{"title":"Introduction to the topical collection on harmful algal blooms","authors":"Dionysios Dionysiou, Nicole Blute, Triantafyllos Kaloudis, Lauren Weinrich, Arash Zamyadi","doi":"10.1002/aws2.1363","DOIUrl":null,"url":null,"abstract":"<p>Cyanobacteria, also known as blue-green algae, are prokaryotic photosynthetic microorganisms present in freshwater and water supply systems worldwide. They are asexual phytoplankton species with gram-negative cell walls, and their pigmentation can vary from blue-green to red.</p><p>The accumulation of many excessively buoyant cyanobacterial cells or colonies (scum) at the surface of water bodies is called a “bloom event” or “proliferation.” In extreme cases, such agglomeration may become very dense and even acquire a gelatinous consistency and sometimes even looks like blue-green paint or jelly. The nature of cyanobacterial proliferation is very dynamic, and bloom events are followed by a dying-off phase.</p><p>Fast increase or accumulation in the population of cyanobacteria or algae in water systems can lead to harmful algal blooms (HABs) accompanied by the production of toxins. These events are exacerbated by climate change and population growth. It should be noted that harmful blooms caused by cyanobacteria are called “cyano-HABs,” but here we use the term <i>HABs</i> to also include cyano-HABs as well.</p><p>Cyanobacteria have long been recognized for their nitrogen fixing capacity (the ability to convert atmospheric N<sub>2</sub> to NH<sub>3</sub>). It is estimated that they have been present in Earth's life cycle for more than 3.5 billion years. However, in the last 30 years, most of the literature covering cyanobacteria has focused on their ability to produce a variety of toxins responsible for intermittent but repeated, widespread poisoning of wild and domestic animals, aquaculture species and fish populations, and humans.</p><p>While many potentially toxic and/or nuisance species of cyanobacteria and their associated toxins have been detected, the mechanisms and drives for toxin production and release are not well understood. The increasing frequency and intensity of cyanobacterial proliferation leading to neurotoxin and hepatotoxin production is a problem for water utilities. The main toxins of interest are microcystins (e.g., MC-LR, MC-RR, MC-YR, MC-LA, MC-LW, MC-LF), nodularins, Anatoxin-a, Anatoxin-a(S), cylindrospermopsins, saxitoxins, aplysiatoxin, debromoaplysiatoxin, lyngbyatoxin-a, lipopolysaccharides, and most recently β-Methylamino-L-alanine. While microcystins such as MC-LR are the most frequently reported of the cyanobacterial toxins worldwide, other toxins are being detected more often than in the past, especially in more temperate climates.</p><p>Indeed, HABs can cause unpleasant taste and odor, which can decrease consumer confidence in the safety of their drinking water. Most often 2-methyl isoborneol (2-MIB) and geosmin, known for their signature earthy and musty odors, are the only two T&O compounds screened by laboratories in the United States. However, a range of compounds beyond those two can contribute to T&O issues. Less commonly studied classes, including sulfides, aldehydes, ketones, and pyrazines, can also be produced from algal and cyanobacterial blooms. Only scant information is available on the occurrence and treatment of other T&O-causing compounds and classes for drinking water utilities because historically we have lacked or not implemented methods to detect them in drinking water sources. However, recent research—including articles published in this issue—provides new guidance to fill the gaps in the development of novel methods for more comprehensive analysis of T&O compounds.</p><p>Efforts to prevent and manage HABs and their effects are underway around the world, but many challenges exist, especially for the management and mitigation of HABs in natural water systems (both freshwater and marine). Various physical, chemical, and biological methods are applied to mitigate or lessen the effects of HABs in these natural systems. On the other hand, physical (i.e., floatation, adsorption, and membranes) or chemical (ozone, oxidants, and advanced oxidation) processes are applied to remove cyanobacteria, cyanotoxins, and T&O metabolites in water treatment plants.</p><p>A study by Choo et al. (<span>2023a</span>) presented an extraordinary picture of cyanobacterial population changes over a 22-year time period in a 1 million sq km watershed in Australia. The effects of drought and wet periods revealed shifts from a watershed with predominantly one cyanobacterial species to a more heterogeneous cyanobacterial community, resulting in increases in T&O compounds. Treatability of cyanobacteria and T&O compounds over that time were assessed at 22 water treatment plants obtaining water from the Murray River. Results showed beneficial use of ultrafiltration–granular activated carbon treatment processes compared with conventional treatment.</p><p>Real-world observations of cyanobacteria blooms in a large lake in California provided observations of elevated microcystin concentrations and cyanobacteria presence with higher concentrations near the shoreline (dependent on intake level). Treatment of lake water by 18 public water systems (PWSs) using multibarrier treatment was compared with 35 self-supplied water system (SSWS) that serve individual houses with different point-of-use or point-of-entry treatment processes. Stanton et al. (<span>2023</span>) showed that PWSs effectively treated even peak microcystin concentrations, whereas SSWSs mostly exceeded the US Environmental Protection Agency's health advisory level of 0.3 μg/L. The study concluded that a combination of rapid bloom identification and effective treatment processes are needed to protect water quality for systems using sources vulnerable to algal blooms.</p><p>Nutrients in water bodies are critical to the growth of cyanobacteria that result in HABs. Nitrogen is known to be a primary nutrient fueling growth, but algal growth has also been linked to phosphorus, even though phosphorus is often present at lower concentrations. A comprehensive characterization of algal species behavior under different nutrient and temperature conditions, such as for microcystin-producing <i>Microcystis aeruginosa</i> PCC 7806, has been lacking. Jafarzadeh et al. (<span>2023</span>) built upon this knowledge by evaluating the physiological and genetic activities of <i>M. aeruginosa</i> by evaluating 16S rRNA gene abundance, cell growth and density, and toxin production under varying nitrogen-to-phosphorus ratios and temperatures. The goal of this study, in addition to advancing our understanding, is to ultimately anticipate and prevent toxin production based on gene expression measurements.</p><p>In another paper, Choo et al. (<span>2023b</span>) more closely evaluated the treatability of a cyanobacterial “challenge” characterized by high cyanobacterial numbers (>20,000 cells/mL) and high T&O compound concentrations (combined geosmin and methylisoborneol concentrations of >100 ng/L) at eight water treatment plants. An important finding from the analysis was that cyanobacterial growth within treatment plants can substantially add to the loading, such as from growth in the flocculation chambers and sludge lagoons. Most of the water treatment plants, however, were able to address their T&O challenges.</p><p>Adsorption with activated carbon is a treatment option for T&O compounds and was further investigated for a range of compound classes. Pochiraju et al. (<span>2022</span>) studied four types of powdered activated carbon (PAC), including bituminous-based, lignite-based, and wood-based. Variables also included contact times and mixing speeds for PAC doses ranging from 1 to 25 ppm (mg/L). The authors showed that PAC treatment was suitable for 15 T&O compounds with removals >90% with at least one of the PACs. In fact, the two bituminous-based PACs had the highest removal. It was also determined that lignite PAC was the most affected by the presence of organic matter in the river water. The results highlight the adsorptive capacity of PAC for various T&O compounds, thereby providing valuable insight to treatment plant operators. Considerations related to the compound's odor thresholds, adsorption behaviors, PAC characteristics, and NOM presence are featured for selecting the right adsorbents to help mitigate T&O issues in drinking water treatment plants.</p><p>Although treatment with PAC can be helpful for many of the compounds in these studies, the researchers also investigate whether oxidants used in water treatment for disinfection or abatement of micropollutants are effective for those classes. In the evaluations by Pochiraju et al. (<span>2023</span>), permanganate, chlorine, and ozone were applied. As a strong oxidant, ozone was able to completely oxidize half of the tested compounds with partial oxidation of the others. Chlorine and permanganate were effective for oxidizing aldehydes, ketones, and alkyl sulfides, but were not effective for anisoles, pyrazines, 2-MIB, and geosmin. The study found that the T&O compounds that were resistant to PAC adsorption were oxidizable by at least one or more of the oxidants studied. Furthermore, these studies underscore the need to understand the characteristics of different T&O compounds when considering treatment approaches.</p><p>While multiple oxidants are effective at removing microcystins in water treatment, research is underway to optimize oxidant usage to minimize disinfection by-products, decrease operational demands, and lower cost. Potassium permanganate has been identified as an oxidant of interest, but dissolved organic matter can affect its ability to oxidize microcystins. Hurd et al. (<span>2023</span>) presented an evaluation of a sequential permanganate dosing strategy to potentially decrease the competition of dissolved organic matter for permanganate oxidant, minimize cell lysis to avoid release of additional microcystins, and oxidize microcystins. Findings of this study concluded that sequential dosing was less effective at oxidizing microcystins compared with a single higher dose, but that this strategy may be effective in source waters with low concentrations of highly competitive organics.</p><p>Bohrerova et al. (<span>2023</span>) explored how a low-power ultrasound process that operates below the cell lysis cavitation threshold effected cyanobacteria cells, using <i>Serratia</i> sp. as surrogate organism as well as samples of blooms containing the cyanobacteria <i>Microcystis</i> sp. and <i>Aphanizomenon</i> sp. A low-energy physical process that doesn't use chemicals, low-power ultrasound can collapse cyanobacteria cell gas vesicles without causing cell lysis and the associated release of intracellular toxins. In their study, the authors evaluated how laboratory results compare with those obtained in controlled studies of HAB-affected water systems that use low-power ultrasound as a mitigation strategy. These results increase our understanding of how low-power ultrasound affects cyanobacterial cell physiology.</p><p>Accurate quantification of cyanotoxins in water plays a crucial role in meeting guideline values and regulations. Quantification relies on cyanotoxin standards, which are supplied by different vendors with varying specifications. In a study by Jia et al. (<span>2023</span>), the quality of 86 cyanotoxin standards from nine vendors was assessed using enzyme-linked immunosorbent assay (ELISA) and liquid chromatography/tandem mass spectrometry (LC–MS/MS). The findings revealed significant variations among vendors and lots, along with the identification of additional microcystin congeners in certain microcystin standards. Nevertheless, certified standards exhibited better agreement and reduced variation across all toxins. The study underscores the necessity for establishing standardized specifications and advocating for the certification of standards, aiming to enhance the consistency and comparability of results.</p><p>While LC–MS/MS is widely acknowledged as the current standard for cyanotoxin analysis, the simplicity and minimal instrument requirements of ELISA have led many laboratories to apply this method. To assess the comparability of results between LC–MS/MS and ELISA, Prescott et al. (<span>2023</span>) conducted interlaboratory comparisons involving 12 laboratories. This study encompassed 12 microcystin congeners, along with nodularin, anatoxin-a, and cylindrospermopsin. Overall, the outcomes revealed congruent results between ELISA and LC–MS/MS analyses. Notably, when accounting for microcystin cross-reactivities in ELISA, the results exhibited even closer alignment with those from LC–MS/MS. The study underscores the significance of considering cross-reactivities in ELISA data interpretation, particularly in relation to comparisons with LC–MS/MS findings.</p><p>The formation of HABs is a problem faced by many freshwater and marine systems. In addition to ecological toxicity and hypoxia affecting their ecologies, many other effects on water quality and aesthetics occur in various sectors including aquaculture, tourism, recreational activities, animal and human health, and the required processes and level of treatment by affected water utilities. Moreover, while cyanotoxin presence and concentration are a critical concern due to their high toxicity, the presence of T&O compounds is also a concern that affects public confidence in safe drinking water. This research effort identified a surprising disconnect between the importance of these issues for customer satisfaction and water quality and the tools available to proactively monitor, detect, and treat HABs.</p><p>A robust multibarrier approach is needed to understand, handle, and mitigate toxic and nontoxic HABs in the face of a changing climate, and warmer water temperatures will likely exacerbate algal growth around the globe. Many places might experience first-time events, and locations with known challenges may have more frequent or severe events. Tools are still needed to address the removal of cyanotoxins to lower concentrations in the presence of water quality changes such as increased organic content. The research in this topical collection from <i>AWWA Water Science</i> highlights recent advancements and areas of proposed research to prepare for and manage HABs to protect drinking water quality, critically linking the science to water utility operations.</p><p><b>Dionysios Dionysiou:</b> Writing – original draft. <b>Nicole Blute:</b> Writing – original draft. <b>Triantafyllos Kaloudis:</b> Writing – original draft. <b>Lauren Weinrich:</b> Writing – original draft. <b>Arash Zamyadi:</b> Writing – original draft.</p>","PeriodicalId":101301,"journal":{"name":"AWWA water science","volume":"6 1","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2024-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/aws2.1363","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"AWWA water science","FirstCategoryId":"1085","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/aws2.1363","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0
Abstract
Cyanobacteria, also known as blue-green algae, are prokaryotic photosynthetic microorganisms present in freshwater and water supply systems worldwide. They are asexual phytoplankton species with gram-negative cell walls, and their pigmentation can vary from blue-green to red.
The accumulation of many excessively buoyant cyanobacterial cells or colonies (scum) at the surface of water bodies is called a “bloom event” or “proliferation.” In extreme cases, such agglomeration may become very dense and even acquire a gelatinous consistency and sometimes even looks like blue-green paint or jelly. The nature of cyanobacterial proliferation is very dynamic, and bloom events are followed by a dying-off phase.
Fast increase or accumulation in the population of cyanobacteria or algae in water systems can lead to harmful algal blooms (HABs) accompanied by the production of toxins. These events are exacerbated by climate change and population growth. It should be noted that harmful blooms caused by cyanobacteria are called “cyano-HABs,” but here we use the term HABs to also include cyano-HABs as well.
Cyanobacteria have long been recognized for their nitrogen fixing capacity (the ability to convert atmospheric N2 to NH3). It is estimated that they have been present in Earth's life cycle for more than 3.5 billion years. However, in the last 30 years, most of the literature covering cyanobacteria has focused on their ability to produce a variety of toxins responsible for intermittent but repeated, widespread poisoning of wild and domestic animals, aquaculture species and fish populations, and humans.
While many potentially toxic and/or nuisance species of cyanobacteria and their associated toxins have been detected, the mechanisms and drives for toxin production and release are not well understood. The increasing frequency and intensity of cyanobacterial proliferation leading to neurotoxin and hepatotoxin production is a problem for water utilities. The main toxins of interest are microcystins (e.g., MC-LR, MC-RR, MC-YR, MC-LA, MC-LW, MC-LF), nodularins, Anatoxin-a, Anatoxin-a(S), cylindrospermopsins, saxitoxins, aplysiatoxin, debromoaplysiatoxin, lyngbyatoxin-a, lipopolysaccharides, and most recently β-Methylamino-L-alanine. While microcystins such as MC-LR are the most frequently reported of the cyanobacterial toxins worldwide, other toxins are being detected more often than in the past, especially in more temperate climates.
Indeed, HABs can cause unpleasant taste and odor, which can decrease consumer confidence in the safety of their drinking water. Most often 2-methyl isoborneol (2-MIB) and geosmin, known for their signature earthy and musty odors, are the only two T&O compounds screened by laboratories in the United States. However, a range of compounds beyond those two can contribute to T&O issues. Less commonly studied classes, including sulfides, aldehydes, ketones, and pyrazines, can also be produced from algal and cyanobacterial blooms. Only scant information is available on the occurrence and treatment of other T&O-causing compounds and classes for drinking water utilities because historically we have lacked or not implemented methods to detect them in drinking water sources. However, recent research—including articles published in this issue—provides new guidance to fill the gaps in the development of novel methods for more comprehensive analysis of T&O compounds.
Efforts to prevent and manage HABs and their effects are underway around the world, but many challenges exist, especially for the management and mitigation of HABs in natural water systems (both freshwater and marine). Various physical, chemical, and biological methods are applied to mitigate or lessen the effects of HABs in these natural systems. On the other hand, physical (i.e., floatation, adsorption, and membranes) or chemical (ozone, oxidants, and advanced oxidation) processes are applied to remove cyanobacteria, cyanotoxins, and T&O metabolites in water treatment plants.
A study by Choo et al. (2023a) presented an extraordinary picture of cyanobacterial population changes over a 22-year time period in a 1 million sq km watershed in Australia. The effects of drought and wet periods revealed shifts from a watershed with predominantly one cyanobacterial species to a more heterogeneous cyanobacterial community, resulting in increases in T&O compounds. Treatability of cyanobacteria and T&O compounds over that time were assessed at 22 water treatment plants obtaining water from the Murray River. Results showed beneficial use of ultrafiltration–granular activated carbon treatment processes compared with conventional treatment.
Real-world observations of cyanobacteria blooms in a large lake in California provided observations of elevated microcystin concentrations and cyanobacteria presence with higher concentrations near the shoreline (dependent on intake level). Treatment of lake water by 18 public water systems (PWSs) using multibarrier treatment was compared with 35 self-supplied water system (SSWS) that serve individual houses with different point-of-use or point-of-entry treatment processes. Stanton et al. (2023) showed that PWSs effectively treated even peak microcystin concentrations, whereas SSWSs mostly exceeded the US Environmental Protection Agency's health advisory level of 0.3 μg/L. The study concluded that a combination of rapid bloom identification and effective treatment processes are needed to protect water quality for systems using sources vulnerable to algal blooms.
Nutrients in water bodies are critical to the growth of cyanobacteria that result in HABs. Nitrogen is known to be a primary nutrient fueling growth, but algal growth has also been linked to phosphorus, even though phosphorus is often present at lower concentrations. A comprehensive characterization of algal species behavior under different nutrient and temperature conditions, such as for microcystin-producing Microcystis aeruginosa PCC 7806, has been lacking. Jafarzadeh et al. (2023) built upon this knowledge by evaluating the physiological and genetic activities of M. aeruginosa by evaluating 16S rRNA gene abundance, cell growth and density, and toxin production under varying nitrogen-to-phosphorus ratios and temperatures. The goal of this study, in addition to advancing our understanding, is to ultimately anticipate and prevent toxin production based on gene expression measurements.
In another paper, Choo et al. (2023b) more closely evaluated the treatability of a cyanobacterial “challenge” characterized by high cyanobacterial numbers (>20,000 cells/mL) and high T&O compound concentrations (combined geosmin and methylisoborneol concentrations of >100 ng/L) at eight water treatment plants. An important finding from the analysis was that cyanobacterial growth within treatment plants can substantially add to the loading, such as from growth in the flocculation chambers and sludge lagoons. Most of the water treatment plants, however, were able to address their T&O challenges.
Adsorption with activated carbon is a treatment option for T&O compounds and was further investigated for a range of compound classes. Pochiraju et al. (2022) studied four types of powdered activated carbon (PAC), including bituminous-based, lignite-based, and wood-based. Variables also included contact times and mixing speeds for PAC doses ranging from 1 to 25 ppm (mg/L). The authors showed that PAC treatment was suitable for 15 T&O compounds with removals >90% with at least one of the PACs. In fact, the two bituminous-based PACs had the highest removal. It was also determined that lignite PAC was the most affected by the presence of organic matter in the river water. The results highlight the adsorptive capacity of PAC for various T&O compounds, thereby providing valuable insight to treatment plant operators. Considerations related to the compound's odor thresholds, adsorption behaviors, PAC characteristics, and NOM presence are featured for selecting the right adsorbents to help mitigate T&O issues in drinking water treatment plants.
Although treatment with PAC can be helpful for many of the compounds in these studies, the researchers also investigate whether oxidants used in water treatment for disinfection or abatement of micropollutants are effective for those classes. In the evaluations by Pochiraju et al. (2023), permanganate, chlorine, and ozone were applied. As a strong oxidant, ozone was able to completely oxidize half of the tested compounds with partial oxidation of the others. Chlorine and permanganate were effective for oxidizing aldehydes, ketones, and alkyl sulfides, but were not effective for anisoles, pyrazines, 2-MIB, and geosmin. The study found that the T&O compounds that were resistant to PAC adsorption were oxidizable by at least one or more of the oxidants studied. Furthermore, these studies underscore the need to understand the characteristics of different T&O compounds when considering treatment approaches.
While multiple oxidants are effective at removing microcystins in water treatment, research is underway to optimize oxidant usage to minimize disinfection by-products, decrease operational demands, and lower cost. Potassium permanganate has been identified as an oxidant of interest, but dissolved organic matter can affect its ability to oxidize microcystins. Hurd et al. (2023) presented an evaluation of a sequential permanganate dosing strategy to potentially decrease the competition of dissolved organic matter for permanganate oxidant, minimize cell lysis to avoid release of additional microcystins, and oxidize microcystins. Findings of this study concluded that sequential dosing was less effective at oxidizing microcystins compared with a single higher dose, but that this strategy may be effective in source waters with low concentrations of highly competitive organics.
Bohrerova et al. (2023) explored how a low-power ultrasound process that operates below the cell lysis cavitation threshold effected cyanobacteria cells, using Serratia sp. as surrogate organism as well as samples of blooms containing the cyanobacteria Microcystis sp. and Aphanizomenon sp. A low-energy physical process that doesn't use chemicals, low-power ultrasound can collapse cyanobacteria cell gas vesicles without causing cell lysis and the associated release of intracellular toxins. In their study, the authors evaluated how laboratory results compare with those obtained in controlled studies of HAB-affected water systems that use low-power ultrasound as a mitigation strategy. These results increase our understanding of how low-power ultrasound affects cyanobacterial cell physiology.
Accurate quantification of cyanotoxins in water plays a crucial role in meeting guideline values and regulations. Quantification relies on cyanotoxin standards, which are supplied by different vendors with varying specifications. In a study by Jia et al. (2023), the quality of 86 cyanotoxin standards from nine vendors was assessed using enzyme-linked immunosorbent assay (ELISA) and liquid chromatography/tandem mass spectrometry (LC–MS/MS). The findings revealed significant variations among vendors and lots, along with the identification of additional microcystin congeners in certain microcystin standards. Nevertheless, certified standards exhibited better agreement and reduced variation across all toxins. The study underscores the necessity for establishing standardized specifications and advocating for the certification of standards, aiming to enhance the consistency and comparability of results.
While LC–MS/MS is widely acknowledged as the current standard for cyanotoxin analysis, the simplicity and minimal instrument requirements of ELISA have led many laboratories to apply this method. To assess the comparability of results between LC–MS/MS and ELISA, Prescott et al. (2023) conducted interlaboratory comparisons involving 12 laboratories. This study encompassed 12 microcystin congeners, along with nodularin, anatoxin-a, and cylindrospermopsin. Overall, the outcomes revealed congruent results between ELISA and LC–MS/MS analyses. Notably, when accounting for microcystin cross-reactivities in ELISA, the results exhibited even closer alignment with those from LC–MS/MS. The study underscores the significance of considering cross-reactivities in ELISA data interpretation, particularly in relation to comparisons with LC–MS/MS findings.
The formation of HABs is a problem faced by many freshwater and marine systems. In addition to ecological toxicity and hypoxia affecting their ecologies, many other effects on water quality and aesthetics occur in various sectors including aquaculture, tourism, recreational activities, animal and human health, and the required processes and level of treatment by affected water utilities. Moreover, while cyanotoxin presence and concentration are a critical concern due to their high toxicity, the presence of T&O compounds is also a concern that affects public confidence in safe drinking water. This research effort identified a surprising disconnect between the importance of these issues for customer satisfaction and water quality and the tools available to proactively monitor, detect, and treat HABs.
A robust multibarrier approach is needed to understand, handle, and mitigate toxic and nontoxic HABs in the face of a changing climate, and warmer water temperatures will likely exacerbate algal growth around the globe. Many places might experience first-time events, and locations with known challenges may have more frequent or severe events. Tools are still needed to address the removal of cyanotoxins to lower concentrations in the presence of water quality changes such as increased organic content. The research in this topical collection from AWWA Water Science highlights recent advancements and areas of proposed research to prepare for and manage HABs to protect drinking water quality, critically linking the science to water utility operations.
Dionysios Dionysiou: Writing – original draft. Nicole Blute: Writing – original draft. Triantafyllos Kaloudis: Writing – original draft. Lauren Weinrich: Writing – original draft. Arash Zamyadi: Writing – original draft.