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.     

Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans

Photosynthetic picoeukaryotes (PPE) are recognized as major primary producers and contributors to phytoplankton biomass in oceanic and coastal environments. Molecular surveys indicate a large phylogenetic diversity in the picoeukaryotes, with members of the Prymnesiophyceae and Chrysophyseae tending to be more common in open ocean waters and Prasinophyceae dominating coastal and Arctic waters. In addition to their role as primary producers, PPE have been identified in several studies as mixotrophic and major predators of prokaryotes. Mixotrophy, the combination of photosynthesis and phagotrophy in a single organism, is well established for most photosynthetic lineages. However, green algae, including prasinophytes, were widely considered as a purely photosynthetic group. The prasinophyte Micromonas is perhaps the most common picoeukaryote in coastal and Arctic waters and is one of the relatively few cultured representatives of the picoeukaryotes available for physiological investigations. In this study, we demonstrate phagotrophy by a strain of Micromonas (CCMP2099) isolated from Arctic waters and show that environmental factors (light and nutrient concentration) affect ingestion rates in this mixotroph. In addition, we show size-selective feeding with a preference for smaller particles, and determine P vs I (photosynthesis vs irradiance) responses in different nutrient conditions. If other strains have mixotrophic abilities similar to Micromonas CCMP2099, the widespread distribution and frequently high abundances of Micromonas suggest that these green algae may have significant impact on prokaryote populations in several oceanic regimes.     

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 Protists In Marine and Freshwater Ecosystems

ABSTRACT Some protists from both marine and freshwater environments function at more than one trophic level by combining photosynthesis and panicle ingestion. Photosynthetic algae from several taxa (most commonly chrysomonads and dinoflagellates) have been reported to ingest living prey or nonliving particles, presumably obtaining part of their carbon and/or nutrients from phagocytosis. Conversely, some ciliates and sarcodines sequester chloroplasts after ingestion of algal prey. Plastid retention or "chloroplast symbiosis" by protists was first demonstrated < 20 years ago in a benthic foraminiferan. Although chloroplasts do not divide within these mixotrophic protists, they continue to function photosynthetically and may contribute to nutrition. Sarcodines and ciliates that harbor endosymbiotic algae could be considered mixotrophic but are not covered in detail here. the role of mixotrophy in the growth of protists and the impact of their grazing on prey populations have received increasing attention. Mixotrophic protists vary in their photosynthetic and ingestion capabilities, and thus, in the relative contribution of photosynthesis and phagotrophy to their nutrition. Abundant in both marine and freshwaters, they are potentially important predators of algae and bacteria in some systems. Mixotrophy may make a stronger link between the microbial and classic planktonic food webs by increasing trophic efficiency.     

Mixotrophy in planktonic protists: an overview

1. An overview is provided of the role of mixotrophic protists in plankton communities. Consideration of the importance of phagotrophy in the evolution of photosynthetic eucaryotes suggests that mixotrophy as a nutritional strategy can arise rather readily.
2. Mixotrophic protists actually present a spectrum of nutritional strategies. However, recognition of distinct groups of mixotrophs based on nutritional behaviour facilitates consideration of their functional role and of competitive interactions with other types of planktonic protists.
3. Consideration of the costs and benefits of mixotrophy as a nutritional strategy allows the development of several empirical predictions about the probable outcome of resource competition between mixotrophs and obligate phototrophs or phagotrophs. Existing results from laboratory and field experiments allow some of these predictions to be evaluated.
4. These results indicate that, under specified conditions, mixotrophs should represent an important link in the flux of materials through planktonic food webs. However, quantifying these fluxes remains a challenge for the future.     

Reverse Evolution: Driving Forces Behind the Loss of Acquired Photosynthetic Traits

Background

The loss of photosynthesis has occurred often in eukaryotic evolution, even more than its acquisition, which occurred at least nine times independently and which generated the evolution of the supergroups Archaeplastida, Rhizaria, Chromalveolata and Excavata. This secondary loss of autotrophic capability is essential to explain the evolution of eukaryotes and the high diversity of protists, which has been severely underestimated until recently. However, the ecological and evolutionary scenarios behind this evolutionary “step back” are still largely unknown.

Methodology/Principal Findings

Using a dynamic model of heterotrophic and mixotrophic flagellates and two types of prey, large bacteria and ultramicrobacteria, we examine the influence of DOC concentration, mixotroph''s photosynthetic growth rate, and external limitations of photosynthesis on the coexistence of both types of flagellates. Our key premises are: large bacteria grow faster than small ones at high DOC concentrations, and vice versa; and heterotrophic flagellates are more efficient than the mixotrophs grazing small bacteria (both empirically supported). We show that differential efficiency in bacteria grazing, which strongly depends on cell size, is a key factor to explain the loss of photosynthesis in mixotrophs (which combine photosynthesis and bacterivory) leading to purely heterotrophic lineages. Further, we show in what conditions an heterotroph mutant can coexist, or even out-compete, its mixotrophic ancestor, suggesting that bacterivory and cell size reduction may have been major triggers for the diversification of eukaryotes.

Conclusions/Significance

Our results suggest that, provided the mixotroph''s photosynthetic advantage is not too large, the (small) heterotroph will also dominate in nutrient-poor environments and will readily invade a community of mixotrophs and bacteria, due to its higher efficiency exploiting the ultramicrobacteria. As carbon-limited conditions were presumably widespread throughout Earth history, such a scenario may explain the numerous transitions from phototrophy to mixotrophy and further to heterotrophy within virtually all major algal lineages. We challenge prevailing concepts that affiliated the evolution of phagotrophy with eutrophic or strongly light-limited environments only.     

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 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.     

Remote control of photosynthetic genes by the mitochondrial respiratory chain

In this paper, we study whether mitochondrial respiration has an impact on the biogenesis of photosynthetic apparatus in the unicellular alga, Chlamydomonas reinhardtii. When respiration was activated by acetate in the dark, mRNAs of nuclear-encoded photosynthetic genes were induced. This induction did not occur in the cells treated with respiration inhibitors or in respiration mutants. An uncoupler of oxidative phosphorylation did not inhibit this mRNA induction; rather, it enhanced it in response to the increase in respiratory electron transport (RET). Plant and algal mitochondria have two RET pathways: the cytochrome pathway and the alternative pathway. Inhibitors of the former pathway inhibited mRNA induction, but inhibitors of the latter enhanced it. Taken together, these indicate that photosynthetic gene mRNAs are induced in response to activation of the cytochrome pathway. This RET-responsive induction is analogous to the photosynthetic electron transport (PET)-responsive induction of photosynthetic gene mRNAs (Matsuo and Obokata, Plant Cell Physiol. 43, 1189). PET-responsive induction occurred in photo-autotrophic and mixotrophic conditions, while RET-responsive induction occurred in mixotrophic and dark heterotrophic conditions. These results indicate that the regulatory system of photosynthetic genes changes between chloroplastic PET-dependent type and mitochondrial RET-dependent type in response to shifts in the dominant energy source between photosynthesis and respiration.     

Costs, benefits and characteristics of mixotrophy in marine oligotrichs

1. Oligotrich ciliates are an important part of most marine plankton communities. Mixotrophic (chloroplast-sequestering) oligotrichs, a common component of marine oligotrich communities, obtain fixed carbon from both photosynthesis as well as the ingestion of particulate food. Mixotrophy, in general, is often considered an adaptation permitting exploitation of food-poor environments. We examined the hypothesis that, among oligotrichs, mixotrophs may be at a disadvantage relative to heterotrophs in food-rich conditions in a nutrient-enrichment experiment. We compared growth responses of mixotrophic and heterotrophic oligotrichs in natural communities from the N.W. Mediterranean Sea in microcosms with daily nutrient additions resulting in increases in nanoflagellates and Synechococcus populations. The results indicated that both mixotrophic and heterotrophic oligotrichs respond to prey increases with rapid growth (μ=1.2 d−1).
2. To examine the hypothesis that the proportion of mixotrophic to heterotrophic oligotrichs changes with the trophic status of a system, increasing with oligotrophy, we examined data from a variety of marine systems. Across systems ranging in chlorophyll concentration from about 0.1 to 40 μg L−1, oligotrich cell concentrations are correlated with chlorophyll concentrations, and mixotrophs are a consistent component of oligotrich communities, averaging about 30% of oligotrich cell numbers.
3. We discuss the costs, benefits and possible uses of mixotrophy in marine oligotrichs and suggest that mixotrophy in marine oligotrichs is not closely linked to the exploitation of food-poor environments, but probably serves a variety of purposes.     

Successful strategies in size structured mixotrophic food webs

This study investigates how food web structures in aquatic microbial communities emerge based on different mixotrophic life strategies. Unicellular mixotrophic organisms that combine osmotrophy and primary production with phagotrophy account for significant amounts of primary production and bacterivory in marine environments, yet mixotrophs are still usually absent in large-scale biogeochemical models. We here present for the first time a thorough analysis of a food web model with a finely resolved structure in both cell size and foraging mode, where foraging mode is a strategy ranging from pure osmotrophy to pure phagotrophy. A trade-off for maximum uptake rates of mixotrophs is incorporated. We study how different factors determine the food web structure, here represented by the topology of the distribution of given amounts of total phosphorous over the cell size-foraging mode plane. We find that mixotrophs successfully coexist with foraging specialists (pure osmo- and phagotrophs) for a wide range of conditions, a result consistent with the observed prevalence of mixotrophs in recent oceanographic surveys. Mixotrophy trade-off and size-dependent parameters have a strong effect on the emerging community structure, stressing the importance of foraging mode and size considerations when working with microbial diversity and food web dynamics. The proposed model may be used to develop timely representations of mixotrophic strategies in larger biogeochemical ocean models.     

Coexistence of mixotrophs, autotrophs, and heterotrophs in planktonic microbial communities

We examine what circumstances allow the coexistence of microorganisms following different nutritional strategies, using a mathematical model. This model incorporates four nutritional types commonly found in planktonic ecosystems: (1) heterotrophic bacteria that consume dissolved organic matter and are prey to some of the other organisms; (2) heterotrophic zooflagellates that depend entirely on bacterial prey; (3) phototrophic algae that depend only on light and inorganic nutrients, and (4) mixotrophs that photosynthesize, take up inorganic nutrients, and consume bacterial prey. Mixotrophs are characterized by a parameter representing proportional mixing of phototrophic and heterotrophic nutritional strategies. Varying this parameter, a range of mixotrophic strategies was examined in hypothetical habitats differing in supplies of light, dissolved organic carbon, and dissolved inorganic phosphorous. Mixotrophs expressing a wide range of mixotrophic strategies persisted in model habitats with low phosphorus supply, but only those with a strategy that is mostly autotrophic persisted with high nutrient supply, and then only when light supply was also high. Organisms representing all four nutritional strategies were predicted to coexist in habitats with high phosphorus and light supplies. Coexistence involves predation by zooflagellates and mixotrophs balancing the high competitive ability of bacteria for phosphorus, the partitioning of partially overlapping resources between all populations, and possibly nonequlibrium dynamics. In most habitats, the strategy predicted to maximize the abundance of mixotrophs is to be mostly photosynthetic and supplement nutritional needs by consuming bacteria.     

Alternative nutritional strategies in protists: symposium introduction and a review of freshwater protists that combine photosynthesis and heterotrophy

The alternative nutritional strategies in protists that were addressed during the symposium by that name at the 2010 annual meeting of the International Society of Protistologists and here in contributed papers, include a range of mechanisms that combine photosynthesis with heterotrophy in a single organism. Often called mixotrophy, these multiple trophic level combinations occur across a broad range of organisms and environments. Consequently, there is great variability in the physiological abilities and relative importance of phototrophy vs. phagotrophy and/or osmotrophy in mixotrophic protists. Recently, research papers addressing ecological questions about mixotrophy in marine systems have been more numerous than those that deal with freshwater systems, a trend that is probably partly due to a realization that many harmful algal blooms in coastal marine systems involve mixotrophic protists. After an introduction to the symposium presentations, recent studies of mixotrophy in freshwater systems are reviewed to encourage continuing research on their importance to inland waters.     

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.     

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.     

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.     

FATTY ACIDS IN PHOTOTROPHIC AND MIXOTROPHIC GYRODINIUM GALATHE‐ANUM (DINOPHYCEAE)

Fatty acids were measured in G. galatheanum grown either phototrophically, or mixotrophically with Storeatula major (Cryptophyceae) as prey. G. galatheanum, like many photosynthetic dinoflagellates, contains high amounts of n‐3 long‐chain‐polyunsaturated fatty acids (LC‐PUFA) such as docosahexaenoic acid (DHA, 22:6n‐3) and the hemolytic toxic fatty acid 18:5n‐3. We hypothesize that a benefit of phagotrophy in G. galatheanum is the acquisition of precursor linolenic acid (18:3n‐3) that fuels LC‐PUFA synthesis. Phototrophs grew at 0.37 d^?1, while mixotrophs grew at 0.40 d^?1 with a feeding rate of 0.62 d^?1. Photosynthesis was lower in mixotrophs (3.7 pg C cell^?1 h^?1) than phototrophs (4.9 pg C cell^?1 h^?1). DHA levels were higher in mixotrophs [3.7 (+/? 0.11) pg cell^?1] than phototrophs [3.0 (+/? 0.16) pg cell^?1] and prey [0.4 (+/? 0.01) pg cell^?1]. 18:5n–3 levels [1.7 (+/? 0.03) pg cell^?1] were similar in phototrophs and mixotrophs. An intermediate in n‐3 LC‐PUFA synthesis, 20:4n‐3, accumulated in mixotrophs [0.6 (+/? 0.27) pg cell^?1] relative to phototrophs (not detected) and prey [0.03 (+/? 0.002) pg cell^?1]. Low ratios of linolenic acid to DHA in phototrophic G. galatheanum (0.14) relative to mixotrophic G. galatheanum (0.29) and prey (2.14) are consistent with substrate limitation of LC‐PUFA synthesis in phototrophs. Accumulation of 20:4n‐3 suggests incomplete conversion of linolenic acid to DHA, possibly due to conditions in batch culture. We conclude that precursors for n‐3 LC‐PUFA biosynthesis in G. galatheanum may be acquired through ingestion of S. major, and may partially control feeding/photosynthesis in mixotrophic populations.     

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.     

Nutrient limitation of autotrophic and mixotrophic phytoplankton in a temperate and tropical humic lake gradient

Nutrient enrichment experiments were carried out in three tropical(once) and three temperate (twice) lakes differing in humiccontent in order to examine whether there was a relationshipbetween the limiting nutrient for algal growth [nitrogen (N)or phosphorus (P)] and humic content, and whether the prevailinglimitation was connected to the relative abundance of autotrophicand phagotrophic phytoplankton (mixotrophs). In both climaticregions, there was a stronger tendency for total phytoplanktonbiomass accumulation to be N limited in lakes with a high humiccontent. However, in contrast to what we expected, there wasno tendency for the mixotrophs to be more favored by the additionof N than of P. In the temperate lakes, the relative abundanceof mixotrophs increased in the treatments receiving N or P separatelyor no nutrients (control) when exposed to a high light availability.In the following year, when the light availability was low,the mixotrophs increased relative to the obligate autotrophsin all treatments, irrespective of nutrient addition. Possibly,this was a result of their ability to supplement photosynthesiswith the ingestion of prey. The results indicate that mixotrophyis an advantageous strategy when the availability of light and/ornutrients is low.     

Acquired phototrophy stabilises coexistence and shapes intrinsic dynamics of an intraguild predator and its prey

In marine ecosystems, acquired phototrophs – organisms that obtain their photosynthetic ability by hosting endosymbionts or stealing plastids from their prey – are omnipresent. Such taxa function as intraguild predators yet depend on their prey to periodically obtain chloroplasts. We present a new theory for the effects of acquired phototrophy on community dynamics by analysing a mathematical model of this predator–prey interaction and experimentally verifying its predictions with a laboratory model system. We show that acquired phototrophy stabilises coexistence, but that the nature of this coexistence exhibits a ‘paradox of enrichment’: as light increases, the coexistence between the acquired phototroph and its prey transitions from a stable equilibrium to boom‐bust cycles whose amplitude increases with light availability. In contrast, heterotrophs and mixotrophic acquired phototrophs (that obtain  < 30% of their carbon from photosynthesis) do not exhibit such cycles. This prediction matches field observations, in which only strict ( > 95% of carbon from photosynthesis) acquired phototrophs form blooms.