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

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

Domoic acid production and elemental composition of two Pseudo-nitzschia multiseries strains from the NW and SW Atlantic Ocean, growing in phosphorus- or nitrogen-limited chemostat cultures

Here we compare cell physiology and domoic acid (DA) production for two strains of the diatom Pseudo-nitzschia multiseries originating from two opposite latitudes: Canada (CA) and Brazil (BR). The algae were grown as chemostat cultures at 0.2, 0.3 and 0.4 day21 under nitrogen (N)- and phosphorus (P)-deficient conditions. The level of deficiency significantly affected the atomic C:N, C:P, C:Si and N:P ratios in both strains. In both strains, P per cell was 2–4 higher in the N- than in the P-deficient cultures. The opposite was not found for N in the P-deficient cultures, as shown by the N:P ratios and C:N ratios. The C:N and C:P ratios were significantly lower in the CA strain, and this did not change due to the level of deficiency. The concentration and production of DA per cell per day were significantly higher for both strains under P deficiency as expected since the toxin is rich in N. However, DA was also produced by both strains during continuous cell division under N deficiency. High or low bacterial densities associated with P. multiseries did not increase or decrease DA production. Our data imply that more attention needs to be given to the N:P ratios and concentrations in the waters where these algae occur, as both N and P deficiencies affect DA production and cellular DA concentrations

Structuring of a postspring phytoplankton community by manipulation of trophic interactions

To study the effects of grazing on a natural post-spring phytoplankton community a land-based mesocosm experiment was performed during late spring 1988 (7-18 June). 300-1 polyethylene cylinders, immersed in a flexible pool for temperature regulation, were filled with a plankton community filtered through a 90-pm nylon net. In duplicate cylinders, the ambient copepod concentration (mainly an Acartia sp.), five times the ambient concentration, ambient concentration + medusae of the scyphozoan Aurelia aurita (L.) and ambient concentration + mussels (Mytilus edulis L.) were added. Nutrients were added throughout the experimental period to keep the concentrations at 5 pM nitrate, 0.5 pM phosphate and l0 #M silica. Chl a, nutrients and densities of phytoplankton, ciliates and copepods were measured throughout the experiment. We observed that the diatoms remaining from the sprimz bloom could, with small additions of nutrients, outgrow their grazers. Only a small reduction in copepod grazing pressure through medusae predation on copepods was required for an even stronger growth and domir:ance by diatoms. This pattern of development could be broken by an increase in Acartia sp. biomass. An initial addition of five times the natural concentration of Acartia sp. led to a rapid growth of monads, < 3 #m, which constituted almost 100°o of the biomass after 3 days. When Acartia sp. decreased in biomass, diatoms and cryptomonads became dominant. As the small naked ciliate Urotricha sp. had already been eliminated by the initially abundant copepods in the cylinders where the copepod concentration was five times the ambient concentration, there were few grazers left to make use of the ample food supply. Urotricha sp. could possibly control the < 3- #m monads if not or only moderately predated by Acartia sp., indicated by the lower increase in monad biomass in the cylinders where mussels or medusae were added. M. edulis was capable of grazing down all phytoplankton species to very low densities, except monads < 3 #m, in spite of nutrient additions, indicating a possible nonspecies-selective control ofphytoplankton abundance by benthic filter-feeders in eutrophicated areas

Impact of a Dinophysis acuminata Bloom on the Copepod Acartia clausi: first indications

Faecal pellet production and content along with egg production of the dominant copepod species Acartia clausi were studied in the Thermaikos Gulf (NW Aegean Sea) during a pre-bloom and a bloom of the toxic dinoflagellate Dinophysis acuminata. Both faecal pellet production (6.8–8.6 ind−1 d−1) and egg production (15.8–47.6 ind−1 d−1) appeared unrelated to the D. acuminata bloom. Less than 11% of the copepod faecal pellets contained one or two D. acuminata cells, almost intact, whereas the other material in the pellets was broken into small pieces or amorphous shapes. The toxin outflux seemed to be insignificant when compared to the mean toxin concentration from the whole D. acuminata population. Finally, the potential grazing impact of A. clausi on D. acuminata during the study period was low.European Commission | Ref. EVK3-2001-00055European Commission | Ref. H2020, n. 87115