Variation in brevetoxin and brevenal content among clonal cultures of Karenia brevis may influence bloom toxicity

Errera, Reagan M.; Bourdelais, Andrea J.; Drennan, M.A.; Dodd, E.B.; Henrichs, Darren W.; Campbell, Lisa

doi:10.1016/j.toxicon.2009.07.013

Cited by 44 publications

(46 citation statements)

References 35 publications

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“…Next, we repeated the experiment with a clone of K. brevis (SP1) that produces very low quantities of brevetoxin (11). After rapid hypoosmotic stress, the average CSA of K. brevis SP1 cells increased from 931 ± 205 to 968 ± 208 μm 2 (SD; Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In addition, the unique ability of brevenal to compete with brevetoxin suggests that it may serve as a solution to aerosolized brevetoxins, and it has also been implicated as a therapy for cystic fibrosis (10). Unfortunately, K. brevis produces on average ∼1 pg per cell, which is only a fraction (∼6%) of the total brevetoxin concentration (11).…”

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confidence: 99%

“…Although a primary cellular function for toxins has remained elusive, responses to environmental conditions, such as salinity, have been shown to influence the growth potential and toxin production of harmful dinoflagellates (11,(19)(20)(21)(22)(23). These studies have examined the role of salinity in growth and toxin production on cells preacclimated to new environmental conditions (11,(19)(20)(21)(22)(23).…”

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confidence: 99%

“…These studies have examined the role of salinity in growth and toxin production on cells preacclimated to new environmental conditions (11,(19)(20)(21)(22)(23). Although these studies have identified the acclimated response to salinity, they do not evaluate differences in growth potential and toxin production in response to rapid shifts in salinity, as would occur when blooms move from oceanic to coastal conditions.…”

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confidence: 99%

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Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis

Errera¹,

Campbell

2011

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

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With the increase in frequency of harmful algal blooms (HABs) worldwide, a better understanding of the mechanisms that influence toxin production is needed. Karenia brevis , the major HAB dinoflagellate in the Gulf of Mexico, produces potent neurotoxins, known as brevetoxins. Human health is directly impacted by blooms of K. brevis through consumption of shellfish contaminated by accumulated brevetoxins (neurotoxic shellfish poisoning) or from aerosolized brevetoxins in sea spray (reduced respiratory function); however, the reason for brevetoxin production has remained a mystery. Here we show that brevetoxin production increased dramatically in response to osmotic stress in three of the four K. brevis clones examined. By rapidly changing salinity to simulate a shift from oceanic conditions to a decreased salinity typical of coastal conditions, brevetoxin production was triggered. As a result, brevetoxin cell quota increased by >14-fold, while growth rate remained unchanged. Live images of K. brevis cells were also examined to assess changes in cell volume. In the K. brevis Wilson clone, cells responded quickly to hypoosmotic stress by increasing their brevetoxin cell quota from ∼10 to 160 pg of brevetoxin per cell, while cell volume remained stable. In contrast, the K. brevis SP1 clone, which has a consistently low brevetoxin cell quota (<1 pg per cell), was unable to balance the hypoosmotic stress, and although brevetoxin production remained low, average cell volume increased. Our findings close a critical gap in knowledge regarding mechanisms for toxin production in K. brevis by providing an explanation for toxin production in this harmful dinoflagellate.

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Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis

Errera¹,

Campbell

2011

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

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“…On the basis of these results, these authors argued that osmoregulation may be the primary cellular function of brevetoxins and that salinity could be a major factor regulating brevetoxins in coastal waters. In previous, longer-term culture experiments from this same research group with the same strains, the authors also reported significantly higher toxin levels per cell for strain TBX4 grown at lower (27) than at higher (35) salinity; however, they reported the same toxin content for the Wilson strain at the two salinities and a sevenfold lower brevetoxin content per cell in strain SP3 grown at the lower salinity (24). This latter result is the opposite of the pattern reported by these authors for this strain in their subsequent short-term salinity stress experiments (22,23).…”

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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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Gene Mining for Environmental Studies and Applications: Examples from Marine Organisms

Dittami

Tonon

2014

Outstanding Marine Molecules

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In this chapter, some of the most common techniques used to generate genomic and transcriptomic data, that is, sequence and gene expression information, are reviewed. Examples are then given as to how these data can be exploited to understand the physiology of marine organisms. Emphasis is placed on studies conducted to gain insights on the response of corals to climate change (temperature and acidification), and on toxin production by dinoflagellates (dinotoxins). Finally, attention is focused on molecular biomonitoring techniques, and how sequence information can be used to assess the quality of food and the environment for the benefit of humans. The integration of genomic and transcriptomic data with other levels of analysis will lay the ground for a better understanding and exploitation of the potential of marine systems.

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Variation in brevetoxin and brevenal content among clonal cultures of Karenia brevis may influence bloom toxicity

Cited by 44 publications

References 35 publications

Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis

Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Gene Mining for Environmental Studies and Applications: Examples from Marine Organisms

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