Disinfection By-products (DBP) formed during chlorination in drinking water treatment process pose great threats to the public health and safety, since most DBPs, such as chloroform and trihalomethane (THM), are carcinogens (1). It has been well believed that the natural organic matter (NOM) present in lakes and reservoirs severs as a precursor for by-product formation during chlorination (2). Therefore, understanding the sources of NOM in lakes and its cycle in ecosystem is of great importance to the DBP control.
Studies have shown that dissolved organic carbon (DOC) released by phytoplankton is one of the main sources of NOM in surface water (3, 4). These extracellular compounds include carbohydrates, polysaccharides, proteins, long-chain lipids and amino acids. It is reported that up to 50% of photosynthetically fixed carbon can be released by phytoplankton to water column (5). Also, the rate at which the DOC is released depends on the growing phase of the cells, the limitation on nutrients, and the specific species of the phytoplankton. Meanwhile, these high molecular-weight DOC compounds can also be uptaken by bacteria, and hence decrease the amount of DBP precursors (6). This paper is aimed to summarize the biological mechanisms to produce DOC by phytoplankton, analyze the consequently potential risks of forming disinfection by-products, and provide a better understanding of the sources of DBP precursors.
3. The composition of DOC produced by phytoplankton
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Phytoplankton mainly produce DOC compounds into water column by releasing the photosynthetically fixed carbon compounds out of their cells. For example, three lakes in Sweden showed that the DOC produced by phytoplankton can be classified as "high-molecule-weight compound (>10,000), low-molecule-weight compounds (<1,000), and intermediate-molecule-weight compounds" (7). Of the three categories, the intermediate-molecule-weight compounds were dominant. For the high molecule-weight compounds, carbohydrates and nucleic acids were the major species. For the intermediate molecule-weight compounds, polysaccharides accounted for the most percentage. For the low molecule-weight compounds, organic acids were dominant through summer to autumn. These organic acids mostly contained carboxyl functional groups, alcohol groups and amino groups. A closer examination revealed that cyanobacteria, mainly Microcystis, dominated the phytoplankton communities in these lakes (8).
In other studies, it was found that polysaccharides composed 33% of total DOC, and monosaccharides composed 15% of total DOC produced (9). One notable point is that the release of DOC is not a simple process of cell leakage of phytoplankton, and there is no direct relationship between cellular and extracellular DOC composition (10). This indicates special mechanisms other than cells breakdown play important roles in the DOC production.
4. The Mechanisms on DOC production by phytoplankton
As mentioned above, cell breakdowns release cellular DOC into water column. However, this process is not sufficient to explain all the DOC data found in lakes or data from culture study. It was suggested that the production of extracellular DOC was a function of phytoplankton biomass and the growth rates.
4.1 Passive diffusion across cell membrane
The first mechanism is called passive diffusion (11, 12). When the phytoplankton grow, their cells accumulate organic compounds as a net result of photosynthesis. These organic compounds within the cell are raw materials to synthesize proteins, enzymes and build cell structures. As more organic compounds are accumulated in the cell, higher concentration gradient is built up across the cell membrane. Therefore, dissolved organic compounds are diffused across the membrane in regardless of other cell activities. Any factors impacting the diffusion process attributes to the DOC production. Given this mechanism, the more the phytoplankton biomass it is, the more the cells are, and the larger the cell membrane surface areas are, and consequently the more DOC production it will be.
The passive diffusion mechanism predicts higher primary production creates higher DOC concentration in lakes. In one study summarizing 25 lakes in Europe and Unite States, it was found that the extracellular DOC concentration and primary production exhibited a linear relationship on log scale (12). However, this mechanism is not sufficient to explain the high molecule-weight compounds released by cells, because these large molecules can't pass the cell membrane simply through diffusion. Furthermore, reports showed that the percentage of DOC released out of cells varies in different phases of phytoplankton growth. For example, one diatom Skeletonema costatum only releases 4% of photosynthetically fixed carbon in exponential growth phase, but releases 14% to 65% of fixed carbon in stationary phase. These results indicate some other mechanisms involved (13).
4.2 Active excretion of DOC by phytoplankton
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This mechanism of releasing DOC differs from the passive diffusion in that the live cells control the excretion rate. It's analogous to say that phytoplankton cells can sensor the availability of fixed carbon and its actual demand. This excretion process was also proposed to be an "overflow mechanism for carbon sink" (10). This is because when the cells have more rapid rate on photosynthesis than it is required to growth, the oversupplied organic compounds couldn't be utilized, and they are disposed by phytoplankton.
Based on this mechanism, it can be expected that the amount of DOC excreted by a single cell varies in time. When the cell is new and has high growth rate, the demand for fixed carbon is very high in order to build the cell structure. So no extra carbon is wasted by the cell, and DOC release rate is slow. On the contrary, when the cell overpasses the maximal growth rate, carbon fixed from photosynthesis can not be totally utilized, so the cell excretes DOC out of the cell. There were reports showing the quick increase of DOC release when the phytoplankton switched from exponential growth phase to stationary phase (14). Amino acids, glucan and polysaccharides were identified as the main composition in some cases (15).
Furthermore, the rate at which DOC is excreted depends on the limitation of the nutrients. In one batch culture study (16), the diatom Chaetoceros affinis excreted at a 30% higher rate when nitrogen was limited (nitrogen to phosphorous ration was 5), and excreted at a 100% higher rate when phosphorous was limited (N to P ratio is 100), respectively, than in Redfield ratio. It also showed that the limitation on nutrient increased the "carbohydrate release during the exponential growth phase of diatom Cylindrotheca closterium (17). This can also be explained by the active excretion mechanism. When the nutrient is limited, the cell growth is decreased, and extra fixed carbon becomes more than needed. So the cell will excrete these DOC. Recently, some studies examined the specific enzymes involved in this process (18). It was reported that in the diatom Thalassiosira weissflogii, a protease was activated by N limitation, which initiated the release of DOC.
4.3 Bacteria uptake of DOC released by phytoplankton
A lot of studies focusing on the outcomes of DOC released by phytoplankton were to explore its bioavailability to heterotrophic bacteria (19, 20). There were few researches focusing on the potential risks to form disinfection by-products (DBP) as an outcome. However, the consequent uptake of DOC by bacteria is an indirect pathway to reduce the amount of DBP precursors, since this mechanism cycles the DOC to bacteria, and DOC will be eventually broken down by the heterotrophs to inorganic CO2. Therefore, the bioavailability of DOC can be an important indicator for the potential amount of DBP precursors, with higher bioavailability resulting in lower potential DBP precursors.
Heterotrophic bacteria can uptake as much as half of their carbon source from DOC released by phytoplankton (21). Experiments using 14C labelled carbon showed low and intermediate molecule-weight compounds, such as polysaccharides, amino acid and peptides, are more bioavailable to bacteria (7). Also, the rate of bacteria uptake was believed to be very fast, with the activity of bacteria extracellular enzymes. Some studies also showed the bacteria maximal yields were about three times higher in media added with phytoplankton excreta than in normal glucose media (6). These results indicated the substantial uptake of DOC compounds from phytoplankton.
5. Assess the potential risks of DBP formation by phytoplankton DOC release
Based on mechanisms illustrated in section 4, on one hand, phytoplankton can release various types of DOC compounds into lake system. On the other hand, whether these compounds have direct links to DBP formation is a question to investigate. DBP formation during chlorination depends on two factors: one is the concentration of DOC; the other is related to their characteristics. This means that knowing the concentration of DOC released by phytoplankton is only the first step. Analysis on the DOC prosperities is the ultimate point to assess the risks on drinking water safety. For example, the molecules of polysaccharides and organic acids contain different functional groups. Each functional group has different kinetics to reacts with chlorine, resulting in different final by-products. Released amino acids lead to the formation of toxic dichloroacetonitriles, while the small organic acid can form trihalomethane or haloacetic acids (22). Even in cases where the total concentrations of phytoplankton DOC release are the same, the portion of different functional groups can vary very much.
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Furthermore, bacteria uptake of DOC also impacts the composition of remaining DOC in lakes, which impacts the DBP formation potentials. Study on a tropic reservoir showed that some bacteria were able to uptake DOC selectively, and left deoxy sugars in the water column, which increased the portion of hydrophobic carbon compounds (23). Since the coagulation process in drinking water treatment prior to chlorination has higher removal efficiency on the hydrophobic compounds, less DBPs are supposed to form.
However, few studies were carried out to exam the direct chlorination of these DOC compounds released by phytoplankton. Only data on this relationship is established can the risks to form DBP as a result of phytoplankton activity be better assessed.
Phytoplankton can release dissolved organic carbon (DOC) compounds in lakes and reservoirs. These compounds include carbohydrates, polysaccharides, amino acids, and nucleic acids and so on. Because of the presence of carboxyl, amino, alcohol and other functional groups in these molecules, they are potential precursors of disinfection by-products (DBPs), which impact the drinking water safety. Three mechanisms contribute to the released process. First, The passive diffusion controls the released of DOC across cell membrane as a result of concentration gradients. It predicts the release rate is determined by the phytoplankton primary production. Second, the active excretion is caused by the oversupply of photosynthetically fixed carbon and serves as a way to dispose the extra carbon compounds out of the cell. During nutrient limitation and in stationary growth phase, more DOC compounds were observed to be released by phytoplankton. Third, some heterotrophic bacteria can uptake the DOC compounds from phytoplankton, change their composition and potentials to be DBP precursors.
Based on these mechanisms, the risks to form DBP from phytoplankton DOC release need to be ascertained in a direct way. Researches on the chlorination reaction of these phytoplanktonic released chemicals are suggested be carried out. Another important point to explore is the seasonal pattern and depth profile of DOC release activity in lakes. Data on this field can give a guide on the usage of these lakes as drinking water resources in the future.
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