophic periphyton organic matter will benefit from nutrient enhancement in a lake where the availability of DOC is high. We performed a field experiment using in situ lake mesocosms to manipulate nutrient concentrations and light availability in a 2 × 2 factorial design. Control treatments (no nutrient added) and nutrient treatments (N + P) were compared in different light conditions: high light (near surface water) and low light (near bottom). No positive correlation was found between autotrophic biomass and non-autotrophic periphyton organic matter, but a negative correlation was observed in high nutrient and light conditions. The low C:P and N:P ratios revealed that the non-autotrophic organic matter mostly comprised a heterotrophic microbial biofilm. High levels of light and nutrients together caused significant changes in periphyton community properties. The non-autotrophic periphyton organic matter was negatively affected by nutrient addition, whereas autotrophic biomass was positively affected, especially in high light conditions. Our results strongly suggest that non-autotrophic periphyton organic matter in a humic lake is primarily comprised of a bacterial biofilm that directly competes for nutrients with autotrophs in the periphytic community. We also observed no effect of nutrient addition on periphyton growing in light-limited conditions. These results suggest that heterotrophic periphytic organisms might experience carbon limitation despite the high availability, but usually low quality, of dissolved carbon in the water column of humic lakes.     

Biophysical aspects of resource acquisition and competition in algal mixotrophs

Mixotrophic organisms combine autotrophic and heterotrophic nutrition and are abundant in both freshwater and marine environments. Recent observations indicate that mixotrophs constitute a large fraction of the biomass, bacterivory, and primary production in oligotrophic environments. While mixotrophy allows greater flexibility in terms of resource acquisition, any advantage must be traded off against an associated increase in metabolic costs, which appear to make mixotrophs uncompetitive relative to obligate autotrophs and heterotrophs. Using an idealized model of cell physiology and community competition, we identify one mechanism by which mixotrophs can effectively outcompete specialists for nutrient elements. At low resource concentrations, when the uptake of nutrients is limited by diffusion toward the cell, the investment in cell membrane transporters can be minimized. In this situation, mixotrophs can acquire limiting elements in both organic and inorganic forms, outcompeting their specialist competitors that can utilize only one of these forms. This advantage can be enough to offset as much as a twofold increase in additional metabolic costs incurred by mixotrophs. This mechanism is particularly relevant for the maintenance of mixotrophic populations and productivity in the highly oligotrophic subtropical oceans.     

Mixotrophy among Dinoflagellates1

Mixotrophy, used herein for the combination of phototrophy and phagotrophy, is widespread among dinoflagellates. It occurs among most, perhaps all, of the extant orders, including the Prorocentrales, Dinophysiales. Gymnodiniales, Noctilucales, Gonyaulacales, Peridiniales, Blastodiniales. Phytodiniales, and Dinamoebales. Many cases of mixotrophy among dinoflagellates are probably undocumented. Primarily photosynthetic dinoflagellates with their “own” plastids can often supplement their nutrition by preying on other cells. Some primarily phagotrophic species are photosynthetic due to the presence of kleptochloroplasts or algal endosymbionts. Some parasitic dinoflagellates have plastids and are probably mixotrophic. For most mixotrophic dinoflagellates, the relative importance of photosynthesis, uptake of dissolved inorganic nutrients, and feeding are unknown. However, it is apparent that mixotrophy has different functions in different physiological types of dinoflagellates. Data on the simultaneous regulation of photosynthesis, assimilation of dissolved inorganic and organic nutrients, and phagotophy by environmental parameters (irradiance. availablity of dissolved nutrients, availability of prey) and by life history events are needed in order to understand the diverse roles of mixotrophy in dinoflagellates.     

ISOLATION AND CHARACTERIZATION OF CHLORELLA SOROKINIANA GXNN01 (CHLOROPHYTA) WITH THE PROPERTIES OF HETEROTROPHIC AND MICROAEROBIC GROWTH1

Heterotrophic and anaerobic microalgae are of significance in both basic research and industrial application. A microalga strain was isolated from a wastewater treatment pond and identified as Chlorella sorokiniana Shihira et W. R. Krauss GXNN01 in terms of morphology, physiology, and phylogeny. The strain grows rapidly in heterotrophic or mixotrophic conditions with addition of various carbon sources, and even in anaerobic conditions. The maximum growth rate reached 0.28 d^?1 when using d,l ‐malate as the carbon source, and the protein content of the microalgae was 75.32% in cell dry weight. The strain was shown to be capable of (1) utilizing d,l ‐malate only with light, (2) inhibiting photosynthesis in mixotrophic growth, and (3) growing in anaerobic conditions with regular photosynthesis and producing oxygen internally. This study demonstrates the influence of oxygen (aerobic vs. anaerobic) and metabolic regime (autotrophy, mixotrophy, heterotrophy) on the physiological state of the cell.     

Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge

The ability of organisms to combine autotrophy and heterotrophy gives rise to one of the most successful nutritional strategies on Earth: mixotrophy. Sponges are integral members of shallow-water ecosystems and many host photosynthetic symbionts, but studies on mixotrophic sponges have focused primarily on species residing in high-light environments. Here, we quantify the contribution of photoautotrophy to the respiratory demand and total carbon diet of the sponge Chondrilla caribensis, which hosts symbiotic cyanobacteria and lives in low-light environments. Although the sponge is net heterotrophic at 20 m water depth, photosynthetically fixed carbon potentially provides up to 52% of the holobiont’s respiratory demand. When considering the total mixotrophic diet, photoautotrophy contributed an estimated 7% to total daily carbon uptake. Visualization of inorganic ¹³C- and ¹⁵N-incorporation using nanoscale secondary ion mass spectrometry (NanoSIMS) at the single-cell level confirmed that a portion of nutrients assimilated by the prokaryotic community was translocated to host cells. Photoautotrophy can thus provide an important supplemental source of carbon for sponges, even in low-light habitats. This trophic plasticity may represent a widespread strategy for net heterotrophic sponges hosting photosymbionts, enabling the host to buffer against periods of nutritional stress.Subject terms: Stable isotope analysis, Microbial ecology, Macroecology     

Small Players, Large Role: Microbial Influence on Biogeochemical Processes in Pelagic Aquatic Ecosystems

Although prokaryotes are small in size, they are a significant biomass component in aquatic planktonic ecosystems and play a major role in biogeochemical processes. A review of the recent literature shows that the relative importance of prokaryotes to material and energy fluxes is maximized in low-productivity (oligotrophic) ecosystems and decreases in high-productivity (eutrophic) ecosystems. We conclude that competition with eukaryotic autotrophs for dissolved nutrients and competition with phagotrophic heterotrophs and physical processes (sinking, photooxidation) for organic carbon (C) play important roles in determining the relative abundance and impact of prokaryotes in aquatic systems. Oligotrophic systems have low nutrient concentrations, with high proportions of dissolved nutrients in organic form, which favors prokaryotic heterotrophs over phytoplankton. Furthermore, a high proportion of the available organic C is dissolved rather than particulate, which favors prokaryotic heterotrophs over phagotrophic heterotrophs. In eutrophic systems, increased relative concentrations and loading of inorganic nutrients and increased relative concentrations of particulate organic C select for phytoplankton and phagotrophic heterotrophs over prokaryotic heterotrophs. Increased particle sinking fluxes and/or decreased excretion of organic carbon (EOC) may also decrease the relative importance of prokaryotic heterotrophs in eutrophic systems. In oligotrophic systems, interactions between autotrophs and heterotrophs are tightly coupled because the dominant heterotrophs are similar in size and growth rates, as well as having similar nutrient composition to the dominant autotrophs, small phytoplankton. In eutrophic systems, increased productivity passes through zooplankton that are larger and have slower growth rates than the autotrophs, leading to a greater potential for decoupled auto- and heterotrophic production and increased export production. Received 18 July 2000; Accepted 13 September 2001.     

From the light to the darkness: thriving at the light extremes in the oceans

Light-acclimation processes are central to allowing photosynthesis in aquatic ecosystems to span from high light conditions, that are 10-fold higher than the light levels required to saturate photosynthesis, to the deep sea with extremely low light levels. In dim light systems, nutrient levels are often high, and cells maximize the absorption of light by increasing the cellular pool of pigments. The upper limits of light absorption are constrained by the package effect, which ultimately restricts the benefit of the light absorption associated with an increase in cellular pigmentation, thus decreasing the cost/benefit ratio relative to the metabolic cost of manufacturing cellular light-harvesting pigments. At extremely low light levels in the deep sea, chloroplasts are sequestered in numerous organisms; however, these species are not obligate autotrophs and supplement a heterotrophic/mixotrophic existence with opportunistic autotrophy. While low light acclimation is based on maximizing light absorption, photosynthetic systems under high light, in addition to decreased light-harvesting cross sections, rely on energy-dissipation processes to avoid light-induced damage to the photosynthetic apparatus and other free radical susceptible cell structures. Dissipation of excess light energy represents the largest sink of the absorbed light in high light environments; however, these processes remain largely unstudied and are rarely quantified. Cells supplement their energy-dissipation processes through increasing the capacity to remove high-light-generated radicals and/or inducing vertical movement. Improved understanding of strategies remains central for the understanding of algal distributions in nature and has broad industrial implications.