The role of mixotrophic protists in the biological carbon pump

The traditional view of the planktonic food web describes consumption of inorganic nutrients by photoautotrophic phytoplankton, which in turn supports zooplankton and ultimately higher trophic levels. Pathways centred on bacteria provide mechanisms for nutrient recycling. This structure lies at the foundation of most models used to explore biogeochemical cycling, functioning of the biological pump, and the impact of climate change on these processes. We suggest an alternative new paradigm, which sees the bulk of the base of this food web supported by protist plankton communities that are mixotrophic – combining phototrophy and phagotrophy within a single cell. The photoautotrophic eukaryotic plankton and their heterotrophic microzooplankton grazers dominate only during the developmental phases of ecosystems (e.g. spring bloom in temperate systems). With their flexible nutrition, mixotrophic protists dominate in more-mature systems (e.g. temperate summer, established eutrophic systems and oligotrophic systems); the more-stable water columns suggested under climate change may also be expected to favour these mixotrophs. We explore how such a predominantly mixotrophic structure affects microbial trophic dynamics and the biological pump. The mixotroph-dominated structure differs fundamentally in its flow of energy and nutrients, with a shortened and potentially more efficient chain from nutrient regeneration to primary production. Furthermore, mixotrophy enables a direct conduit for the support of primary production from bacterial production. We show how the exclusion of an explicit mixotrophic component in studies of the pelagic microbial communities leads to a failure to capture the true dynamics of the carbon flow. In order to prevent a misinterpretation of the full implications of climate change upon biogeochemical cycling and the functioning of the biological pump, we recommend inclusion of multi-nutrient mixotroph models within ecosystem studies

Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies

Arranging organisms into functional groups aids ecological research by grouping organisms (irrespective of phylogenetic origin) that interact with environmental factors in similar ways. Planktonic protists traditionally have been split between photoautotrophic “phytoplankton” and phagotrophic “microzoo-plankton”. However, there is a growing recognition of the importance of mixotrophy in euphotic aquatic systems, where many protists often combine photoautotrophic and phagotrophic modes of nutrition. Such organisms do not align with the traditional dichotomy of phytoplankton and microzooplankton. To reflect this understanding,we propose a new functional grouping of planktonic protists in an eco- physiological context: (i) phagoheterotrophs lacking phototrophic capacity, (ii) photoautotrophs lacking phagotrophic capacity,(iii) constitutive mixotrophs (CMs) as phagotrophs with an inherent capacity for phototrophy, and (iv) non-constitutive mixotrophs (NCMs) that acquire their phototrophic capacity by ingesting specific (SNCM) or general non-specific (GNCM) prey. For the first time, we incorporate these functional groups within a foodweb structure and show, using model outputs, that there is scope for significant changes in trophic dynamics depending on the protist functional type description. Accord- ingly, to better reflect the role of mixotrophy, we recommend that as important tools for explanatory and predictive research, aquatic food-web and biogeochemical models need to redefine the protist groups within their frameworks

Contribution of phagotrophy versus autotrophy to Prymnesium parvum growth under nitrogen and phosphorus sufficiency and deficiency

Laboratory experiments were conducted to test the effects of nitrogen (N) and phosphorus (P) sufficiency and deficiency on mixotrophy in Prymnesium parvum (Haptophyta). P. parvum was grown with and without algal prey (Rhodomonas salina) and observed for 120 h. Detection and enumeration of cells containing food vacuoles with prey (i.e. phagotrophy) was based on flow cytometric detection of fluorescence of an acidotropic probe. Overall, the presence of R. salina increased phagotrophy in P. parvum suggesting that, at least in this strain of P. parvum, the presence of suitable prey can stimulate phagotrophic behavior in P. parvum. Feeding frequency (the percentage of P. parvum cells containing food vacuoles in a given time) was significantly higher under N and P deficiency than in the nutrient-sufficient treatments. A nutrient budget constructed from the data indicated that ingestion of organic matter (OM) supplied with 78 ± 7% of the N (3.9 ± 0.3 μM) incorporated by P. parvum in the N-deficient treatment, and 45 ± 9% of the P (0.3 ± 0 μM) acquired in the P-deficient cultures. Even under nutrient sufficiency, ingestion of OM was estimated to have supplied 43 ± 16% of the N and 48 ± 16% of the P incorporated into P. parvum cells. Phagotrophy was observed even in the NP-sufficient cultures (non-axenic mixed and monocultures), although P. parvum cells did not lose their photosynthetic capability, suggesting that phagotrophy is probably a permanent nutritional adaptation to this species. The ingestion of organic nutrients played an important role in P. parvum growth, being a reliable source of nutrition for P. parvum inorganic nutrient limitation, and could explain its capabilities to form persistent blooms

Effect of tertiary sewage effluent additions on Prymnesium parvum cell toxicity and stable isotope ratios

We investigated the ability of the ichthyotoxic haptophyte Prymnesium parvum to use sewage-originated nutrients applying stable carbon (C) and nitrogen (N) isotope techniques. P. parvum was cultured under N and phosphorus (P) sufficient and deficient conditions in either sewage effluent-based medium or in a nitrate- and phosphate-based control. Cell densities and toxicities were monitored and stable carbon N isotopes signatures (delta C-13 and delta N-15) of P. parvum and the sewage effluent analysed. Nitrogen and P sufficient cultures achieved the highest biomass followed by P and N deficient cultures, regardless of sewage effluent additions. The P deficient cultures with sewage effluent had higher toxicity, estimated as haemolytic activity (9.4 +/- 0 x 10(-5) mg Saponin equiv. cell(-1)) compared to the P deficient control and to all N deficient and NP sufficient cultures. Nutrient deficient conditions had no effect on the cell delta N-15, but a decreasing effect on delta C-13 in the inorganic N deficient treatment. Growth in sewage-based media was followed by a substantial increase in the cell delta N-15 (10.4-16.1.60) compared to the control treatments (2.4-4.9%o), showing that P. parvum is capable of direct use of sewage-originated N, inorganic as well as organic. Uptake of terrestrial derived C in the sewage treatments was confirmed by a decrease in cell delta C-13, implying that P. parvum is able to utilize organic nutrients in sewage effluent. (C) 2008 Elsevier B.V. All rights reserved

Nitrogen uptake kinetics of Prymnesium parvum (Haptophyte)

The uptake rates of different nitrogen (N) forms (NO3−, urea, and the amino acids glycine and glutamic acid) by N-deficient, laboratory-grown cells of the mixotrophic haptophyte, Prymnesium parvum, were measured and the preference by the cells for the different forms determined. Cellular N uptake rates (ρcell, fmol N cell−1 h−1) were measured using 15N-labeled N substrates. P. parvum showed high preference for the tested amino acids, in particular glutamic acid, over urea and NO3− under the culture nutrient conditions. However, extrapolating these rates to Baltic Seawater summer conditions, P. parvum would be expected to show higher uptake rates of NO3− and the amino acids relative to urea because of the difference in average concentrations of these substrates. A high uptake rate of glutamic acid at low substrate concentrations suggests that this substrate is likely used through extracellular enzymes. Nitrate, urea and glycine, on the other hand, showed a non-saturating uptake over the tested substrate concentration (1–40 μM-N for NO3− and urea, 0.5–10 μM-N for glycine), indicating slower membrane-transport rates for these substrates

Minimizing economical losses with the help of “real-time” algal surveillance

Cyanobacterial blooms covering almost the entire Baltic Sea is a yearly feature during July-August. For the tourism industry at Öland island, SE Sweden, the economical losses during the summer 2005 amounted to 17-23 million euros. Remote sensing satellite images show that all the Öland beaches are covered with decomposing algae. In reality, these blooms rarely reach the western side of the island. To more accurately inform the public on the quality of the water for swimming, with the help of volunteers, a daily real-time surveillance of the algal densities on the beaches was performed. The volunteers (from 15 years old to pensioners) were trained at the Linnaeus University, from simple laboratory techniques, to more complicated ones such as identification and enumeration of the toxic cyanobacteria species. By latest 9.00 a.m., the public had access to information on the algal situation on 17 beaches. We could show that: 1) although remote sensing images showed Öland being surrounded by the blooms, our surveillance showed no algal accumulations on the beaches 2) that the real-time warning system boosted public confidence in the local water quality and during the first “Miss Algae”-summer 2006, the economical losses by the tourism industry turned in profits, the gain amounting to 17 million euros, 3) this kind of real-time surveillance is economical feasible due to low-costs involved, but also, the project has a great social value for the volunteers who mostly were pensioners. The volunteers who participated in “Miss Algae” had a good knowledge about the area they monitored (as their houses are located nearby) and could disseminate knowledge to the public in these areas. This kind of project also render a lot of interest regional, national and international, and can be used in advertising campaigns to increase tourism in the areas affected by algal blooms

Carbon isotope signature variability among cultured microalgae: Influence of species, nutrients and growth

In this study we have investigated whether the carbon isotopic signature differs between different groups and species of marine phytoplankton depending on growth phase, nutrient conditions and salinity. The 15 investigated algal species, representing the Bacillariophyceae, Chlorophyceae, Cryptophyceae, Cyanophyceae, Dinophyceae and Haptophyceae classes were grown in batch monocultures and analysed for delta C-13 in both exponential and stationary phase. For all the cultured species, delta C-13 signatures ranged from -23.5 parts per thousand (Imantonia sp.) to - 12.3 parts per thousand (Nodulania spumigena) in the exponential phase and from - 18.8 parts per thousand (Amphidinium carterae) to - 8.0 parts per thousand (Anabaena lemmermannii) in the stationary phase. Three species (Dunaliella tertiolecta, Rhodomonas sp.. Heterocapsa triquetra) were also grown under nutrient sufficient and nitrogen or phosphorus deficient conditions. Nitrogen limitation resulted in a more negative delta C-13 signature, whereas no effect could be observed during phosphorus limitation compared to nutrient sufficient conditions. Growth of Prymnesium parvum in two different salinities resulted in a more negative delta C-13 signature in the 26 parts per thousand-media compared to growth in 7 parts per thousand-media. Our results show that the carbon isotopic signature of phytoplankton may be affected by salinity, differ among different phytoplankton species, between exponential and stationary phase, as well as between nutrient treatments. (C) 2009 Elsevier B.V. All rights reserved

The ecophysiology and bloom dynamics of Prymnesium spp.

Members of Prymnesium belong to the division Haptophyta, class Prymnesiophyceae, order Prymnesiales and family Prymnesiaceae. As most haptophytes, members of the genus Prymnesium are unicellular and planktonic. The most known of these species is the ichthyotoxic P. parvum, which may form nearly monospecific dense blooms in coastal and inland waters. This species possesses extraordinary plasticity concerning life survival strategies, and is specifically addressed in this review. Toxins produced by P. parvum have hemolytic properties, that not only kill fish but also co-existing plankton. These substances are allelopathic (when other algae are killed) and grazer deterrent (when grazers are killed). Allelopathy enables P. parvum to utilize inorganic nutrients present in the surrounding water without competition from other algal species; and by eliminating its grazers P. parvum reduces cell losses. The paralized microalgae and/or zooplankton, are therefter ingested by the P. parvum cells, a process called phagotrophy. P. parvum is also able of osmotrophy, i.e. utilization of dissolved organic matter. In this review, the cellular characteristics, life cycles, bloom formation, and factors affecting toxicity, allelopathy, phagotrophy, and osmotrophy of P. parvum are discussed