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.     

MIXOTROPHY AND NITROGEN UPTAKE BY PFIESTERIA PISCICIDA (DINOPHYCEAE)

The nutritional versatility of dinoflagellates is a complicating factor in identifying potential links between nutrient enrichment and the proliferation of harmful algal blooms. For example, although dinoflagellates associated with harmful algal blooms (e.g. red tides) are generally considered to be phototrophic and use inorganic nutrients such as nitrate or phosphate, many of these species also have pronounced heterotrophic capabilities either as osmotrophs or phagotrophs. Recently, the widespread occurrence of the heterotrophic toxic dinoflagellate, Pfiesteria piscicida Steidinger et Burkholder, has been documented in turbid estuarine waters. Pfiesteria piscicida has a relatively proficient grazing ability, but also has an ability to function as a phototroph by acquiring chloroplasts from algal prey, a process termed kleptoplastidy. We tested the ability of kleptoplastidic P. piscicida to take up ¹⁵N-labeled NH     , NO     , urea, or glutamate. The photosynthetic activity of these cultures was verified, in part, by use of the fluorochrome, primulin, which indicated a positive relationship between photosynthetic starch production and growth irradiance. All four N substrates were taken up by P. piscicida , and the highest uptake rates were in the range cited for phytoplankton and were similar to N uptake estimates for phagotrophic P. piscicida . The demonstration of direct nutrient acquisition by kleptoplastidic P. piscicida suggests that the response of the dinoflagellate to nutrient enrichment is complex, and that the specific pathway of nutrient stimulation (e.g. indirect stimulation through enhancement of phytoplankton prey abundance vs. direct stimulation by saprotrophic nutrient uptake) may depend on P. piscicida 's nutritional state (phagotrophy vs. phototrophy).     

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.     

Mixotrophy in ciliates

Mixotrophy is the occurrence of phagotrophy and phototrophy in the same organism. In ciliates the intracellular phototroph can be unicellular green algae (zoochlorellae), dinoflagellates (zooxanthellae), cryptomonads or sequestered chloroplasts from ingested algae. An intermediate mixotrophic mechanism is that where the phagotroph ingests algal cells, maintains them intact and functional in the cytoplasm for some time, but the algae are afterwards digested. This seems to occur in some species of Mesodinium. Ciliates with phototrophic endosymbionts have evolved independently in marine and freshwater habitats. The enslaved algal cells or chloroplasts provide host cells with organic matter. Mixotrophs flourish in oxygen-rich, but also in micro-aerobic waters and in the complete absence of oxygen. In the latter case, the aerobic host retains aerobic metabolism, sustained by the oxygen produced by the phototrophic endosymbionts or the sequestered chloroplasts. Mixotrophic ciliates can attain spectacular abundances in some habitats, and entirely dominate the ciliate community.     

Molecular approaches to diagnosing nutritional physiology in harmful algae: Implications for studying the effects of eutrophication

Every year harmful algal blooms (HABs) cause serious impacts to local economies, coastal ecosystems, and human health on a global scale. It is well known that nutrient availability can influence important aspects of harmful algae biology and ecology, such as growth, toxin production, and life cycle stage, as well as bloom initiation, persistence and decline. Increases in the rate of supply of organic matter to ecosystems (eutrophication) carries many possible ramifications to coastal systems, including the potential for nutrient enrichment and the potential for stimulation of harmful algal blooms. Traditional studies on algal nutrition typically use either cultured isolates or community level assays, to examine nutrient uptake, nutrient preference, elemental composition, and other metrics of a species’ response to nutrients. In the last decade, technological advances have led to a great increase in the number of sequences available for critical harmful species. This, in turn, has led to new insights with regards to algal nutrition, and these advances highlight the promise of molecular technologies, and genomic approaches, to improving our understanding of algal nutrient acquisition and nutritional physiological ecology, in both cultures and field populations. With these developments increased monitoring of nutritional physiology in field populations of harmful algae will allow us to better discriminate how eutrophication impacts these groups.     

Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp.

Receiving coastal waters and estuaries are among the most nutrient‐enriched environments on earth, and one of the symptoms of the resulting eutrophication is the proliferation of opportunistic, fast‐growing marine seaweeds. Here, we used a widespread macroalga often involved in blooms, Ulva spp., to investigate how supply of nitrogen (N) and phosphorus (P), the two main potential growth‐limiting nutrients, influence macroalgal growth in temperate and tropical coastal waters ranging from low‐ to high‐nutrient supplies. We carried out N and P enrichment field experiments on Ulva spp. in seven coastal systems, with one of these systems represented by three different subestuaries, for a total of nine sites. We showed that rate of growth of Ulva spp. was directly correlated to annual dissolved inorganic nitrogen (DIN) concentrations, where growth increased with increasing DIN concentration. Internal N pools of macroalgal fronds were also linked to increased DIN supply, and algal growth rates were tightly coupled to these internal N pools. The increases in DIN appeared to be related to greater inputs of wastewater to these coastal waters as indicated by high δ¹⁵N signatures of the algae as DIN increased. N and P enrichment experiments showed that rate of macroalgal growth was controlled by supply of DIN where ambient DIN concentrations were low, and by P where DIN concentrations were higher, regardless of latitude or geographic setting. These results suggest that understanding the basis for macroalgal blooms, and management of these harmful phenomena, will require information as to nutrient sources, and actions to reduce supply of N and P in coastal waters concerned.     

Promotion of harmful algal blooms by zooplankton predatory activity

The relationship between algae and their zooplanktonic predators typically involves consumption of nutrients by algae, grazing of the algae by zooplankton which in turn enhances predator biomass, controls algal growth and regenerates nutrients. Eutrophication raises nutrient levels, but does not simply increase normal predator-prey activity; rather, harmful algal bloom (HAB) events develop often with serious ecological and aesthetic implications. Generally, HAB species are outwardly poor competitors for nutrients, while their development of grazing deterrents during nutrient stress ostensibly occurs too late, after the nutrients have largely been consumed already by fast-growing non-HAB species. A new mechanism is presented to explain HAB dynamics under these circumstances. Using a multi-nutrient predator-prey model, it is demonstrated that these blooms can develop through the self-propagating failure of normal predator-prey activity, resulting in the transfer of nutrients into HAB growth at the expense of competing algal species. Rate limitation of this transfer provides a continual level of nutrient stress that results in HAB species exhibiting grazing deterrents protecting them from top-down control. This process is self-stabilizing as long as nutrient demand exceeds supply, maintaining the unpalatable status of HABs; such events are most likely under eutrophic conditions with skewed nutrient ratios.     

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.     

Recombinase-aided amplification combined with lateral flow dipstick for the rapid detection of Amphidinium carterae

Journal of Applied Phycology - In the context of global climate change, the frequency and duration of harmful algal blooms (HABs) due to eutrophic coastal waters have increased. HABs can cause...     

Factors influencing seaweed responses to eutrophication: some results from EU-project EUMAC

Seaweed responses to eutrophication and their role in coastal eutrophication processes were compared at 8 different sites along the European coasts from the Baltic to the Mediterranean as part of the EU-ENVIRONMENT Project Marine Eutrophication and benthic Macrophytes (EUMAC). Structural and functional changes of marine benthic vegetation typical of eutrophic waters, in particular mass development (blooms) of certain seaweeds, are not merely the result of increased nutrient loading, but must be attributed to complex interactions of primary and secondary effects during the eutrophication process. Due to species-specific physiological properties of the algae (nutrient kinetics, growth potential, light, temperature requirements), the combined effects of abiotic and biotic factors on juvenile or adult developmental stages control the development of algal blooms in different ways. In particular the role of light, temperature, water motion and oxygen depletion, as well as of grazers, on early and adult developmental stages of the algae are considered. The result are discussed in the context of coastal eutrophication control and management. This revised version was published online in June 2006 with corrections to the Cover Date.     

The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles

Many non-photosynthetic species of protists and metazoans are capable of hosting viable algal endosymbionts or their organelles through adaptations of phagocytic pathways. A form of mixotrophy combining phototrophy and heterotrophy, acquired phototrophy (AcPh) encompasses a suite of endosymbiotic and organelle retention interactions, that range from facultative to obligate. AcPh is a common phenomenon in aquatic ecosystems, with endosymbiotic associations generally more prevalent in nutrient poor environments, and organelle retention typically associated with more productive ones. All AcPhs benefit from enhanced growth due to access to photosynthetic products; however, the degree of metabolic integration and dependency in the host varies widely. AcPh is found in at least four of the major eukaryotic supergroups, and is the driving force in the evolution of secondary and tertiary plastid acquisitions. Mutualistic resource partitioning characterizes most algal endosymbiotic interactions, while organelle retention is a form of predation, characterized by nutrient flow (i.e., growth) in one direction. AcPh involves adaptations to recognize specific prey or endosymbionts and to house organelles or endosymbionts within the endomembrane system but free from digestion. In many cases, hosts depend upon AcPh for the production of essential nutrients, many of which remain obscure. The practice of AcPh has led to multiple independent secondary and tertiary plastid acquisition events among several eukaryote lineages, giving rise to the diverse array of algae found in modern aquatic ecosystems. This article highlights those AcPhs that are model research organisms for both metazoans and protists. Much of the basic biology of AcPhs remains enigmatic, particularly (1) which essential nutrients or factors make certain forms of AcPh obligatory, (2) how hosts regulate and manipulate endosymbionts or sequestered organelles, and (3) what genomic imprint, if any, AcPh leaves on non-photosynthetic host species.     

Behavioural differences underlie toxicity and predation variation in blooms of Prymnesium parvum

Much of the evolutionary ecology of toxic algal blooms (TABs) remains unclear, including the role of algal toxins in the adaptive ‘strategies’ of TAB-forming species. Most eukaryotic TABs are caused by mixotrophs that augment autotrophy with organic nutrient sources, including competing algae (intraguild predation). We leverage the standing diversity of TABs formed by the toxic, invasive mixotroph Prymnesium parvum to identify cell-level behaviours involved in toxin-assisted predation using direct observations as well as comparisons between genetically distinct low- and high-toxicity isolates. Our results suggest that P. parvum toxins are primarily delivered at close range and promote subsequent prey capture/consumption. Surprisingly, we find opposite chemotactic preferences for organic (prey-derived) and inorganic nutrients between differentially toxic isolates, respectively, suggesting behavioural integration of toxicity and phagotrophy. Variation in toxicity may, therefore, reflect broader phenotypic integration of key traits that ultimately contribute to the remarkable flexibility, diversity, and success of invasive populations.     

沿岸海域富营养化与赤潮发生的关系

综述了赤潮的发生与沿岸海域富营养化的关系。近几十年来,人类活动使得天然水体的富营养化进程大大加速。营养负荷的增加与高生物量水华的增多相联系。控制营养输入后,浮游植物生物量或有害藻类水华事件也相应减少。营养的组成与浮游植物的种类组成及水华的形成有密切联系。有机营养对有害藻类水华的促进作用受到关注。营养输入时机影响浮游植物种间竞争的结果,因而对浮游植物的群落演替具有深远影响。由于浮游植物存在生理差异,因而对营养加富的反应因种而异。营养在调控某些有毒藻类的毒素产量方面也发挥着重要作用。此外,营养输入与藻类水华之间存在复杂的间接联系。当然,营养状况并非浮游植物群落演替的唯一决定因素。研究结果提示,控制营养输入、减缓水域富营养化是减少有害藻类水华发生的有效途径,而深入研究典型有害藻类的营养生理对策则为防治并最终消除有害藻类水华提供了理论基础。     

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.     

Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations

Many ciliates acquire the capacity for photosynthesis through stealing plastids or harboring intact endosymbiotic algae. Both phenomena are a form of mixotrophy and are widespread among ciliates. Mixotrophic ciliates may be abundant in freshwater and marine ecosystems, sometimes making substantial contributions toward community primary productivity. While mixotrophic ciliates utilize phagotrophy to capture algal cells, their endomembrane system has evolved to partially bypass typical heterotrophic digestion pathways, enabling metabolic interaction with foreign cells or organelles. Unique adaptations may also be found in certain algal endosymbionts, facilitating establishment of symbiosis and nutritional interactions, while reducing their fitness for survival as free-living cells. Plastid retaining oligotrich ciliates possess little selectivity from which algae they sequester plastids, resulting in unstable kleptoplastids that require frequent ingestion of algal cells to replace them. Mesodinium rubrum (=Myrionecta rubra) possesses cryptophyte organelles that resemble a reduced endosymbont, and is the only ciliate capable of functional phototrophy and plastid division. Certain strains of M. rubrum may have a stable association with their cryptophyte organelles, while others need to acquire a cryptophyte nucleus through feeding. This process of stealing a nucleus, termed karyoklepty, was first described in M. rubrum and may be an evolutionary precursor to a stable, reduced endosymbiont, and perhaps eventually a tertiary plastid. The newly described Mesodinium"chamaeleon," however, is less selective of which cryptophyte species it will retain organelles, and appears less capable of sustained phototrophy. Ciliates likely stem from a phototrophic ancestry, which may explain their propensity to practice acquired phototrophy.     

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.     

Prorocentrum minimum (Pavillard) Schiller: A review of a harmful algal bloom species of growing worldwide importance

Prorocentrum minimum (Pavillard) Schiller, a common, neritic, bloom-forming dinoflagellate, is the cause of harmful blooms in many estuarine and coastal environments. Among harmful algal bloom species, P. minimum is important for the following reasons: it is widely distributed geographically in temperate and subtropical waters; it is potentially harmful to humans via shellfish poisoning; it has detrimental effects at both the organismal and environmental levels; blooms appear to be undergoing a geographical expansion over the past several decades; and, a relationship appears to exist between blooms of this species and increasing coastal eutrophication. Although shellfish toxicity with associated human impacts has been attributed to P. minimum blooms from a variety of coastal environments (Japan; France; Norway; Netherlands; New York, USA), only clones isolated from the Mediterranean coast of France, and shellfish exposed to P. minimum blooms in this area, have been shown to contain a water soluble neurotoxic component which killed mice. Detrimental ecosystem effects associated with blooms range from fish and zoobenthic mortalities to shellfish aquaculture mortalities, attributable to both indirect biomass effects (e.g., low dissolved oxygen) and toxic effects. P. minimum blooms generally occur under conditions of high temperatures and incident irradiances and low to moderate salinities in coastal and estuarine environments often characterized as eutrophic, although they have been found under widely varying salinities and temperatures if other factors are conducive for growth. The physiological flexibility of P. minimum in response to changing environmental parameters (e.g., light, temperature, salinity) as well as its ability to utilize both inorganic and organic nitrogen, phosphorus, and carbon nutrient sources, suggest that increasing blooms of this species are a response to increasing coastal eutrophication.     

The potential role of anthropogenically derived nitrogen in the growth of harmful algae in California,USA

Cultural eutrophication is frequently invoked as one factor in the global increase in harmful algal blooms, but is difficult to definitively prove due to the myriad of factors influencing coastal phytoplankton bloom development. To assess whether eutrophication could be a factor in the development of harmful algal blooms in California (USA), we review the ecophysiological potential for urea uptake by Pseudo-nitzschia australis (Bacillariophyceae), Heterosigma akashiwo (Raphidophyceae), and Lingulodinium polyedrum (Dinophyceae), all of which have been found at bloom concentrations and/or exhibited noxious effects in recent years in California coastal waters. We include new measurements from a large (Chlorophyll a > 500 mg m⁻³) red tide event dominated by Akashiwo sanguinea (Dinophyceae) in Monterey Bay, CA during September 2006. All of these phytoplankton are capable of using nitrate, ammonium, and urea, although their preference for these nitrogenous substrates varies. Using published data and recent coastal time series measurements conducted in Monterey Bay and San Francisco Bay, CA, we show that urea, presumably from coastal eutrophication, was present in California waters at measurable concentrations during past harmful algal bloom events. Based on these observations, we suggest that urea uptake could potentially sustain these harmful algae, and that urea, which is seldom measured as part of coastal monitoring programs, may be associated with these harmful algal events in California.     

Harmful algal blooms of allelopathic microalgal species: The role of eutrophication

The ability of certain harmful algal species to produce and release chemicals that inhibit the growth of co-occurring phytoplankton species, here considered as allelopathy, is closely associated with competition for limiting nutrient resources. Many phytoplankton cells are known to release elevated amounts of organic compounds under nutrient limitation. Eutrophication alters the nitrogen-to-phosphorus balance and, when nutrient availability is unbalanced, nutrient limitation may result. Algal species that can compete successfully for available growth-limiting nutrient(s) have the potential to become dominant and form blooms. The stress conditions imposed by the shifted nutrient supply ratios can, in some algae, stimulate production of allelochemicals that inhibit potential competitors. Thus, under cultural eutrophication, altered nutrient (N, P) ratios and limiting nutrient supplies can stimulate increased production of allelochemicals, including toxins, by some algal species and accentuate the adverse effects of these substances on other algae. Future investigation on the characterization of the chemical compounds involved in the allelopathic process are needed to advance the study of the mode of action of phytoplankton allelochemicals.     

Modeling the bacterial contribution to planktonic community respiration in the regulation of solar energy and nutrient availability

In planktonic ecosystems, algae and bacteria exhibit complex interrelationships, as algae provide an important organic matter source for microbial growth while microbial metabolism recycles limiting nutrients for algae in a loose commensalism. However, algae and bacteria can also compete for available nutrients if supplies of organic matter are sufficient to satisfy bacterial demand. We developed a stoichiometrically explicit model of bacteria–algae interactions that incorporated realistic assumptions about algal light and nutrient utilization, algal exudation of organic matter, and bacterial processing of organic matter and nutrients. The model makes specific predictions about how the relative balance of algae and bacteria should change in response to varied nutrient and light availability seen in lakes and oceans. The model successfully reproduces published empirical data and indicates that, under moderate nutrient supply, the bacterial percentage of total respiration should be maximal at intermediate light intensity.