Toxigenic Pfiesteria species—Updates on biology, ecology, toxins, and impacts

Burkholder, JoAnn M.; Marshall, Harold G.

doi:10.1016/j.hal.2011.10.022

Cited by 28 publications

(11 citation statements)

References 247 publications

(445 reference statements)

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“…Our findings contrast with those of Errera and Campbell (22,23), who reported that "brevetoxin production increased in response to low salinity stress." Because of the substantial adverse effects of K. brevis and brevetoxins in the Gulf of Mexico and a desire to understand their regulation, Errera and Campbell's reported findings have garnered much attention from researchers (e.g., [25][26][27], as well as media outlets, but we found that their reported findings are not reproducible. Furthermore, their claims that they "close a critical gap in knowledge" are unsubstantiated.…”

Section: Discussionmentioning

confidence: 70%

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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Section: Discussionmentioning

confidence: 70%

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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“…Our results show that Pfiesteria piscicida expresses numerous genes involved in metabolic pathways of plastids despite it not having any sub-cellular membranous structure assignable to plastids [29]. The heterogeneous origins of the plastid genes (especially the genes directly related to photosynthesis) suggest that P. piscicida had experienced multiple endosymbioses, both from a secondary plastid (grouping with peridinin-containing dinoflagellate lineages) and at least one tertiary endosymbiosis (grouping with diatoms that have formed endosymbioses with dinoflagellates).…”

Section: Discussionmentioning

confidence: 85%

“…P. piscicida has been studied over the last 20 years as it is involved in fish deaths. While some aspects of its biology (life cycle and toxicity) are still controversial [28], [29], it is clear that P. piscicida is not photosynthetic and a TEM study could not find any membranous structures assignable as plastids [29]. P. piscicida has been implicated as being kleptoplastidic when it feeds upon cryptophyte algae as they have been shown to persist in vacuoles of starved P. piscicida for a week, apparently fixing carbon and accumulating starch [30].…”

Section: Introductionmentioning

confidence: 99%

Still Acting Green: Continued Expression of Photosynthetic Genes in the Heterotrophic Dinoflagellate Pfiesteria piscicida (Peridiniales, Alveolata)

et al. 2013

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The loss of photosynthetic function should lead to the cessation of expression and finally loss of photosynthetic genes in the new heterotroph. Dinoflagellates are known to have lost their photosynthetic ability several times. Dinoflagellates have also acquired photosynthesis from other organisms, either on a long-term basis or as “kleptoplastids” multiple times. The fate of photosynthetic gene expression in heterotrophs can be informative into evolution of gene expression patterns after functional loss, and the dinoflagellates ability to acquire new photosynthetic function through additional endosymbiosis. To explore this we analyzed a large-scale EST database consisting of 151,091 unique sequences (29,170 contigs, 120,921 singletons) obtained from 454 pyrosequencing of the heterotrophic dinoflagellate Pfiesteria piscicida. About 597 contigs from P. piscicida showed significant homology (E-value

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“…Particularly, the considerable number of so far unknown Pfiesterialike sequences (Burkholder & Marshall, 2012;Calado, Craveiro, Daugbjerg, & Moestrup, 2009;Litaker et al, 2005) is impressive. A targeted search in future will assess this diversity and address questions, such as whether these are already accepted species without hitherto known DNA sequence information or even new species.…”

Section: Discussionmentioning

confidence: 99%

Phylogenetic placement of environmental sequences using taxonomically reliable databases helps to rigorously assess dinophyte biodiversity in Bavarian lakes (Germany)

et al. 2019

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1. Reliable determination of organisms is a prerequisite to explore their spatial and temporal occurrence and to study their evolution, ecology, and dispersal. In Europe, Bavaria (Germany) provides an excellent study system for research on the origin and diversification of freshwater organisms including dinophytes, due to the presence of extensive lake districts and ice age river valleys. Bavarian freshwater environments are ecologically diverse and range from deep nutrient-poor mountain lakes to shallow nutrient-rich lakes and ponds.2. We obtained amplicon sequence data (V4 region of small subunit-rRNA, c. 410 bp long) from environmental samples collected at 11 sites in Upper Bavaria. We found 186 operational taxonomic units (OTUs) associated with Dinophyceae that were further classified by means of a phylogenetic placement approach.3. The maximum likelihood tree inferred from a well-curated reference alignment comprised a systematically representative set of 251 dinophytes, covering the currently known molecular diversity and OTUs linked to type material if possible. Environmental OTUs were scattered across the reference tree, but accumulated mostly in freshwater lineages, with 79% of OTUs placed in either Apocalathium, Ceratium, or Peridinium, the most frequently encountered taxa in Bavaria based on morphology.4. Twenty-one Bavarian OTUs showed identical sequences to already known and vouchered accessions, two of which are linked to type material, namely Palatinus apiculatus and Theleodinium calcisporum. Particularly within Peridiniaceae, delimitation of Peridinium species was based on the intraspecific sequence variation. 5. Our approach indicates that high-throughput sequencing of environmental samples is effective for reliable determination of dinophyte species in Bavarian lakes.We further discuss the importance of well-curated reference databases that remain to be developed in the future. K E Y W O R D Samplicon sequencing, dinoflagellates, distribution, molecular phylogenetics, operational taxonomic unit

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Toxigenic Pfiesteria species—Updates on biology, ecology, toxins, and impacts

Cited by 28 publications

References 247 publications

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Still Acting Green: Continued Expression of Photosynthetic Genes in the Heterotrophic Dinoflagellate Pfiesteria piscicida (Peridiniales, Alveolata)

Phylogenetic placement of environmental sequences using taxonomically reliable databases helps to rigorously assess dinophyte biodiversity in Bavarian lakes (Germany)

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