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The Green Macroalga, Ulva lactuca, Inhibits the Growth of Seven Common Harmful Algal Bloom Species via Allelopathy
Harmful algal blooms (HABs) are a significant threat to fisheries, public health, and economies around the world, and both HABs and macroalgae are often promoted by nutrient loading. We report on experiments examining the effects of the macroalga, Ulva lactuca, collected from estuaries of NY, USA, on the growth of seven common HAB species:
Aureococcus anophagefferens,
Chattonella marina,
Cochlodinium polykrikoides,
Karlodinium veneficum,
Karenia brevis,
Prorocentrum minimum
Pseudo-Nitzschia multiseries.
Fresh thalli of U. lactuca added at environmentally realistic levels (mg L−1) were capable of lysing or strongly inhibiting the growth of all seven HAB species in a dose-dependent manner within controlled laboratory experiments during which high nutrient levels, low bacterial levels, and common pH levels among treatments and controls were maintained. The dramatic allelopathic effects of extracts of dried and powdered U. lactuca with and without post-extraction heat treatment on the HAB species demonstrated that U. lactuca contains heat-stable allelochemicals that play a major role in the observed allelopathic effects. The addition of live U. lactuca thalli in bottle and mesocosm experiments conducted in the field during blooms of A. anophagefferens (‘brown tide’; >105 cells mL−1) consistently yielded a significant (p < 0.05) and often large (>50%) reduction in cell densities in ∼48 h. Our findings combined with the well-known nutrient removal capacity of seaweeds collectively suggest that the use of macroalgae may be a promising mitigation strategy for HABs in coastal ecosystems.
Highlights
► Ulva lactuca lysed or strongly inhibited seven HAB species.
► HAB inhibition was due to allelochemicals, not changes in bacteria, nutrients, or pH.
► U. lactuca reduced Aureococcus anophagefferens densities during blooms.
► Macroalgae may be a promising mitigation strategy for HABs.
Aureococcus anophagefferens is a species of heterokont alga. Its cells have a single chloroplast, nucleus, and mitochondrion and an unusual exocellular polysaccharide-like layer. It causes harmful algal blooms.
The heterokonts or stramenopiles are a major line of eukaryotes currently containing more than 25,000 known species. Most are algae, ranging from the giant multicellular kelp to the unicellular diatoms, which are a primary component of plankton. Other notable members of the Stramenopiles include the (generally) parasitic oomycetes, including Phytophthora of Irish potato famine infamy and Pythium which causes seed rot and damping off.
Chattonella marina. Chattonella is a genus of marine raphidophytes associated with red tides.[1] A technique using monoclonal antibodies can be used to identify the genus, while the RAPD reaction can be used to distinguish between different species within the genus. It includes the species Chattonella antiqua, a bloom forming alga responsible for large scale fish deaths due to the synthesis of toxic compounds related to brevetoxin.
Brevetoxin (PbTx), or brevetoxins, are a suite of cyclic polyether compounds produced naturally by a species of dinoflagellate known as Karenia brevis. Brevetoxins are neurotoxins that bind to voltage-gated sodium channels in nerve cells, leading to disruption of normal neurological processes and causing the illness clinically described as neurotoxic shellfish poisoning (NSP)
Cochlodinium polykrikoides is a species of red tide producing marine dinoflagellates known for causing fish kills around the world, and well known for fish kills in marine waters of Southeast Asia.
Cochlodinium polykrikoides is a highly motile organism. They are generally found in aggregations of 4 or 8 cell zooids. Cochlodinium polykrikoides is capable of mix trophy, which makes them extremely persistent during a large algal bloom. Cochlodinium is thought to have a cyst-type overwintering stage in their life cycle. This process allows C. polykrikoides to produce a specialized cell that is non-motile. These cells aggregate and rest in certain basins until conditions allow for reproduction and colonies to form.
Karlodinium veneficum is part of the Eukarya domain and a marine planktonic dinoflagellate found in oceans and estuaries all around the world. It is a photosynthetic species that contains multiple chloroplasts.
Gymnodinium veneficum was originally named and discovered by Mary Parke and D. Ballantine in 1956. It was found to be very closely related to Gymnodinium vitiligo, due to its small size and similar structural characteristics. The most distinct difference between G. veneficum and G. vilitgo was that, G. veneficum produced and released toxins. After more research was performed on this particular species, the genus name was changed from Gymnodinium to Karlodinium. The species was renamed Karlodinium veneficum due to the discovery of harmful toxins produced by this species which has been known to cause harmful algae blooms and kill fish in marine ecosystems . Multiple articles including Algaebase (which is a database of information on algae that includes terrestrial, marine and freshwater organisms) have stated that Karlodinium micrum is a taxonomic synonym of Karlodinium veneficum. In the article by Bergholtz et al. 2005, it was stated that K. micrum should be changed to K. veneficum due to the fact that they are identical in size, both have golden brown chloroplasts with pyrenoids and an epicone (part that is located near the apical groove in dinoflagellate) present.
Karenia brevis is a microscopic, single-celled, photosynthetic organism that is part of the Karenia (dinoflagellate) genus, a marine dinoflagellate commonly found in the waters of the Gulf of Mexico. It is the organism responsible for the "Florida Red Tides" (coastal infestations), commonly referred to as red tides that affect the Gulf coasts of Florida and Texas in the U.S., and nearby coasts of Mexico. K. brevis has been known to travel great lengths around the Florida peninsula and as far north as the Carolinas.
Each cell has two flagella that allow it to move through the water in a spinning motion. K. brevis is unarmored, and does not contain peridinin. Cells are between 20 and 40 μm in diameter. K. brevis naturally produces a suite of potent neurotoxins collectively called brevetoxins, which cause gastrointestinal and neurological problems in other organisms and are responsible for large die-offs of marine organisms and seabirds.
Prorocentrum minimum is an armoured, marine, planktonic, bloom-forming dinoflagellate. It is a toxic cosmopolitan species common in cold temperate brackish waters to tropical regions.
P. minimum is a toxic species; it produces venerupin (hepatotoxin) which has caused shellfish poisoning resulting in gastrointestinal illnesses in humans and a number of deaths. This species is also responsible for shellfish kills in Japan and the Gulf of Mexico, Florida (Nakazima, 1965, Nakazima, 1968, Okaichi and Imatomi, 1979, Tangen, 1983, Shimizu, 1987, Smith, 1975, Steidinger and Tangen, 1996).
Pseudo-Nitzschia multiseries is a marine planktonic diatom genus containing some species capable of producing the neurotoxin domoic acid (DA), which is responsible for the neurological disorder known as amnesic shellfish poisoning (ASP). Currently, 51 species are known, 26 of which have been shown to produced DA. It was originally hypothesized that only dinoflagellates could produce harmful algal toxins, but a deadly bloom of Pseudo-nitzschia occurred in 1987 in the bays of Prince Edward Island, Canada, and led to an outbreak of ASP.[2] Over 100 people were affected by this outbreak after consuming contaminated mussels; three people died.[3] Blooms have since been characterized in coastal waters worldwide and have been linked to increasing marine nutrient concentrations.
Harmful algal blooms (HABs) are a significant threat to fisheries, public health, and economies around the world, and both HABs and macroalgae are often promoted by nutrient loading. We report on experiments examining the effects of the macroalga, Ulva lactuca, collected from estuaries of NY, USA, on the growth of seven common HAB species:
Aureococcus anophagefferens,
Chattonella marina,
Cochlodinium polykrikoides,
Karlodinium veneficum,
Karenia brevis,
Prorocentrum minimum
Pseudo-Nitzschia multiseries.
Fresh thalli of U. lactuca added at environmentally realistic levels (mg L−1) were capable of lysing or strongly inhibiting the growth of all seven HAB species in a dose-dependent manner within controlled laboratory experiments during which high nutrient levels, low bacterial levels, and common pH levels among treatments and controls were maintained. The dramatic allelopathic effects of extracts of dried and powdered U. lactuca with and without post-extraction heat treatment on the HAB species demonstrated that U. lactuca contains heat-stable allelochemicals that play a major role in the observed allelopathic effects. The addition of live U. lactuca thalli in bottle and mesocosm experiments conducted in the field during blooms of A. anophagefferens (‘brown tide’; >105 cells mL−1) consistently yielded a significant (p < 0.05) and often large (>50%) reduction in cell densities in ∼48 h. Our findings combined with the well-known nutrient removal capacity of seaweeds collectively suggest that the use of macroalgae may be a promising mitigation strategy for HABs in coastal ecosystems.
Highlights
► Ulva lactuca lysed or strongly inhibited seven HAB species.
► HAB inhibition was due to allelochemicals, not changes in bacteria, nutrients, or pH.
► U. lactuca reduced Aureococcus anophagefferens densities during blooms.
► Macroalgae may be a promising mitigation strategy for HABs.
Aureococcus anophagefferens is a species of heterokont alga. Its cells have a single chloroplast, nucleus, and mitochondrion and an unusual exocellular polysaccharide-like layer. It causes harmful algal blooms.
The heterokonts or stramenopiles are a major line of eukaryotes currently containing more than 25,000 known species. Most are algae, ranging from the giant multicellular kelp to the unicellular diatoms, which are a primary component of plankton. Other notable members of the Stramenopiles include the (generally) parasitic oomycetes, including Phytophthora of Irish potato famine infamy and Pythium which causes seed rot and damping off.
Chattonella marina. Chattonella is a genus of marine raphidophytes associated with red tides.[1] A technique using monoclonal antibodies can be used to identify the genus, while the RAPD reaction can be used to distinguish between different species within the genus. It includes the species Chattonella antiqua, a bloom forming alga responsible for large scale fish deaths due to the synthesis of toxic compounds related to brevetoxin.
Brevetoxin (PbTx), or brevetoxins, are a suite of cyclic polyether compounds produced naturally by a species of dinoflagellate known as Karenia brevis. Brevetoxins are neurotoxins that bind to voltage-gated sodium channels in nerve cells, leading to disruption of normal neurological processes and causing the illness clinically described as neurotoxic shellfish poisoning (NSP)
Cochlodinium polykrikoides is a species of red tide producing marine dinoflagellates known for causing fish kills around the world, and well known for fish kills in marine waters of Southeast Asia.
Cochlodinium polykrikoides is a highly motile organism. They are generally found in aggregations of 4 or 8 cell zooids. Cochlodinium polykrikoides is capable of mix trophy, which makes them extremely persistent during a large algal bloom. Cochlodinium is thought to have a cyst-type overwintering stage in their life cycle. This process allows C. polykrikoides to produce a specialized cell that is non-motile. These cells aggregate and rest in certain basins until conditions allow for reproduction and colonies to form.
Karlodinium veneficum is part of the Eukarya domain and a marine planktonic dinoflagellate found in oceans and estuaries all around the world. It is a photosynthetic species that contains multiple chloroplasts.
Gymnodinium veneficum was originally named and discovered by Mary Parke and D. Ballantine in 1956. It was found to be very closely related to Gymnodinium vitiligo, due to its small size and similar structural characteristics. The most distinct difference between G. veneficum and G. vilitgo was that, G. veneficum produced and released toxins. After more research was performed on this particular species, the genus name was changed from Gymnodinium to Karlodinium. The species was renamed Karlodinium veneficum due to the discovery of harmful toxins produced by this species which has been known to cause harmful algae blooms and kill fish in marine ecosystems . Multiple articles including Algaebase (which is a database of information on algae that includes terrestrial, marine and freshwater organisms) have stated that Karlodinium micrum is a taxonomic synonym of Karlodinium veneficum. In the article by Bergholtz et al. 2005, it was stated that K. micrum should be changed to K. veneficum due to the fact that they are identical in size, both have golden brown chloroplasts with pyrenoids and an epicone (part that is located near the apical groove in dinoflagellate) present.
Karenia brevis is a microscopic, single-celled, photosynthetic organism that is part of the Karenia (dinoflagellate) genus, a marine dinoflagellate commonly found in the waters of the Gulf of Mexico. It is the organism responsible for the "Florida Red Tides" (coastal infestations), commonly referred to as red tides that affect the Gulf coasts of Florida and Texas in the U.S., and nearby coasts of Mexico. K. brevis has been known to travel great lengths around the Florida peninsula and as far north as the Carolinas.
Each cell has two flagella that allow it to move through the water in a spinning motion. K. brevis is unarmored, and does not contain peridinin. Cells are between 20 and 40 μm in diameter. K. brevis naturally produces a suite of potent neurotoxins collectively called brevetoxins, which cause gastrointestinal and neurological problems in other organisms and are responsible for large die-offs of marine organisms and seabirds.
Prorocentrum minimum is an armoured, marine, planktonic, bloom-forming dinoflagellate. It is a toxic cosmopolitan species common in cold temperate brackish waters to tropical regions.
P. minimum is a toxic species; it produces venerupin (hepatotoxin) which has caused shellfish poisoning resulting in gastrointestinal illnesses in humans and a number of deaths. This species is also responsible for shellfish kills in Japan and the Gulf of Mexico, Florida (Nakazima, 1965, Nakazima, 1968, Okaichi and Imatomi, 1979, Tangen, 1983, Shimizu, 1987, Smith, 1975, Steidinger and Tangen, 1996).
Pseudo-Nitzschia multiseries is a marine planktonic diatom genus containing some species capable of producing the neurotoxin domoic acid (DA), which is responsible for the neurological disorder known as amnesic shellfish poisoning (ASP). Currently, 51 species are known, 26 of which have been shown to produced DA. It was originally hypothesized that only dinoflagellates could produce harmful algal toxins, but a deadly bloom of Pseudo-nitzschia occurred in 1987 in the bays of Prince Edward Island, Canada, and led to an outbreak of ASP.[2] Over 100 people were affected by this outbreak after consuming contaminated mussels; three people died.[3] Blooms have since been characterized in coastal waters worldwide and have been linked to increasing marine nutrient concentrations.
