Literature Review of the Microalga Prymnesium parvum and its Associated Toxicity
Sean Watson, Texas Parks and Wildlife Department, August 2001
A study by McLaughlin (1958) showed that optimal NaCl concentrations for the growth of one Scottish and two Israeli strains P. parvum occurred at 0.3%-6% with growth possible at 0.1%-10%. Padilla (1970) observed that low salinities (less than 10%) increased the doubling time of P. parvum cells and induced high levels of protein and nucleic acid. Paster (1973) noted 0.3%-5% NaCl as optimal for growth of P. parvum. P. parvum germinated in the low-salinity environment (4-5%) of the fjord branch Hylsfjorden in the Sandsfjord system of southwest Norway (Kaartvedt et al. 1991). A 1993 study reported an optimal salinity range of 8-25% for a P. parvum strain from Denmark (Larsen et al. 1993). Larsen and Bryant (1998) reported that the Norwegian, Danish and English P. parvum strains they tested grew over a wide range of salinities each with different optimum growth concentrations, and that all three strains survived salinities from 3 to 30 psu (or .3%-3%). These researchers also speculated that discrepancies from earlier studies could have been due to the unknowing use of different strains of P. parvum. The water associated with the fish kill in Morocco was characterized by an elevated salinity of 8.6-12.4% (Sabour et al. 2000).
Dickson and Kirst (1987) speculated that the success of P. parvum in variable saline environments may be due to its ability to synthesize compatible solutes. In this 1987 study of osmotic adjustment in marine algae, the researchers found that P. parvum showed an increase in DMSP (a tertiary sulphonium compound: B-dimethylsulphoniopropionate), as compared to other algae in this study, and an increase in the synthesis of an unknown polyol. The authors suggested that the increasing synthesis of these two molecules may aid in osmoregulation. They concluded that thcontrol of compatible solute synthesis by P. parvum may give this microalga an advantage in environments with fluctuating salinities.
Shilo and Aschner (1953) observed that temperatures greater than 30 C were inhibitory to the growth of P. parvum, and 35 C resulted in lysis. The authors also discovered that P. parvum cells survive 2 C for many days. In the 1958 study by McLaughlin, it was found that the three strains of P. parvum tested (1 Scottish strain and 2 Israeli strains) showed erratic growth above 32 C with death occurring at 34 C. separate study by Larsen, Eikrem and Paasche (1993) found that the Denmark strain of P. parvum used had a growth temperature optimum of 26 C. The authors noted that this same strain was found to be severely limited at 10 C. The Danish, Norwegian and English strains of P. parvum tested by Larsen and Bryant (1998) exhibited a maximum growth rate at 15 C with two of the strains (Norwegian and Danish) tolerating a wide temperature range of 5 C to 30 C. The authors noted that this finding supports the notion that P. parvum is a eurythermal organism. The P. parvum outbreak in Morocco was characterized by water with moderate temperatures between 15C-23.5C (Sabour et al. 2000).
McLaughlin (1958) found that the success of P. parvum growth below pH 7 depended on the adjustment of concentrations of metal ions. The author discovered that the metal ions Fe, Zn, Mo, Cu or Co, with an increase in the concentration of any of these, resulted in increased growth with the adjustment of Fe concentrations determined to be the most important. The author also noted that, for the three strains tested, growth below pH 5.8 was erratic, and all cells remained viable to pH 5. The P. parvum outbreak in Morocco occurred in water with a pH of 7.67-9.04 (Sabour et al. 2000).
Wynne and Rhee (1988) noticed that, in P. parvum, the activity of alkaline phosphatase is higher at saturation light intensities. The authors also noted that an increase in light intensities allows P. parvum to increase the speed at which it is able to take up phosphate from its environment, and it therefore seems that changes in light intensities have a profound affect on competition. However, it has been found that excessive illumination inhibits the growth of P. parvum (Padan et al. 1967).
Rahat and Jahn (1965) discovered that heterotrophic growth of P. parvum is possible in the dark with high concentrations of glycerol available. They noted that the optimal concentration of glycerol was found to be lower in the light than in the dark. Chisholm and Brand (1981) found that P. parvum divided primarily in the dark period (L:D 14:10), and that this division is phased (synchronized) by the light/dark cycle. Jochem (1999) tested the dark survival strategies of P. parvum, and determined that P. parvum was a Type II cell when exposed to prolonged darkness (in Type II cells, metabolic activity continues ‘as usual’ in the dark resulting in a decrease in cell abundance). The author found that the surviving cells needed new energy upon illumination to refill exhausted cellular reserves before the cells could divide, and would therefore not be advantageous in long or short dark periods.
It is known that phosphate is limiting to phytoplankton growth in the summer (Larsen et al. 1993). McLaughlin (1958) determined that P. parvum is able to satisfy its phosphate requirement from a wide range of compounds. The author noted that the three strains of P. parvum were indifferent to high or low levels of inorganic phosphate, and speculated that this may be due to the presence of many phosphatases. This obligate phototroph was also found to graze bacteria, especially when phosphate is limiting, and it therefore seems that bacteria may be a source of phosphate for this microalga when phosphate is scarce (Nygaard and Tobiesen 1993).
McLaughlin (1958) found that ammonia is a good source of nitrogen for P. parvum in the acid pH range. The author discovered that in acidic media, ammonium
salts, the amino acids aspartic and glutamic acid, alanine, methionine, histidine,
proline, glycine, tyrosine, serine, leucine, and isoleucine all can be utilized
as a nitrogen source by this organism. In alkaline media, nitrate, creatine,
asparagines, arginine, alanine,
histidine, methionine and acetyl-urea were found by the author to be good sources of nitrogen. Syrett (1962) reported that P. parvum is not able to utilize urea as a nitrogen source. Methionine and ethionine can be utilized as sole nitrogen sources by P. parvum, and they are not inhibitory at high concentrations (Rahat and Reich 1963).
Increases in the concentrations of nitrogen and phosphorous (and other nutrients) in water ultimately leads to eutrophication. The introduction of phosphorous to waterways may be from agricultural runoff (including fish ponds and aquaculture) and domestic sources. Nitrogen also comes from agriculture and is also introduced through airborne nitrogen precipitation from traffic emissions (Finnish Environmental Administration 2001). Holdway , Watson and Moss (1978) noted that there could be a relationship between the degree of eutrophication and population sizes of P. parvum. This is likely since eutrophication is known to cause an increase in phytoplankton and algae along with other aquatic plant life (Finnish Environmental Administration 2001).
Holdway, Watson and Moss (1978) noted that, in the Thurne system of Norfolk Broads, England, P. parvum competes poorly with Chlorococcalean, small cyanophytan and diatoms. They suggested that an increase of phosphorous and nitrogen may ease this competition and allow P. parvum to capture available nutrients more quickly. The authors noted that increases in fertility in the Hicking Broad-Horsey Mare-Heigham Sound area of River Thurne system caused eutrophication followed by heavy phytoplankton growth and a decrease in submerged macrophytes in these areas where P. parvum blooms occurred (Martham Broad, also in the Thurne system, was noted as having submerged macrophytes and also lower levels of P. parvum cells). They believed that the increase in nitrogen in the Thurne system was most probably from agriculture, and phosphorous-loading was likely from a large population of black-headed gulls. The authors remarked that a connection may be seen in the 1938 bloom of P. parvum in Ketting Nor, Denmark where it was noted that gulls were polluting the water causing it to turn turbid followed by the disappearance of macrophytes.
Kaartvedt, Johnsen, Aksnes and Lie (1991) noted that currents in the Hylsfjorden branch of the Sandsfjorden system, Norway, were weak which led to a long residence time of the brackish water in this fjord branch. The authors suggested that this resulted in low advective loss of P. parvum, relatively high temperatures and depletion in nitrogen and silica derived from freshwater with the low silicate levels favoring the proliferation of flagellates over diatoms. They speculated that low exchange rates and benthic settlement (P. parvum was found associated with the benthic green macroalgae Cladophora spp., and on nets of fish farms) of P. parvum could have facilitated an increased efficiency in the use of nutrients supplied by fish farms. They noted that the discharge of a hydroelectric power plant just after the first observed fish mortalities caused advection of P. parvum and its associated toxin throughout the Sandsfjord system. The authors suggested that subsequent large amounts of additional freshwater runoff from other sources aided in the dispersal of the algae, and may have also played a part in phosphorous limitation since the freshwater input contained low concentrations of phosphates. Overall, the authors concluded that fertilization associated with fish farming seems to have created a favorable environment for a P. parvum bloom in the Sandsfjord system. The association of P. parvum with Cladophora sp. and other macroalgae was tested by Johnsen and Lein (1989) with the conclusion that P. parvum is attracted to macroalgae (P. parvum grown in nutrient-poor solutions swam toward Cladophora sp.). The authors offered the possible explanation that P. parvum is chemotactic and may attach to macroalgae (via the haptonema) that give off dissolved organic matter when the concentrations of nutrients in the water is low. They also suggested that microalgae with the ability to utilize organic matter given off by macroalgae would have a definite advantage over other autotrophic algae.
In the Morocco P. parvum bloom, the water was high in organic matter, and
characterized by elevated levels of total nitrogen, limited concentrations
of nitrates and undetectable amounts of orthophosphates. This eutrophic, phosphorous-limiting
environment is believed to have lead to the extensive fish mortalities (Sabour
et al. 2000).
Wynne and Rhee (1988) found extracellular alkaline phosphatase activity to be highest in P. parvum when compared to the other species of algae tested. These authors discovered that phosphate uptake and enzyme activity increased with an increase in the N:P ratio, and concluded that this would give P. parvum a competitive advantage in phosphate-limited environments. They also determined that a decrease in phosphate concentrations was found to cause a disruption in the membrane synthesis of P. parvum that may lead to leakage of intercellular molecules including toxins.
Past studies indicate that vitamin B12 and thiamine are absolutely required for the growth of Prymnesium parvum (McLaughlin 1958, Shilo and Sarig 1989). Biotin was found not to be necessary for growth (McLaughlin 1958). Droop (1962) noted that thiamine is a component of the enzyme thiamine pyrophosphate (cocarboxylase), but no algae are known to be able to utilize the complete enzyme in place of thiamine as some bacteria do (the enzyme is probably less permeable). He found that P. parvum requires the pyrimidine component of thiamine, but does not require the thiazole component of thiamine. The author also noted that pyrimidine-requiring organisms require the molecule some 200 times more than vitamin B12. Another study indicates that with a given concentration of vitamin B12, growth in the light equals growth in the dark, and that this outcome may mean that B12 is not required for the immediate metabolism of the photosynthetic product (Rahat and Jahn 1965). Rahat and Reich (1963) discerned that a small portion of the B12 molecule is utilized in methyl metabolism for methionine or methyl group synthesis, and the rest of vitamin B12 (majority) used in other metabolic processes. They suggested that this may be why there is no sparing of B12 in the presence of methionine. The authors also found that some B12 analogs were found to inhibit the growth of P. parvum.
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