Alveolate phylogeny inferred using concatenated ribosomal proteins

Dinoflagellates and apicomplexans are a strongly supported monophyletic group in rDNA phylogenies, although this phylogeny is not without controversy, particularly between the two groups. Here we use concatenated protein-coding genes from expressed sequence tags or genomic data to construct phylogenies including "typical" dinophycean dinoflagellates, a parasitic syndinian dinoflagellate, Amoebophrya sp., and two related species, Oxyrrhis marina, and Perkinsus marinus. Seventeen genes encoding proteins associated with the ribosome were selected for phylogenetic analysis. The dataset was limited for the most part by data availability from the dinoflagellates. Forty-five taxa from four major lineages were used: the heterokont outgroup, ciliates, dinoflagellates, and apicomplexans. Amoebophrya sp. was included in this phylogeny as a sole representative of the enigmatic marine alveolate or syndinian lineage. The atypical dinoflagellate O. marina, usually excluded from rDNA analyses due to long branches, was also included. The resulting phylogenies were well supported in concatenated analyses with only a few unstable or weakly supported branches; most features were consistent when different lineages were pruned from the tree or different genes were concatenated. The least stable branches involved the placement of Cryptosporidium spp. within the Apicomplexa and the relationships between P. marinus, Amoebophrya sp., and O. marina. Both bootstrap and approximately unbiased test results confirmed that P. marinus, Amoebophrya sp., O. marina, and the remaining dinoflagellates form a monophyletic lineage to the exclusion of Apicomplexa.     

Genetic diversity, morphological uniformity and polyketide production in dinoflagellates (Amphidinium, Dinoflagellata)

Dinoflagellates are an intriguing group of eukaryotes, showing many unusual morphological and genetic features. Some groups of dinoflagellates are morphologically highly uniform, despite indications of genetic diversity. The species Amphidinium carterae is abundant and cosmopolitan in marine environments, grows easily in culture, and has therefore been used as a 'model' dinoflagellate in research into dinoflagellate genetics, polyketide production and photosynthesis. We have investigated the diversity of 'cryptic' species of Amphidinium that are morphologically similar to A. carterae, including the very similar species Amphidinium massartii, based on light and electron microscopy, two nuclear gene regions (LSU rDNA and ITS rDNA) and one mitochondrial gene region (cytochrome b). We found that six genetically distinct cryptic species (clades) exist within the species A. massartii and four within A. carterae, and that these clades differ from one another in molecular sequences at levels comparable to other dinoflagellate species, genera or even families. Using primers based on an alignment of alveolate ketosynthase sequences, we isolated partial ketosynthase genes from several Amphidinium species. We compared these genes to known dinoflagellate ketosynthase genes and investigated the evolution and diversity of the strains of Amphidinium that produce them.     

Molecular phylogeny of ocelloid-bearing dinoflagellates (Warnowiaceae) as inferred from SSU and LSU rDNA sequences

Background  

Dinoflagellates represent a major lineage of unicellular eukaryotes with unparalleled diversity and complexity in morphological features. The monophyly of dinoflagellates has been convincingly demonstrated, but the interrelationships among dinoflagellate lineages still remain largely unresolved. Warnowiid dinoflagellates are among the most remarkable eukaryotes known because of their possession of highly elaborate ultrastructural systems: pistons, nematocysts, and ocelloids. Complex organelles like these are evolutionary innovations found only in a few athecate dinoflagellates. Moreover, the taxonomy of warnowiids is extremely confusing and inferences about the evolutionary history of this lineage are mired by the absence of molecular phylogenetic data from any member of the group. In this study, we provide the first molecular phylogenetic data for warnowiids and couple them with a review of warnowiid morphological features in order to formulate a hypothetical framework for understanding character evolution within the group. These data also enabled us to evaluate the evolutionary relationship(s) between warnowiids and the other group of dinoflagellates with complex organelles: polykrikoids.     

EARLY EVOLUTIONARY HISTORY OF DINOFLAGELLATES AND APICOMPLEXANS (ALVEOLATA) AS INFERRED FROM HSP90 AND ACTIN PHYLOGENIES1

Three extremely diverse groups of unicellular eukaryotes comprise the Alveolata: ciliates, dinoflagellates, and apicomplexans. The vast phenotypic distances between the three groups along with the enigmatic distribution of plastids and the economic and medical importance of several representative species (e.g. Plasmodium, Toxoplasma, Perkinsus, and Pfiesteria) have stimulated a great deal of speculation on the early evolutionary history of alveolates. A robust phylogenetic framework for alveolate diversity will provide the context necessary for understanding the basic biological properties of the group and for developing appropriate strategies for management. We addressed the earliest stages of alveolate evolution by sequencing heat shock protein 90 (hsp90) genes from several ciliates, apicomplexans, and dinoflagellates, including key species thought to represent early diverging lineages: Oxyrrhis marina, Perkinsus marinus, Cryptosporidium parvum, and the eugregarine Monocystis agilis. Moreover, by sequencing the actin gene from Monocystis, we were able to examine the sister relationship between gregarines and cryptosporidians with a three‐protein concatenated data set (hsp90, actin, and β‐tubulin). Phylogenetic analyses of the hsp90 data set provided a robust topology for alveolate relationships: Alveolates were monophyletic and apicomplexans and dinoflagellates formed sister groups to the exclusion of ciliates. Oxyrrhis formed the earliest diverging sister lineage to the “core” dinoflagellates, and Perkinsus formed the earliest diverging sister lineage to the Oxyrrhis–dinoflagellate clade. This topology was strongly supported inall analyses and by a unique indel shared by Oxyrrhis and dinoflagellates. A sister relationship between Cryptosporidium and Monocystis was weakly supported by the hsp90 data set but strongly supported by the three‐protein concatenated data set.     

Dinoflagellate phylogeny revisited: reconciling morphological and molecular based phylogenies

Ultrastructural and molecular phylogenetic data suggest that dinoflagellates diverged as a lineage possibly as early as the Precambrian. However, the fossil record is problematic before the Mesozoic. From the mid Triassic, though, the fossil record of dinoflagellates is a rich source of information on Mesozoic-Cenozoic dinoflagellates, especially the gonyaulacoids and peridinioids. From the sequence of appearance of species and tabulation types and the impression of early morphological experimentation and later stabilization, the early Mesozoic radiation of dinoflagellates appears to be a real evolutionary event: indeed, dinoflagellate morphology as we know it today may originate in that event. This would explain why it is so difficult to interpret earlier fossils as dinoflagellates. However, that the dinoflagellate lineage existed in some form in the pre-Mesozoic is supported by biogeochemical data, early results of which indicate that certain early Paleozoic acanthomorph acritarchs may belong to the lineage.

A surprising degree of consistency is observed between ultrastructural (including tabulational), coarse biochemical and molecular sequence data. For example, sequence data provided by small subunit (SSU) rRNA support the hypothesis of progressive loss of histones within the dinoflagellates. Gymnodinioids have long been considered to be polyphyletic but are thought of generally as forerunners to the strongly thecate groups such as gonyaulacoids and peridinioids. In molecular trees they appear in both early-derived and late-derived positions, but mostly the latter. SSU data clearly support the gonyaulacoid/peridinioid ordinal separation, as does the fossil record. Prorocentroids are now thought to be the among the most derived dinoflagellates (and presumably the morphologically similar dinophysoids), but SSU sequences have so far failed to resolve the relationships of most gymnodinioids, peridinioids and prorocentroids (the so-called GPP complex) to one another. However, they do suggest the origin of prorocentroids from peridinioids rather than gonyaulacoids and that gymnodinioids probably had several origins.     

THE PHYLOGENETIC RELATIONSHIP OF PFIESTERIA PISCICIDA, CRYPTOPERIDINIOPSOID SP. AMYLOODINOUM OCELLATUM AND A PFIESTERIA-LIKE DINOFLAGELLATE TO OTHER DINOFLAGELLATES AND APICOMPLEXANS

The taxonomic relationship between heterotrophic and parasitic dinoflagellates has not been studied extensively at the molecular level. In order to investigate these taxonomic relationships, we sequenced the small subunit (SSU) ribosomal RNA gene of Pfiesteria piscicida (Steidinger et Burkholder), a Pfiesteria -like dinoflagellate, Cryptoperidiniopsoid sp., and Amyloodinium ocellatum (Brown) and submitted those sequences to GenBank. Pfiesteria piscicida and Cryptoperidiniopsoid sp. are heterotrophic dinoflagellates, purportedly pathogenic to fish, and A. ocellatum, a major fish pathogen, has caused extensive economic losses in both the aquarium and aquaculture industries. The pathogenicity of the Pfiesteria -like dinoflagellate is unknown at this time, but its growth characteristics and in vitro food preferences are similar to those of P. piscicda. The SSU sequences of these species were aligned with the other full-length dinoflagellate sequences, as well as those of representative apicomplexans and Perkinsus species, the groups most closely related to dinoflagellates. Phylogenetic analyses indicate that Cryptoperidiniopsoid sp., P. piscicida, and the Pfiesteria -like dinoflagellate are closely related and group into the class Blastodiniphyceae, as does A. ocellatum. None of the species examined were closely related to the apicomplexans or to Perkinsus marinus, the parasite that causes "Dermo disease" in oysters. The overall phylogenetic analyses largely supported the current class and subclass groupings within the dinoflagellates.     

Dinoflagellate phylogeny as inferred from heat shock protein 90 and ribosomal gene sequences

Background

Interrelationships among dinoflagellates in molecular phylogenies are largely unresolved, especially in the deepest branches. Ribosomal DNA (rDNA) sequences provide phylogenetic signals only at the tips of the dinoflagellate tree. Two reasons for the poor resolution of deep dinoflagellate relationships using rDNA sequences are (1) most sites are relatively conserved and (2) there are different evolutionary rates among sites in different lineages. Therefore, alternative molecular markers are required to address the deeper phylogenetic relationships among dinoflagellates. Preliminary evidence indicates that the heat shock protein 90 gene (Hsp90) will provide an informative marker, mainly because this gene is relatively long and appears to have relatively uniform rates of evolution in different lineages.

Methodology/Principal Findings

We more than doubled the previous dataset of Hsp90 sequences from dinoflagellates by generating additional sequences from 17 different species, representing seven different orders. In order to concatenate the Hsp90 data with rDNA sequences, we supplemented the Hsp90 sequences with three new SSU rDNA sequences and five new LSU rDNA sequences. The new Hsp90 sequences were generated, in part, from four additional heterotrophic dinoflagellates and the type species for six different genera. Molecular phylogenetic analyses resulted in a paraphyletic assemblage near the base of the dinoflagellate tree consisting of only athecate species. However, Noctiluca was never part of this assemblage and branched in a position that was nested within other lineages of dinokaryotes. The phylogenetic trees inferred from Hsp90 sequences were consistent with trees inferred from rDNA sequences in that the backbone of the dinoflagellate clade was largely unresolved.

Conclusions/Significance

The sequence conservation in both Hsp90 and rDNA sequences and the poor resolution of the deepest nodes suggests that dinoflagellates reflect an explosive radiation in morphological diversity in their recent evolutionary past. Nonetheless, the more comprehensive analysis of Hsp90 sequences enabled us to infer phylogenetic interrelationships of dinoflagellates more rigorously. For instance, the phylogenetic position of Noctiluca, which possesses several unusual features, was incongruent with previous phylogenetic studies. Therefore, the generation of additional dinoflagellate Hsp90 sequences is expected to refine the stem group of athecate species observed here and contribute to future multi-gene analyses of dinoflagellate interrelationships.     

Molecular Phylogeny of Parvilucifera prorocentri (Alveolata, Myzozoa): Insights into Perkinsid Character Evolution

ABSTRACT. Perkinsids and colpodellids are lineages that diverged near the origins of dinoflagellates and apicomplexans, respectively, and provide compelling insights into the earliest stages of alveolate evolution. Perkinsids, including Perkinsus and Parvilucifera , are intracellular parasites of animals and dinoflagellates and possess traits also known in syndineans, dinokaryotes (mainly free living dinoflagellates), and colpodellids. An improved understanding of perkinsid biodiversity and phylogeny is expected to shed considerable light on the evolutionary origins of syndineans and dinokaryotes as well as the cellular identities of environmental sequences derived from marine and freshwater habitats. Accordingly, the small subunit (SSU) rDNA sequence from Parvilucifera prorocentri , a tube-forming intracellular parasite of the marine benthic dinoflagellate Prorocentrum fukuyoi , was determined. Molecular phylogenetic analyses demonstrated, with very high statistical support, that P. prorocentri branched as a sister lineage to a divergent clade consisting of Parvilucifera infectans and Parvilucifera sinerae . The entire Parvilucifera clade was nested within a more inclusive and modestly supported clade consisting of Perkinsus and several environmental sequences. Because P. prorocentri possessed a novel combination of ultrastructural features known in Perkinsus, Parvilucifera , and/or syndineans (i.e. germ tubes, trichocysts, and a syndinean-like nucleus), establishing the molecular phylogenetic position of this species enabled us to build a more comprehensive framework for understanding the earliest stages in the evolution of myzozoans.     

Molecular evidence for plastid robbery (Kleptoplastidy) in Dinophysis,a dinoflagellate causing diarrhetic shellfish poisoning

The dinoflagellate genus Dinophysis contains species known to cause diarrhetic shellfish poisoning. Although most photosynthetic dinoflagellates have plastids with peridinin, photosynthetic Dinophysis species have cryptophyte-like plastids containing phycobilin rather than peridinin. We sequenced nuclear- and plastid-encoded SSU rDNA from three photosynthetic species of Dinophysis for phylogenetic analyses. In the tree of nuclear SSU rDNA, Dinophysis was a monophyletic group nested with peridinin-containing dinoflagellates. However, in the tree of plastid SSU rDNA, the Dinophysis plastid lineage was within the radiation of cryptophytes and was closely related to Geminigera cryophila. These analyses indicate that an ancestor of Dinophysis, which may have originally possessed peridinin-type plastid and lost it subsequently, adopted a new plastid from a cryptophyte. Unlike dinoflagellates with fully integrated plastids, the Dinophysis plastid SSU rDNA sequences were identical among the three species examined, while there were species-specific base substitutions in their nuclear SSU rDNA sequences. Queries of the DNA database showed that the plastid SSU rDNA sequence of Dinophysis is almost identical to that of an environmental DNA clone of a <10 pm sized plankter, possibly a cryptophyte and a likely source of the Dinophysis plastid. The present findings suggest that these Dinophysis species engulfed and temporarily retained plastids from a cryptophyte.     

Cyanobacterial endosymbionts in the benthic dinoflagellate Sinophysis canaliculata (Dinophysiales, Dinophyceae)

Photosynthetic dinoflagellates possess a great diversity of plastids that have been acquired through successful serial endosymbiosis. The peridinin-containing plastid in dinoflagellates is canonical, but many other types are known within this group. Within the Dinophysiales, several species of Dinophysis contain plastids, derived from cryptophytes or haptophytes. In this work, the presence of numerous intracellular cyanobacteria-like microorganisms compartmentalized by a separate membrane is reported for the first time within the benthic dinophysoid dinoflagellate Sinophysis canaliculata Quod et al., a species from a genus morphologically close to Dinophysis. Although the contribution of these cyanobacterial endosymbionts to S. canaliculata is still unknown, this finding suggests a possible undergoing primary endosymbiosis in a dinoflagellate.     

Phylogenetic analyses indicate that the 19'Hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin

The three anomalously pigmented dinoflagellates Gymnodinium galatheanum, Gyrodinium aureolum, and Gymnodinium breve have plastids possessing 19'-hexanoyloxy-fucoxanthin as the major carotenoid rather than peridinin, which is characteristic of the majority of the dinoflagellates. Analyses of SSU rDNA from the plastid and the nuclear genome of these dinoflagellate species indicate that they have acquired their plastids via endosymbiosis of a haptophyte. The dinoflagellate plastid sequences appear to have undergone rapid sequence evolution, and there is considerable divergence between the three species. However, distance, parsimony, and maximum-likelihood phylogenetic analyses of plastid SSU rRNA gene sequences place the three species within the haptophyte clade. Pavlova gyrans is the most basal branching haptophyte and is the outgroup to a clade comprising the dinoflagellate sequences and those of other haptophytes. The haptophytes themselves are thought to have plastids of a secondary origin; hence, these dinoflagellates appear to have tertiary plastids. Both molecular and morphological data divide the plastids into two groups, where G. aureolum and G. breve have similar plastid morphology and G. galatheanum has plastids with distinctive features.     

Comparative morphology and molecular phylogeny of Apicoporus n. Gen.: a new genus of marine benthic dinoflagellates formerly classified within Amphidinium

The composition of the dinoflagellate genus Amphidinium is currently polyphyletic and includes several species in need of re-evaluation using modern morphological and phylogenetic methods. We investigated a broad range of uncultured morphotypes extracted from marine sediments in the Eastern Pacific Ocean that were similar in morphology to Amphidinium glabrum Hoppenrath and Okolodkov. To determine the number of distinct species associated with this phenotypic diversity, we collected LM, SEM, TEM and small subunit ribosomal DNA sequence information from different morphotypes, including the previously described A. glabrum. Both comparative morphological and molecular phylogenetic data supported the establishment of a new genus, Apicoporus n. gen., including at least two species, A. glaber n. comb., and A. parvidiaboli n. sp. Apicoporus is characterized by having amphiesmal pores and an apical pore covered by a hook-like protrusion; neither of these characters has been observed in other athecate dinoflagellates. The posterior end of Apicoporus parvidiaboli possessed varying degrees of "horn formation", ranging from slight to prominent. By contrast, the posterior end of Apicoporus glaber was distinctively rounded and lacked evidence of horn formation. Although these species were previously interpreted to be obligate heterotrophs, TEM and epifluorescence microscopy demonstrated that some cells of both species had unusually small but otherwise typical dinoflagellate plastids. The number and density of plastids in any particular cell varied significantly in the genus, but the plastids were almost always concentrated at the posterior end of the cells or around the nucleus. The presence of cryptic photosynthetic plastids in these benthic species suggests that photosynthesis might be much more widespread in dinoflagellates than is currently assumed.     

THECATE HETEROPHIC DINOFLAGELLATES: FEEDING BEHAVIOR AND MECHANISMS1

The feeding of 18 species of thrcale hetrophi dinoflagellates from three genera (Protoperidininm, Oblea, Zygabikodinium) can all be described within one general framework. These species engulf diatoms and other prey with a pseudopod (herein terned a “Pallium”)which originates at the flagellar pore in the sulcus. The pallium is a highly plastic, membranous organ which rasily strethes to accommodate spines and many as 58 diatom cells in a chain. The contents of the phytoplanklon prey are liquified and transporued throughthe pallioum typically within 7 to 30 minutes of capture (although feeding may last 2 h) teaving an intact but empty cell wall or frustule. Thus far, with few exceptions, Protoperidinium specises have been observed feeding inly on diatoms, whereas two diplopsaloid species feed on dinoflagellates and prasinophytes as well. In four species from the three genera studied. a capture filament has been observed that connects the food to the dinoflagellate prior to extension of the pallium, sometimes allowing the cell to pull the food while swimming. A distinctive precapture swimming behavior is also deseribed foe six species, suggesting that the dinoflagellates are selective grazers.     

Plastid genes in a non-photosynthetic dinoflagellate

Dinoflagellates are a diverse group of protists, comprising photosynthetic and heterotrophic free-living species, as well as parasitic ones. About half of them are photosynthetic with peridinin-containing plastids being the most common. It is uncertain whether non-photosynthetic dinoflagellates are primitively so, or have lost photosynthesis. Studies of heterotrophic species from this lineage may increase our understanding of plastid evolution. We analyzed an EST project of the early-diverging heterotrophic dinoflagellate Crypthecodinium cohnii looking for evidence of past endosymbiosis. A large number of putative genes of cyanobacterial or algal origin were identified using BLAST, and later screened by metabolic function. Phylogenetic analyses suggest that several proteins could have been acquired from a photosynthetic endosymbiont, arguing for an earlier plastid acquisition in dinoflagellates. In addition, intact N-terminal plastid-targeting peptides were detected, indicating that C. cohnii may contain a reduced plastid and that some of these proteins are imported into this organelle. A number of metabolic pathways, such as heme and isoprenoid biosynthesis, seem to take place in the plastid. Overall, these data indicate that C. cohnii is derived from a photosynthetic ancestor and provide a model for loss of photosynthesis in dinoflagellates and their relatives. This represents the first extensive genomic analysis of a heterotrophic dinoflagellate.     

Re-examining alveolate evolution using multiple protein molecular phylogenies

Alveolates are a diverse group of protists that includes three major lineages: ciliates, apicomplexa, and dinoflagellates. Among these three, it is thought that the apicomplexa and dinoflagellates are more closely related to one another than to ciliates. However, this conclusion is based almost entirely on results from ribosomal RNA phylogeny because very few morphological characters address this issue and scant molecular data are available from dinoflagellates. To better examine the relationships between the three major alveolate groups, we have sequenced six genes from the non-photosynthetic dinoflagellate, Crypthecodinium cohnii: actin, beta-tubulin, hsp70, BiP, hsp90, and mitochondrial hsp10. Beta-tubulin, hsp70, BiP, and hsp90 were found to be useful for intra-alveolate phylogeny, and trees were inferred from these genes individually and in combination. Trees inferred from individual genes generally supported the apicomplexa-dinoflagellate grouping, as did a combined analysis of all four genes. However, it was also found that the outgroup had a significant effect on the topology within alveolates when using certain methods of phylogenetic reconstruction, and an alternative topology clustering dinoflagellates and ciliates could not be rejected by the combined data. Altogether, these results support the sisterhood of apicomplexa and dinoflagellates, but point out that the relationship is not as strong as is often assumed.     

Serological affinities of the oyster pathogen Perkinsus marinus (Apicomplexa) with some dinoflagellates (Dinophyceae)

The protozoan oyster pathogen Perkinsus marinus is classified in the phylum Apicomplexa, although molecular-genetic and ultrastructural evidence increasingly concur on its closer phylogenetic relationship with the dinoflagellates. To test for evidence of serological epitopes common to P. marinus and dinoflagellates, we probed 19 free-living and 8 parasitic dinoflagellate, or dinoflagellate-like, species for cross-reactivity with polyclonal antibodies to P. marinus. Three of 19 free-living dinoflagellates (16%), and 7 of 8 parasitic dinoflagellates (88%) were labeled by anti-P. marinus antibodies. In reciprocal immunoassays using polyclonal antibodies to the Hematodinium sp. dinoflagellate parasite of Norway lobsters, Nephrops norvegicus, P. marinus and the same 7 parasitic dinoflagellates labeled by anti-P. marinus antibodies, were again labeled. The dinoflagellate-like parasite of prawns Pandalus platyceros was not labeled by either antibody reagent. These reciprocal results confirm the presence of shared antibody-binding epitopes on cells of P. marinus and several dinoflagellates. The apparent widespread serological affinity between P. marinus and the parasitic dinoflagellates suggests a closer phylogenetic link to the syndinean dinoflagellate lineage. The consistent failure of the dinoflagellate-like prawn parasite to bind either antibody reagent shows that this parasite is serologically distinct from both P. marinus and Hematodinium-species parasitic dinoflagellates.     

Description of two species of early branching dinoflagellates, Psammosa pacifica n. g., n. sp. and P. atlantica n. sp

In alveolate evolution, dinoflagellates have developed many unique features, including the cell that has epicone and hypocone, the undulating transverse flagellum. However, it remains unclear how these features evolved. The early branching dinoflagellates so far investigated such as Hematodinium, Amoebophrya and Oxyrrhis marina differ in many ways from of core dinoflagellates, or dinokaryotes. Except those handful of well studied taxa, the vast majority of early branching dinoflagellates are known only by environmental sequences, and remain enigmatic. In this study we describe two new species of the early branching dinoflagellates, Psammosa pacifica n. g., n. sp. and P. atlantica n. sp. from marine intertidal sandy beach. Molecular phylogeny of the small subunit (SSU) ribosomal RNA and Hsp90 gene places Psammosa spp. as an early branch among the dinoflagellates. Morphologically (1) they lack the typical dinoflagellate epicone-hypocone structure, and (2) undulation in either flagella. Instead they display a mosa?c of dinokaryotes traits, i.e. (3) presence of bi-partite trychocysts; Oxyrrhis marina-like traits, i.e. (4) presence of flagellar hairs, (5) presence of two-dimensional cobweb scales ornamenting both flagella (6) transversal cell division; a trait shared with some syndineansand Parvilucifera spp. i.e. (7) a nucleus with a conspicuous nucleolus and condensed chromatin distributed beneath the nuclear envelope; as well as Perkinsus marinus -like features i.e. (8) separate ventral grooves where flagella emerge and (9) lacking dinoflagellate-type undulating flagellum. Notably Psammosa retains an apical complex structure, which is shared between perkinsids, colpodellids, chromerids and apicomplexans, but is not found in dinokaryotic dinoflagellates.     

THE COMPOSITION AND TOXICITY OF DINOFLAGELLATE BLOOMS IN THE SALTON SEA, CALIFORNIA

Phytoplankton blooms have been implicated in mortality events of diverse groups of organisms including fish, birds and humans. About 300 species have been reported to form "red tides," or surface discolorations due to high densities, but only 60–80 of these species produce harmful blooms. In marine systems, dinoflagellates account for 75% of all harmful algal bloom species. The Salton Sea is a large saline lake located in southeastern California, USA. The lake is eutrophic largely because it is in a closed basin and receives most of its input from agricultural and municipal wastewaters. Dinoflagellates comprise a significant portion of the phytoplankton biomass, particularly in winter, often resulting in "red" or "brown" tides. To date, 16 species of dinoflagellates have been identified from the Salton Sea, and many other unidentified forms have also been documented. In 1992, 150,000 eared grebes were found dead over a period of several months at the Salton Sea. This mortality event was among the largest of any bird species. The principal cause remains unknown, but algal toxins were suspected. A survey of the composition and toxicity of algal blooms was undertaken in 1999, and we report results from blooms where dinoflagellates dominated. Dominant species included Gonyaulax grindleyi , Gymnodinium spp., Gyrodinium uncatenum , Heterocapsa niei , and an unidentified scrippsielloid. Although most samples showed activity in a brine shrimp lethality assay, all were negative in a mouse bioassay. This evidence suggests that toxins from dinoflagellate blooms in the Salton Sea are not responsible for eared grebe mortality events.