Toxicity and nutritional inadequacy of Karenia brevis: synergistic mechanisms disrupt top-down grazer control

Waggett, RJ; Hardison,; Tester, PA

doi:10.3354/meps09401

Cited by 48 publications

(60 citation statements)

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“…Competition experiments reveal that K. brevis produces allelopathic compounds, which inhibit the growth of competing phytoplankton and thereby help enable this slowgrowing species to dominate; however, brevetoxins themselves do not appear to be responsible for this inhibition (10,11). Recent studies support the hypothesis that brevetoxins serve as grazing deterrents, which promote population survival by decreasing grazing mortality rates (12)(13)(14), consistent with a classic defensive role for this neurotoxin. Furthermore, very recently published experiments show that limitation of growth rate by nitrogen and phosphorus increases cellular brevetoxin concentrations by two-to threefold, consistent with the behavior of other grazing defense toxins in terrestrial plants and phytoplankton (15)(16)(17)(18).…”

mentioning

confidence: 61%

“…Because the defensive function of toxic secondary metabolites in organisms is indisputable, it is often accepted that toxin production has largely evolved to defend prey against predators (e.g., 16,[34][35][36]. Within aquatic systems, there is substantial evidence in support of the evolution of chemical defenses (37,38), and this evidence extends to both macro-and microalgae (13,(39)(40)(41). As such, productive lines of inquiry regarding the function of brevetoxins not only should include how production changes with environmental factors but also must consider the role of biological interactions, especially those between phytoplankton and grazing organisms.…”

Section: Discussionmentioning

confidence: 99%

“…However, there is increasing evidence that brevetoxins promote the survival of K. brevis by deterring grazing by zooplankton (12)(13)(14). Studies investigating the functional role of toxins in organisms have a long history, and one that is deep-seated in terrestrial systems, including numerous terrestrial plants (e.g., 16,32,33).…”

Section: Discussionmentioning

confidence: 99%

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Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Sunda

Burleson

Hardison

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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With the global proliferation of toxic harmful algal bloom species, there is a need to identify the environmental and biological factors that regulate toxin production. One such species, Karenia brevis, forms nearly annual blooms that threaten coastal regions throughout the Gulf of Mexico. This dinoflagellate produces brevetoxins, which are potent neurotoxins that cause neurotoxic shellfish poisoning and respiratory illness in humans, as well as massive fish kills. A recent publication reported that a rapid decrease in salinity increased cellular toxin quotas in K. brevis and hypothesized that brevetoxins serve a role in osmoregulation. This finding implied that salinity shifts could significantly alter the toxic effects of blooms. We repeated the original experiments separately in three different laboratories and found no evidence for increased brevetoxin production in response to low-salinity stress in any of the eight K. brevis strains we tested, including three used in the original study. Thus, we find no support for an osmoregulatory function of brevetoxins. The original publication also stated that there was no known cellular function for brevetoxins. However, there is increasing evidence that brevetoxins promote survival of the dinoflagellates by deterring grazing by zooplankton. Whether they have other as-yet-unidentified cellular functions is currently unknown. red tides | toxic blooms | HABs H armful algal blooms threaten human health and damage coastal ecosystems worldwide. In the Gulf of Mexico, the athecate dinoflagellate Karenia brevis causes nearly annual toxic blooms. The physiology, ecology, and adverse effects of K. brevis have been well studied since the species was described in the 1940s (1). Notably, K. brevis produces brevetoxins, a family of potent polyether neurotoxins that bind to voltage-activated sodium channels in cell membranes, preventing normal nerve and muscle activity (2, 3). A nontoxic polyether that inhibits brevetoxin function, brevenal, is also produced in small amounts by this species (4). In humans, brevetoxins cause neurotoxic shellfish poisoning, and brevetoxin-contaminated aerosols cause respiratory irritation and illness (2, 5). Blooms also cause massive fish kills (6), as well as bird and marine mammal mortalities (7,8). In 2005, a bloom of K. brevis lasted for more than a year and caused extensive mortalities at all trophic levels in lagoons, coastal ecosystems, and offshore reefs on the west Florida shelf (8, 9).Because of the extensive damage caused by K. brevis, there has been considerable interest in understanding the function and regulation of brevetoxins. Competition experiments reveal that K. brevis produces allelopathic compounds, which inhibit the growth of competing phytoplankton and thereby help enable this slowgrowing species to dominate; however, brevetoxins themselves do not appear to be responsible for this inhibition (10, 11). Recent studies support the hypothesis that brevetoxins serve as grazing deterrents, which promote population survival by decrea...

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mentioning

confidence: 61%

Section: Discussionmentioning

confidence: 99%

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Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Sunda

Burleson

Hardison

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Under these conditions plants (including algae) divert some of the excess fixed carbon into C-based defensive compounds, such as toxins, to help alleviate this imbalance. This diversion serves two important functions: it protects the photosynthetic apparatus from overreduction and resulting oxidative stress (Niyogi 1999) until a balance between photosynthesis and growth can be achieved, and it decreases specific rates of grazing mortality (Hong et al 2012;Waggett et al 2012) to bring them more into line with the lower nutrient-limited specific rates of cellular growth and reproduction. Studies of N and P limitation of K. brevis have shown that, depending on the isolate, the percentage of the cell carbon pool invested in brevetoxins increases from 0.8% to 2.1% under nutrient sufficiency to 1.6-5.3% under growth limitation in accordance with predictions of the CNB hypothesis (Hardison et al , 2013.…”

Section: Discussionmentioning

confidence: 99%

“…The red tide dinoflagellate Karenia brevis produces a suite of polyether neurotoxins (brevetoxins) that serve as a potent grazing defense against copepods and likely other zooplankton (Cohen et al 2007;Hong et al 2012;Waggett et al 2012). Recent experiments have shown that growth rate limitation of K. brevis by nitrogen (N) and phosphorus (P) increase cellular brevetoxin (PbTx) concentrations (Hardison et al , 2013.…”

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confidence: 99%

Increased cellular brevetoxins in the red tide dinoflagellate Karenia brevis under CO₂ limitation of growth rate: Evolutionary implications and potential effects on bloom toxicity

Hardison¹,

Sunda²,

Tester³

et al. 2014

Limnology & Oceanography

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Karenia brevis blooms impair human health, marine ecosystems, and coastal economies in the Gulf of Mexico via their production of carbon-based neurotoxins (brevetoxins), which contain no nitrogen (N) or phosphorus (P). N and P limitation of growth rate substantially increases brevetoxins in this dinoflagellate, consistent with predictions of the carbon nutrient balance (CNB) hypothesis. This hypothesis further predicts that an increase in carbon-based brevetoxins should not occur if growth rate is limited by carbon dioxide (CO 2 ). We tested this prediction by examining the effect of CO 2 limitation of K. brevis growth rate on cellular brevetoxins. In contradiction to the prediction of the CNB hypothesis, brevetoxins normalized to cell carbon were on average 81% higher in CO 2 -limited cells growing at a rate of 0.1 d 21 than in cells growing at their maximum rates (0.4-0.5 d 21 ). This increase in brevetoxin : C values in the CO 2 -limited cells, however, was 23-42% lower than that previously observed for comparable growth rate limitation by phosphate. The CO 2 -limited cells also exhibited 40% higher cellular N : C and 60-100% higher chlorophyll a : C than observed in P-limited cells at equivalent growth rates. These effects were likely due to the up-regulation of the cell's CO 2 -concentrating mechanism under CO 2 limitation, which increased the demand for photosynthetically produced adenosine-59-triphosphate. The results indicate that anthropogenic increases in CO 2 concentrations in surface ocean waters are likely to increase the toxicity of K. brevis blooms due to potential increases in bloom biomass yield and to a greater likelihood that dense blooms will become N or P limited rather than CO 2 limited.

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Brevetoxin, the Dinoflagellate Neurotoxin, Localizes to Thylakoid Membranes and Interacts with the Light‐Harvesting Complex II (LHCII) of Photosystem II

et al. 2015

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The brevetoxins are neurotoxins that are produced by the "Florida red tide" dinoflagellate Karenia brevis. They bind to and activate the voltage-gated sodium channels in higher organisms, specifically the Nav 1.4 and Nav 1.5 channel subtypes. However, the native physiological function that the brevetoxins perform for K. brevis is unknown. By using fluorescent and photoactivatable derivatives, brevetoxin was shown to localize to the chloroplast of K. brevis where it binds to the light-harvesting complex II (LHCII) and thioredoxin. The LHCII is essential to non-photochemical quenching (NPQ), whereas thioredoxins are critical to the maintenance of redox homeostasis within the chloroplast and contribute to the scavenging of reactive oxygen. A culture of K. brevis producing low levels of toxin was shown to be deficient in NPQ and produced reactive oxygen species at twice the rate of the toxic culture, implicating a role in NPQ for the brevetoxins.

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Toxicity and nutritional inadequacy of Karenia brevis: synergistic mechanisms disrupt top-down grazer control

Cited by 48 publications

References 55 publications

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Increased cellular brevetoxins in the red tide dinoflagellate Karenia brevis under CO₂ limitation of growth rate: Evolutionary implications and potential effects on bloom toxicity

Brevetoxin, the Dinoflagellate Neurotoxin, Localizes to Thylakoid Membranes and Interacts with the Light‐Harvesting Complex II (LHCII) of Photosystem II

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Toxicity and nutritional inadequacy of Karenia brevis: synergistic mechanisms disrupt top-down grazer control

Cited by 48 publications

References 55 publications

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Increased cellular brevetoxins in the red tide dinoflagellate Karenia brevis under CO2 limitation of growth rate: Evolutionary implications and potential effects on bloom toxicity

Brevetoxin, the Dinoflagellate Neurotoxin, Localizes to Thylakoid Membranes and Interacts with the Light‐Harvesting Complex II (LHCII) of Photosystem II

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Increased cellular brevetoxins in the red tide dinoflagellate Karenia brevis under CO₂ limitation of growth rate: Evolutionary implications and potential effects on bloom toxicity