Mixotrophy,a major mode of nutrition for harmful algal species in eutrophic waters

Historically most harmful algal species (HAS) have been thought to be strictly phototrophic. Mixotrophy, the use of phototrophy and heterotrophy in combination, has been emphasized as operative mainly in nutrient-poor habitats as a mechanism for augmenting nutrient supplies. Here we examine an alternate premise, that many harmful algae which thrive in eutrophic habitats are mixotrophs that respond both directly to nutrient inputs, and indirectly through high abundance of bacterial and algal prey that are stimulated by the elevated nutrients. From review and synthesis of the available data, mixotrophy occurs in all HAS examined thus far in the organic substrate- and prey-rich habitats of eutrophic estuarine and marine coastal waters. Where data are available comparing phototrophy versus mixotrophy, mixotrophy in eutrophic habitats generally is significant in nutrient acquisition and growth of HAS and, therefore, likely important in the development and maintenance of their blooms. In eutrophic habitats phagotrophic mixotrophs, in particular, have been shown to attain higher growth than when in phototrophic mode. Yet for many HAS, quantitative data about the role of mixotrophy in nutrition, growth, and blooms are lacking, especially relating laboratory information to natural field assemblages, so that the relative importance of photosynthesis, dissolved organic nutrients, and ingestion of prey largely remain unknown. Research is needed to assess simultaneously the roles of phototrophy, osmotrophy and phagotrophy in the nutritional ecology of HAS in eutrophic habitats, spanning bloom initiation, development and senescence. From these data, models that include the role of mixotrophy can be developed to gain more realistic insights about the nutritional factors that control harmful algae in eutrophic waters, and to strengthen predictive capability in predicting their blooms. An overall forecast that can be tested, as well, is that harmful mixotrophic algae will become more abundant as their food supplies increase in many estuaries and coastal waters that are sustaining chronic, increasing cultural eutrophication.     

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.     

The mixotroph Ochromonas tuberculata may invade and suppress specialist phago- and phototroph plankton communities depending on nutrient conditions

Mixotrophic organisms combine light, mineral nutrients, and prey as supplementary resources. Based on theoretical assumptions and field observations, we tested experimentally the hypothesis that mixotrophs may invade established plankton communities depending on the trophic status of the system, and investigated possible effects on food web structure, species diversity, and nutrient dynamics. To test our hypothesis, we inoculated the mixotrophic nanoflagellate Ochromonas tuberculata into established planktonic food webs, consisting of specialist phototrophs, specialist phagotrophs, and bacteria at different supplies of soluble inorganic nutrients and dissolved organic carbon. Oligotrophic systems facilitated the invasion of O. tuberculata in two different ways. First, the combination of photosynthesis and phagotrophy gave mixotrophs a competitive advantage over specialist phototrophs and specialist phagotrophs. Second, low nutrient supplies supported the growth of small plankton organisms that fell into the food size spectrum of mixotrophs. Conversely, high nutrient supplies prevented O. tuberculata from successfully invading the food webs. Two important conclusions were derived from our experiments. First, in contrast to a paradigm of ecology, specialization may not necessarily be the most successful strategy for survival under stable conditions. Indeed, the use of several resources with lower efficiency can be an equally, or even more, successful strategy in nature. Second, when limiting nutrients promote the growth of bacterio- and picophytoplankton, invading mixotrophs may have a habitat-ameliorating effect for higher trophic levels, gauged in terms of food quantity and quality. Using given resources more efficiently, O. tuberculata generated higher biomasses and expressed an increased nutritional value for potential planktivores, due to decreased cellular carbon to phosphorus (C:P) ratios compared to specialized plankton taxa. Our findings may help to explain why energy transfer efficiency between phytoplankton and higher trophic levels is generally higher in oligotrophic systems than in nutrient rich environments.     

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.     

MIXOTROPHIC ALGAE CONSTRAIN THE LOSS OF ORGANIC CARBON BY EXUDATION1

Algae of various taxonomic groups are capable of assimilating dissolved organic carbon (DOC) from their environments (mixotrophy). Recently, we reported that, with increasing biomass of mixotrophs, heterotrophic bacteria did not increase. We hypothesized that algal uptake of external DOC may outweigh their release of DOC by exudation (H1). Here, we addressed an alternative hypothesis that algae did not assimilate external DOC but constrained the release of DOC (H2). In chemostat experiments, we cultured the mixotrophic Chlamydomonas acidophila Negoro together with heterotrophic bacteria. As external substrates, we used glucose, which was potentially available for both bacteria and algae, or fructose, which was available only for bacteria. We increased the biomass of algae by the stepwise addition of phosphorus. Bacterial biomass did not increase in experiments using glucose or when fructose was offered, suggesting that mechanisms other than algal mixotrophy (H1) kept concentrations of bacteria low. Measured exudation rates (percent extracellular release, PER) of mixotrophic algae (Cd. acidophila, Chlorella protothecoides W. Krüger) were very low and ranged between 1.0% and 3.5% at low and moderately high phosphorus concentrations. In contrast, an obligately phototrophic alga (Chlamydomonas segnis H. Ettl) showed higher exudation rates, particularly under phosphorus limitation (70%). The results support H2. If mixotrophy is considered as a mechanism to recycle organic exudates from near the cell surface, this would explain why algae retained mixotrophic capabilities although they cannot compete with bacteria for external organic carbon.     

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

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Bacterial grazing by phagotrophic phytoflagellates in a deep humic lake in northern Sweden

Bacterial grazing was measured from June to August 1995 in Lake Ortrasket, a deep brown-water lake in northern Sweden. Mixotrophic chrysophytes were the dominating bacterivores at all times, grazing 3-14% of bacterial standing stock daily. The effects of altered nutrient supply and light availability on grazing activity and growth were studied in two mesocosm experiments. Incubation in the dark did not stimulate phagotrophy, which would otherwise be expected if bacteria were mainly being used as an energy source. Furthermore, clearance rates were not reduced after alleviation of nutrient limitation conditions. Rather, phagotrophy may work as a relatively fixed attribute of the mixotrophic community in this lake. When availability of dissolved nutrients is restricted, phagotrophy permits the mixotrophs to outcompete other phytoplankton, but they become less competitive at high nutrient concentrations. The relative share of mixotrophs in relation to total phytoplankton decreased considerably after enrichment with nitrogen + phosphorus.      

Environment-dependent metabolic investments in the mixotrophic chrysophyte Ochromonas

Mixotrophic protists combine photosynthesis and phagotrophy to obtain energy and nutrients. Because mixotrophs can act as either primary producers or consumers, they have a complex role in marine food webs and biogeochemical cycles. Many mixotrophs are also phenotypically plastic and can adjust their metabolic investments in response to resource availability. Thus, a single species's ecological role may vary with environmental conditions. Here, we quantified how light and food availability impacted the growth rates, energy acquisition rates, and metabolic investment strategies of eight strains of the mixotrophic chrysophyte, Ochromonas. All eight Ochromonas strains photoacclimated by decreasing chlorophyll content as light intensity increased. Some strains were obligate phototrophs that required light for growth, while other strains showed stronger metabolic responses to prey availability. When prey availability was high, all eight strains exhibited accelerated growth rates and decreased their investments in both photosynthesis and phagotrophy. Photosynthesis and phagotrophy generally produced additive benefits: In low-prey environments, Ochromonas growth rates increased to maximum, light-saturated rates with increasing light but increased further with the addition of abundant bacterial prey. The additive benefits observed between photosynthesis and phagotrophy in Ochromonas suggest that the two metabolic modes provide nonsubstitutable resources, which may explain why a tradeoff between phagotrophic and phototrophic investments emerged in some but not all strains.     

Mixotrophy everywhere on land and in water: the grand écart hypothesis

There is increasing awareness that many terrestrial and aquatic organisms are not strictly heterotrophic or autotrophic but rather mixotrophic. Mixotrophy is an intermediate nutritional strategy, merging autotrophy and heterotrophy to acquire organic carbon and/or other elements, mainly N, P or Fe. We show that both terrestrial and aquatic mixotrophs fall into three categories, namely necrotrophic (where autotrophs prey on other organisms), biotrophic (where heterotrophs gain autotrophy by symbiosis) and absorbotrophic (where autotrophs take up environmental organic molecules). Here we discuss their physiological and ecological relevance since mixotrophy is found in virtually every ecosystem and occurs across the whole eukaryotic phylogeny, suggesting an evolutionary pressure towards mixotrophy. Ecosystem dynamics tend to separate light from non‐carbon nutrients (N and P resources): the biological pump and water stratification in aquatic ecosystems deplete non‐carbon nutrients from the photic zone, while terrestrial plant successions create a canopy layer with light but devoid of non‐carbon soil nutrients. In both aquatic and terrestrial environments organisms face a grand écart (dancer's splits, i.e., the need to reconcile two opposing needs) between optimal conditions for photosynthesis vs. gain of non‐carbon elements. We suggest that mixotrophy allows adaptation of organisms to such ubiquist environmental gradients, ultimately explaining why mixotrophic strategies are widespread.     

A classification of mixotrophic protists based on their behaviour

1. Mixotrophs are organisms which combine phototrophy and heterotrophy; such nutritional behaviour is widespread among protists. This ability to combine multiple modes of nutrition varies between species and is not related to their taxonomic grouping. A classification of mixotrophic protists, based on their behaviour, is proposed, dividing them into four groups.
2. Group A includes protists whose primary mode of nutrition is heterotrophy and where phototrophy is employed only when prey concentrations limit heterotrophic growth. In groups B, C and D phototrophy is the dominant mode of nutrition. In group B phagotrophy supplements growth when light is limiting, therefore ingestion of prey is inversely proportional to light intensity; in group C phagotrophy provides essential substances for growth and ingestion is proportional to light intensity; and group D includes those who have very low ingestion rates, ingesting prey only, for example, for cell maintenance during prolonged dark periods.
3. This classification is aimed towards predicting the impact of any particular mixotrophic protist on the aquatic food web, and how this impact may vary depending on the environmental conditions. A model representation of the four groups is discussed.     

Purple Sulfur Bacteria Control the Growth of Aerobic Heterotrophic Bacterioplankton in a Meromictic Salt Lake

In meromictic Mahoney Lake, British Columbia, Canada, the heterotrophic bacterial production in the mixolimnion exceeded concomitant primary production by a factor of 7. Bacterial growth rates were correlated neither to primary production nor to the amount of chlorophyll a. Both results indicate an uncoupling of bacteria and phytoplankton. In the chemocline of the lake, an extremely dense population of the purple sulfur bacterium Amoebobacter purpureus is present year round. We investigated whether anoxygenic phototrophs are significant for the growth of aerobic bacterioplankton in the overlaying water. Bacterial growth rates in the mixolimnion were limited by inorganic phosphorus or nitrogen most of the time, and the biomass of heterotrophic bacteria did not increase until, in autumn, 86% of the cells of A. purpureus appeared in the mixolimnion because of their reduced buoyant density. The increase in heterotrophic bacterial biomass, soluble phosphorus concentrations below the detection limit, and an extraordinarily high activity of alkaline phosphatase in the mixolimnion indicate a rapid liberation of organically bound phosphorus from A. purpureus cells accompanied by a simultaneous incorporation into heterotrophic bacterioplankton. High concentrations of allochthonously derived dissolved organic carbon (mean, 60 mg of C(middot)liter(sup-1)) were measured in the lake water. In Mahoney Lake, liberation of phosphorus from upwelling purple sulfur bacteria and degradation of allochthonous dissolved organic carbon as an additional carbon source render heterotrophic bacterial production largely independent of the photosynthesis of phytoplankton. A recycling of inorganic nutrients via phototrophic bacteria also appears to be relevant in other lakes with anoxic bottom waters.     

A classification of mixotrophic protists based on their behaviour

1. Mixotrophs are organisms which combine phototrophy and heterotrophy; such nutritional behaviour is widespread among protists. This ability to combine multiple modes of nutrition varies between species and is not related to their taxonomic grouping. A classification of mixotrophic protists, based on their behaviour, is proposed, dividing them into four groups.
2. Group A includes protists whose primary mode of nutrition is heterotrophy and where phototrophy is employed only when prey concentrations limit heterotrophic growth. In groups B, C and D phototrophy is the dominant mode of nutrition. In group B phagotrophy supplements growth when light is limiting, therefore ingestion of prey is inversely proportional to light intensity; in group C phagotrophy provides essential substances for growth and ingestion is proportional to light intensity; and group D includes those who have very low ingestion rates, ingesting prey only, for example, for cell maintenance during prolonged dark periods.
3. This classification is aimed towards predicting the impact of any particular mixotrophic protist on the aquatic food web, and how this impact may vary depending on the environmental conditions. A model representation of the four groups is discussed.     

Relationship between photosynthetic activity and assimilation of organic matter in marine plankton mixotrophic algae--the possibility of different metabolic strategies

The relationship between photosynthetic and heterotrophic activities of plankton mixotrophic algae is characterized by the type of metabolic strategy. Algae with a primary photoautotrophic strategy grow at the expense of photosynthesis without uptake of organic substrates when inorganic and organic nutrients are available. They assimilate only organic substrates when inorganic nutrients are in shortage, while heterotrophic activity supports photosynthesis under conditions of inorganic nutrients deficiency. Algae with a primary heterotrophic strategy grow heterotrophicaly under repletion of inorganic and organic nutrients. Photosynthesis occurs only when organic substrates are depleted. The most mixotrophic algae combine the features of a primary photoautotrophic and a primary heterotrophic strategies. The varieties of metabolic types of mixotrophic algae form a continuum with a primary photoautotrophic strategy on the one end and a primary heterotrophic strategy on the other. The natural conditions allowing mixotrophic algae to use one or other metabolic strategy are determined by the dynamic of inorganic and organic nutrients.     

Nutrient Acquisition and Population Growth of a Mixotrophic Alga in Axenic and Bacterized Cultures

Axenic growth of a mixotrophic alga, Ochromonas sp., was compared in several inorganic and organic media, and in the presence of live bacteria under nutrient-replete and low-nutrient conditions. Axenic growth in the light was negligible in inorganic media with or without the addition of glucose. Addition of vitamins increased growth rate, but average cell size declined, resulting in no net increase in biomass. Supplementing axenic cultures with a more complex organic substrate resulted in moderate growth and higher maximal abundance (and biomass) than in the inorganic media with added vitamins. The absence of light did not greatly affect population growth rate in the presence of complex dissolved organic compounds, although cell size was significantly greater in the light than in the dark. The highest growth rates for the alga (up to 2.6 d-1) were measured in treatments containing live bacteria. Increases in cell number of Ochromonas sp. in the presence of bacterial prey were similar in the light and dark, although chloroplast and cell sizes differed. Bacterial abundance was reduced and dissolved phosphorus and ammonia were rapidly released in bacterized cultures in the light and dark, indicating high rates of bacterial ingestion and suggesting an inability of the alga to store or utilize N and P in excess of the quantities required for heterotrophic growth. Low-nutrient conditions in the presence of bacteria were promoted by adding glucose to stimulate bacterial growth and the uptake of N and P released by algal phagotrophy. Subsequent decreases in dissolved N and P following the addition of glucose corresponded to a second period of rapid growth of the alga in both light and dark. This result, combined with evidence for slow axenic growth of this strain, indicated that nutrient acquisition for this species in the presence of bacteria was accomplished primarily via ingestion of bacteria.     

The role of mixotrophic protists in the population dynamics of the microbial food web in a small artificial pond

• 1 The seasonal variations of protist and rotifer populations were monitored over 1 year in a small artificial pond. Grazing rates on fluorescently labelled bacteria were also determined.
• 2 The data showed population dynamics similar to other small freshwater bodies; diatoms were numerous during the spring, chlorophytes dominated during the summer months, and mixotrophs, in particular Gymnodinium, dominated during the autumn and winter.
• 3 The mixotrophic dinoflagellates were responsible for a high chlorophyll concentration during the autumn and winter. Mixotrophs were important consumers of bacteria, particularly during the autumn when population densities of pure heterotrophs were low. Mixotrophs were an important component of the microbial food web in this pond.

     

Mixotrophic organisms become more heterotrophic with rising temperature

The metabolic theory of ecology predicts that temperature affects heterotrophic processes more strongly than autotrophic processes. We hypothesized that this differential temperature response may shift mixotrophic organisms towards more heterotrophic nutrition with rising temperature. The hypothesis was tested in experiments with the mixotrophic chrysophyte Ochromonas sp., grown under autotrophic, mixotrophic and heterotrophic conditions. Our results show that (1) grazing rates on bacterial prey increased more strongly with temperature than photosynthetic electron transport rates, (2) heterotrophic growth rates increased exponentially with temperature over the entire range from 13 to 33 °C, while autotrophic growth rates reached a maximum at intermediate temperatures and (3) chlorophyll contents during mixotrophic growth decreased at high temperature. Hence, the contribution of photosynthesis to mixotrophic growth strongly decreased with temperature. These findings support the hypothesis that mixotrophs become more heterotrophic with rising temperature, which alters their functional role in food webs and the carbon cycle.     

Mixotrophy of a photosynthetic flagellate viewed from an optimal foraging perspective

Mixotrophy, a combination of phototrophic and phagotrophic nutrition, has been found in several classes of phytoplankton (Booras et al. 1988, Jones 2000) and appears to be a successful evolutionary strategy. Heterotrophic nutrition of phytoplankton has been suggested to be an important source of mineral nutrients (Nygaard and Tobiesen 1993). Potentially limiting mineral nutrients, particularly phosphorus (P), are often several orders of magnitude more concentrated in the biomass of food organisms of mixotrophs (e.g. in bacteria) than in the dissolved phase (Vadstein 2000). We used radioactive tracer experiments to show that the simultaneous uptake of P from dissolved inorganic and particular P sources by the marine phytoflagellate Chrysochromulina polylepis followed basic predictions of optimal foraging theory (Stephens and Krebs 1986). Chrysochromulina takes up its P rather unselectively from both bacterial P and dissolved P sources at low dissolved P concentrations, while it becomes more selective at higher dissolved inorganic P (DIP) concentrations. The onset of mixotrophic processes was dependent on DIP concentrations. These findings support the view of mixotrophy as a strategy of nutrient uptake in nutrient poor (oligotrophic) pelagic environments (Nygaard and Tobiesen 1993) and show that ideas of optimal foraging can be applied to unicellular organisms.     

Importance of mixotrophic bacterivory can be predicted by light and loss rates

Recent observational studies form oligotrophic waters provide ample evidence that mixotrophic flagellates often account for the bulk of bacterivory. However, we lack a general framework that allows a mechanistic understanding of success of mixotrophs in the competition with heterotrophic bacterivores. This is especially needed for integrating mixotrophy in models of the microbial loop. Based on general tradeoffs linked to the combined resource use in mixotrophs (generalist versus specialist), we propose a concept where mixotrophs are favored by conditions of high light – low losses, corresponding to the situation found in the surface waters of oligotrophic oceans. Under such conditions, they can achieve positive net growth at very low resource levels, allowing simultaneous competition with specialized protists. Conversely, heterotrophic bacterivores and photoautotrophs should be especially favored in more productive and low‐light conditions. We show experimentally that the combined effect of light and loss rates (dilution) predicts the success of mixotrophic bacterivorous flagellates. Moreover, our results suggest that total bacterivory, contrary as seen in the traditional microbial loop concept, has a more intricate coupling to light.     

When do mixotrophs specialize? Adaptive dynamics theory applied to a dynamic energy budget model

In evolutionary history, several events have occurred at which mixotrophs specialized into pure autotrophs and heterotrophs. We studied the conditions under which such events take place, using the Dynamic Energy Budget (DEB) theory for physiological rules of the organisms' metabolism and Adaptive Dynamics (AD) theory for evolutionary behavior of parameter values. We modeled a population of mixotrophs that can take up dissolved inorganic nutrients by autotrophic assimilation and detritus by heterotrophic assimilation. The organisms have a certain affinity for both pathways; mutations that occur in the affinities enable the population to evolve. One of the possible evolutionary outcomes is a branching point which provides an opportunity for the mixotrophic population to split up and specialize into separate autotrophs and heterotrophs. Evolutionary branching is not a common feature of the studied system, but is found to occur only under specific conditions. These conditions depend on intrinsic properties such as the cost function, the level of the costs and the boundaries of the trait space: only at intermediate cost levels and when an explicit advantage exists to pure strategies over mixed ones may evolutionary branching occur. Usually, such an advantage (and hence evolutionary branching) can be induced by interference between the two affinities, but this result changes due to the constraints on the affinities. Now, only some of the more complicated cost functions give rise to a branching point. In contrast to the intrinsic properties, extrinsic properties such as the total nutrient content or light intensity were found to have no effect on the evolutionary outcomes at all.     

Flagellate grazing on bacteria in a small dystrophic lake

Fluorescent beads were used to determine the grazing on bacteria by heterotrophic and mixotrophic flagellates in a highly humic (water colour 300–600 mg Pt l^–1) small lake. In summer phagotrophic flagellates constituted about three quarters of the numbers of phytoplankton (including heterotrophic or mixotrophic flagellates) in the uppermost epilimnion. Due to their small size their respective contribution to the biomass was about one quarter. The most important phagotrophic species were Ochromonas sp., and Chromulina spp. which ingested 75–203% of their body carbon per day from bacteria.In view of the abundance and biomass of phagotrophic and mixotrophic flagellates and their very high growth potential, they clearly play a significant role in the food chains of this lake. In addition to providing energy, bacteriovory also represents an important supply of inorganic and organic nutrients under nutrient limiting conditions.