In this paper, we focus on dinoflagellate ecology, toxin production, fossil record, and a molecular phylogenetic analysis of hosts and plastids. Of ecological interest are the swimming and feeding behavior, bioluminescence, and symbioses of dinoflagellates with corals. The many varieties of dinoflagellate toxins, their biological effects, and current knowledge of their origin are discussed. Knowledge of dinoflagellate evolution is aided by a rich fossil record that can be used to document their emergence and diversification. However, recent biogeochemical studies indicate that dinoflagellates may be much older than previously believed. A remarkable feature of dinoflagellates is their unique genome structure and gene regulation. The nuclear genomes of these algae are of enormous size, lack nucleosomes, and have permanently condensed chromosomes. This chapter reviews the current knowledge of gene regulation and transcription in dinoflagellates with regard to the unique aspects of the nuclear genome. Previous work shows the plastid genome of typical dinoflagellates to have been reduced to single-gene minicircles that encode only a small number of proteins. Recent studies have demonstrated that the majority of the plastid genome has been transferred to the nucleus, which makes the dinoflagellates the only eukaryotes to encode the majority of typical plastid genes in the nucleus. The evolution of the dinoflagellate plastid and the implications of these results for understanding organellar genome evolution are discussed.
Dinoflagellates produce a variety of toxic secondary metabolites that have a significant impact on marine ecosystems and fisheries. Saxitoxin (STX), the cause of paralytic shellfish poisoning, is produced by three marine dinoflagellate genera and is also made by some freshwater cyanobacteria. Genes involved in STX synthesis have been identified in cyanobacteria but are yet to be reported in the massive genomes of dinoflagellates. We have assembled comprehensive transcriptome data sets for several STX-producing dinoflagellates and a related non-toxic species and have identified 265 putative homologs of 13 cyanobacterial STX synthesis genes, including all of the genes directly involved in toxin synthesis. Putative homologs of four proteins group closely in phylogenies with cyanobacteria and are likely the functional homologs of sxtA, sxtG, and sxtB in dinoflagellates. However, the phylogenies do not support the transfer of these genes directly between toxic cyanobacteria and dinoflagellates. SxtA is split into two proteins in the dinoflagellates corresponding to the N-terminal portion containing the methyltransferase and acyl carrier protein domains and a C-terminal portion with the aminotransferase domain. Homologs of sxtB and N-terminal sxtA are present in non-toxic strains, suggesting their functions may not be limited to saxitoxin production. Only homologs of the C-terminus of sxtA and sxtG were found exclusively in toxic strains. A more thorough survey of STX+ dinoflagellates will be needed to determine if these two genes may be specific to SXT production in dinoflagellates. The A. tamarense transcriptome does not contain homologs for the remaining STX genes. Nevertheless, we identified candidate genes with similar predicted biochemical activities that account for the missing functions. These results suggest that the STX synthesis pathway was likely assembled independently in the distantly related cyanobacteria and dinoflagellates, although using some evolutionarily related proteins. The biological role of STX is not well understood in either cyanobacteria or dinoflagellates. However, STX production in these two ecologically distinct groups of organisms suggests that this toxin confers a benefit to producers that we do not yet fully understand.
BackgroundDinoflagellates are unicellular, often photosynthetic protists that play a major role in the dynamics of the Earth's oceans and climate. Sequencing of dinoflagellate nuclear DNA is thwarted by their massive genome sizes that are often several times that in humans. However, modern transcriptomic methods offer promising approaches to tackle this challenging system. Here, we used massively parallel signature sequencing (MPSS) to understand global transcriptional regulation patterns in Alexandrium tamarense cultures that were grown under four different conditions.Methodology/Principal FindingsWe generated more than 40,000 unique short expression signatures gathered from the four conditions. Of these, about 11,000 signatures did not display detectable differential expression patterns. At a p-value < 1E-10, 1,124 signatures were differentially expressed in the three treatments, xenic, nitrogen-limited, and phosphorus-limited, compared to the nutrient-replete control, with the presence of bacteria explaining the largest set of these differentially expressed signatures.Conclusions/SignificanceAmong microbial eukaryotes, dinoflagellates contain the largest number of genes in their nuclear genomes. These genes occur in complex families, many of which have evolved via recent gene duplication events. Our expression data suggest that about 73% of the Alexandrium transcriptome shows no significant change in gene expression under the experimental conditions used here and may comprise a “core” component for this species. We report a fundamental shift in expression patterns in response to the presence of bacteria, highlighting the impact of biotic interaction on gene expression in dinoflagellates.
Under conditions of iron stress, many organisms replace the comlnon iron-sulfur redox protein ferredoxin with flavodoxin, a functionally equivalent, non-iron-containing protein These 2 proteins have been proposed to be ind~cators of iron nutritional status in marine phytoplankton, but llttle is known of their expression and regulation. This study charactenzed their expression by. (1) testing 17 marine phytoplankton lsolates from 4 different algal classes for their ability to induce flavodoxin under iron limtatlon, ( 2 ) determining the effect of ecologically relevant limiting factors (other than iron) on flavodoxin expression using the marine centric diatom Thalassiosira weissflogu as a model organism, and (3) exdmining, in detail, the relationship between iron availability and relatlve ferredoxin/flavodoxin abundance again using T welssflogii as a model. In the organisms exammed, the most common response (12 of 17 isolates) to iron limitation was induction of flavodoxin and suppression of ferredoxin expression. The remaining 5 isolates, largely of coastal origin, were never observed to produce flavodoxin. These 5 non-inducing organisms have been shown to have high intrinsic Fe requirements for growth and should therefore not present a problem for field measurements of ferredoxin and flavodoxin in iron-poor areas. Expression of flavodoxin in T we~ssflogii was found to b e specific to iron limitation, and was not induced by nitrate, phosphate, silicate, zinc or light deficiency. The prevalence of the flavodoxin response and its insensitivity to other limiting factors support its use as a n inhcator of the presence of iron limitation. Iron regulation of relative ferredoxin and flavodoxln abundance (the Fd index) and iron availabhty was examined in greater detail by measuring the Fd index in T. welssflogii grown over a range of h t i n g iron concentrations. The relationship between Fd index and growth rate (a proxy for iron availability) is composed of 2 distinct regions. In the first region, at low growth rates, ferredoxln is undetectable and the Fd index is uniformly zero In the second region, at moderate-to-fast growth rates, ferredoxin and flavodoxln co-occur in the cells. This implies that flavodoxin substitution is not a sunple 'on-or-off' response Flavodoxin expression is also very sensitive to iron limitation, occurring even at fast growth rates (80 to 90% pmau). When the 2 proteins CO-occurred in cells, their relative abundance (the Fd Index) tended to increase along with Increasing iron availability Thus, variation In the Fd index has the potential to ~ndlcate spatial and temporal changes in the severity of iron stress in the phytoplankton community
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