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Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton.

J Phycol. 2016 Feb;52(1):10-36

Authors: Lin S, Litaker RW, Sunda WG

Abstract
Phosphorus (P) is an essential nutrient for marine phytoplankton and indeed all life forms. Current data show that P availability is growth-limiting in certain marine systems and can impact algal species composition. Available P occurs in marine waters as dissolved inorganic phosphate (primarily orthophosphate [Pi]) or as a myriad of dissolved organic phosphorus (DOP) compounds. Despite numerous studies on P physiology and ecology and increasing research on genomics in marine phytoplankton, there have been few attempts to synthesize information from these different disciplines. This paper is aimed to integrate the physiological and molecular information on the acquisition, utilization, and storage of P in marine phytoplankton and the strategies used by these organisms to acclimate and adapt to variations in P availability. Where applicable, we attempt to identify gaps in our current knowledge that warrant further research and examine possible metabolic pathways that might occur in phytoplankton from well-studied bacterial models. Physical and chemical limitations governing cellular P uptake are explored along with physiological and molecular mechanisms to adapt and acclimate to temporally and spatially varying P nutrient regimes. Topics covered include cellular Pi uptake and feedback regulation of uptake systems, enzymatic utilization of DOP, P acquisition by phagotrophy, P-limitation of phytoplankton growth in oceanic and coastal waters, and the role of P-limitation in regulating cell size and toxin levels in phytoplankton. Finally, we examine the role of P and other nutrients in the transition of phytoplankton communities from early succession species (diatoms) to late succession ones (e.g., dinoflagellates and haptophytes).

PMID: 26987085 [PubMed – indexed for MEDLINE]

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A small mitochondrial protein present in myzozoans is essential for malaria transmission.

Open Biol. 2016 Apr;6(4):160034

Authors: Klug D, Mair GR, Frischknecht F, Douglas RG

Abstract
Myzozoans (which include dinoflagellates, chromerids and apicomplexans) display notable divergence from their ciliate sister group, including a reduced mitochondrial genome and divergent metabolic processes. The factors contributing to these divergent processes are still poorly understood and could serve as potential drug targets in disease-causing protists. Here, we report the identification and characterization of a small mitochondrial protein from the rodent-infecting apicomplexan parasite Plasmodium berghei that is essential for development in its mosquito host. Parasites lacking the gene mitochondrial protein ookinete developmental defect (mpodd) showed malformed parasites that were unable to transmit to mosquitoes. Knockout parasites displayed reduced mitochondrial mass without affecting organelle integrity, indicating no role of the protein in mitochondrial biogenesis or morphology maintenance but a likely role in mitochondrial import or metabolism. Using genetic complementation experiments, we identified a previously unrecognized Plasmodium falciparum homologue that can rescue the mpodd(-) phenotype, thereby showing that the gene is functionally conserved. As far as can be detected, mpodd is found in myzozoans, has homologues in the phylum Apicomplexa and appears to have arisen in free-living dinoflagellates. This suggests that the MPODD protein has a conserved mitochondrial role that is important for myzozoans. While previous studies identified a number of essential proteins which are generally highly conserved evolutionarily, our study identifies, for the first time, a non-canonical protein fulfilling a crucial function in the mitochondrion during parasite transmission.

PMID: 27053680 [PubMed – indexed for MEDLINE]

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Ultrastructural and Single-Cell-Level Characterization Reveals Metabolic Versatility in a Microbial Eukaryote Community from an Ice-Covered Antarctic Lake.

Appl Environ Microbiol. 2016 06 15;82(12):3659-3670

Authors: Li W, Podar M, Morgan-Kiss RM

Abstract
UNLABELLED: The McMurdo Dry Valleys (MCM) of southern Victoria Land, Antarctica, harbor numerous ice-covered bodies of water that provide year-round liquid water oases for isolated food webs dominated by the microbial loop. Single-cell microbial eukaryotes (protists) occupy major trophic positions within this truncated food web, ranging from primary producers (e.g., chlorophytes, haptophytes, and cryptophytes) to tertiary predators (e.g., ciliates, dinoflagellates, and choanoflagellates). To advance the understanding of MCM protist ecology and the roles of MCM protists in nutrient and energy cycling, we investigated potential metabolic strategies and microbial interactions of key MCM protists isolated from a well-described lake (Lake Bonney). Fluorescence-activated cell sorting (FACS) of enrichment cultures, combined with single amplified genome/amplicon sequencing and fluorescence microscopy, revealed that MCM protists possess diverse potential metabolic capabilities and interactions. Two metabolically distinct bacterial clades (Flavobacteria and Methylobacteriaceae) were independently associated with two key MCM lake microalgae (Isochrysis and Chlamydomonas, respectively). We also report on the discovery of two heterotrophic nanoflagellates belonging to the Stramenopila supergroup, one of which lives as a parasite of Chlamydomonas, a dominate primary producer in the shallow, nutrient-poor layers of the lake.
IMPORTANCE: Single-cell eukaryotes called protists play critical roles in the cycling of organic matter in aquatic environments. In the ice-covered lakes of Antarctica, protists play key roles in the aquatic food web, providing the majority of organic carbon to the rest of the food web (photosynthetic protists) and acting as the major consumers at the top of the food web (predatory protists). In this study, we utilized a combination of techniques (microscopy, cell sorting, and genomic analysis) to describe the trophic abilities of Antarctic lake protists and their potential interactions with other microbes. Our work reveals that Antarctic lake protists rely on metabolic versatility for their energy and nutrient requirements in this unique and isolated environment.

PMID: 27084010 [PubMed – indexed for MEDLINE]

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Transcriptome Analysis of Scrippsiella trochoidea CCMP 3099 Reveals Physiological Changes Related to Nitrate Depletion.

Front Microbiol. 2016;7:639

Authors: Cooper JT, Sinclair GA, Wawrik B

Abstract
Dinoflagellates are a major component of marine phytoplankton and many species are recognized for their ability to produce harmful algal blooms (HABs). Scrippsiella trochoidea is a non-toxic, marine dinoflagellate that can be found in both cold and tropic waters where it is known to produce “red tide” events. Little is known about the genomic makeup of S. trochoidea and a transcriptome study was conducted to shed light on the biochemical and physiological adaptations related to nutrient depletion. Cultures were grown under N and P limiting conditions and transcriptomes were generated via RNAseq technology. De novo assembly reconstructed 107,415 putative transcripts of which only 41% could be annotated. No significant transcriptomic response was observed in response to initial P depletion, however, a strong transcriptional response to N depletion was detected. Among the down-regulated pathways were those for glutamine/glutamate metabolism as well as urea and nitrate/nitrite transporters. Transcripts for ammonia transporters displayed both up- and down-regulation, perhaps related to a shift to higher affinity transporters. Genes for the utilization of DON compounds were up-regulated. These included transcripts for amino acids transporters, polyamine oxidase, and extracellular proteinase and peptidases. N depletion also triggered down regulation of transcripts related to the production of Photosystems I & II and related proteins. These data are consistent with a metabolic strategy that conserves N while maximizing sustained metabolism by emphasizing the relative contribution of organic N sources. Surprisingly, the transcriptome also contained transcripts potentially related to secondary metabolite production, including a homolog to the Short Isoform Saxitoxin gene (sxtA) from Alexandrium fundyense, which was significantly up-regulated under N-depletion. A total of 113 unique hits to Sxt genes, covering 17 of the 34 genes found in C. raciborskii were detected, indicating that S. trochoidea has previously unrecognized potential for the production of secondary metabolites with potential toxicity.

PMID: 27242681 [PubMed]

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Genome-wide analysis of transcription and photosynthesis inhibition in the harmful dinoflagellate Prorocentrum minimum in response to the biocide copper sulfate.

Harmful Algae. 2016 Jul;57(Pt A):27-38

Authors: Guo R, Lim WA, Ki JS

Abstract
Copper is an essential trace metal for organisms; however, excess copper may damage cellular processes. Their efficiency and physiological effects of biocides have been well documented; however, molecular transcriptome responses to biocides are insufficiently studied. In the present study, a 6.0K oligonucleotide chip was developed to investigate the molecular responses of the harmful dinoflagellate Prorocentrum minimum to copper sulfate (CuSO4) treatment. The results revealed that 515 genes (approximately 8.6%) responded to CuSO4, defined as being within a 2-fold change. Further, KEGG pathway analysis showed that differentially expressed genes (DEGs) were involved in ribosomal function, RNA transport, carbon metabolism, biosynthesis of amino acids, photosystem maintenance, and other cellular processes. Among the DEGs, 49 genes were related to chloroplasts and mitochondria. Furthermore, the genes involved in the RAS signaling pathway, MAPK signaling pathway, and transport pathways were identified. An additional experiment showed that the photosynthesis efficiency decreased considerably, and reactive oxygen species (ROS) production increased in P. minimum after CuSO4 exposure. These results suggest that CuSO4 caused cellular oxidative stress in P. minimum, affecting the ribosome and mitochondria, and severely damaged the photosystem. These effects may potentially lead to cell death, although the dinoflagellate has developed a complex signal transduction process to combat copper toxicity.

PMID: 30170719 [PubMed]

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Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems.

Annu Rev Microbiol. 2016 09 08;70:317-40

Authors: Bourne DG, Morrow KM, Webster NS

Abstract
Corals are fundamental ecosystem engineers, creating large, intricate reefs that support diverse and abundant marine life. At the core of a healthy coral animal is a dynamic relationship with microorganisms, including a mutually beneficial symbiosis with photosynthetic dinoflagellates (Symbiodinium spp.) and enduring partnerships with an array of bacterial, archaeal, fungal, protistan, and viral associates, collectively termed the coral holobiont. The combined genomes of this coral holobiont form a coral hologenome, and genomic interactions within the hologenome ultimately define the coral phenotype. Here we integrate contemporary scientific knowledge regarding the ecological, host-specific, and environmental forces shaping the diversity, specificity, and distribution of microbial symbionts within the coral holobiont, explore physiological pathways that contribute to holobiont fitness, and describe potential mechanisms for holobiont homeostasis. Understanding the role of the microbiome in coral resilience, acclimation, and environmental adaptation is a new frontier in reef science that will require large-scale collaborative research efforts.

PMID: 27482741 [PubMed – indexed for MEDLINE]

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Transcription of the apicoplast genome.

Mol Biochem Parasitol. 2016 Nov – Dec;210(1-2):5-9

Authors: Nisbet RE, McKenzie JL

Abstract
Many members of the Apicomplexa contain a remnant chloroplast, known as an apicoplast. The apicoplast encodes numerous genes, and loss of the organelle is lethal. Here, we present a summary of what is known about apicoplast transcription. Unlike plant chloroplasts, there is a single RNA polymerase, and initial transcription is polycistronic. RNA is then cleaved into tRNA, mRNA and rRNA molecules. Significant levels of antisense transcription have been reported, together with a single case of RNA editing. Polycistronic transcription is also observed in the related algae Chromera and Vitrella, which retain a photosynthetic chloroplast. Surprisingly, a polyU tail is added to Chromera and Vitrella transcripts which encode proteins involved in photosynthesis. No such tail is added to Plasmodium transcripts. Transcription in the Apicomplexa is remarkably similar to that seen in the chloroplast of the related peridinin dinoflagellate algae, reflecting the common evolutionary origins of the organelle.

PMID: 27485555 [PubMed – indexed for MEDLINE]

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Evolutionary processes and cellular functions underlying divergence in Alexandrium minutum.

Mol Ecol. 2016 10;25(20):5129-5143

Authors: Le Gac M, Metegnier G, Chomérat N, Malestroit P, Quéré J, Bouchez O, Siano R, Destombe C, Guillou L, Chapelle A

Abstract
Understanding divergence in the highly dispersive and seemingly homogeneous pelagic environment for organisms living as free drifters in the water column remains a challenge. Here, we analysed the transcriptome-wide mRNA sequences, as well as the morphology of 18 strains of Alexandrium minutum, a dinoflagellate responsible for harmful algal blooms worldwide, to investigate the functional bases of a divergence event. Analysis of the joint site frequency spectrum (JSFS) pointed towards an ancestral divergence in complete isolations followed by a secondary contact resulting in gene flow between the two diverging groups, but heterogeneous across sites. The sites displaying fixed SNPs were associated with a highly restricted gene flow and a strong overrepresentation of nonsynonymous polymorphism, suggesting the importance of selective pressures as drivers of the divergence. The most divergent transcripts were homologs to genes involved in calcium/potassium fluxes across the membrane, calcium transduction signal and saxitoxin production. The implication of these results in terms of ecological divergence and build-up of reproductive isolation is discussed. Dinoflagellates are especially difficult to study in the field at the ecological level due to their small size and the dynamic nature of their natural environment, but also at the genomic level due to their huge and complex genome and the absence of closely related model organism. This study illustrates the possibility to identify the traits of primary importance in ecology and evolution starting from high-throughput sequencing data, even for such organisms.

PMID: 27543851 [PubMed – indexed for MEDLINE]

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Draft genome sequence of Mameliella alba strain UMTAT08 isolated from clonal culture of toxic dinoflagellate Alexandrium tamiyavanichii.

Genom Data. 2016 Dec;10:12-4

Authors: Danish-Daniel M, Han Ming G, Noor ME, Yeong YS, Usup G

Abstract
Mameliella alba strain UMTAT08 was isolated from clonal culture of paralytic shellfish toxin producing dinoflagellate, Alexandrium tamiyavanichii. Genome of the strain UMTAT08 was sequenced in order to gain insights into the dinoflagellate-bacteria interactions. The draft genome sequence of strain UMTAT08 contains 5.84Mbp with an estimated G + C content of 65%, 5717 open reading frames, 5 rRNAs and 49 tRNAs. It contains genes related to nutrients uptake, quorum sensing and environmental tolerance related genes. Gene clusters for the biosynthesis of type 1 polyketide synthase, bacteriocin, microcin, terpene and ectoine were also identified. This is suggesting that the bacterium possesses diverse adaptation strategy to survive within the dinoflagellate phycosphere. The draft genome sequence and annotation have been deposited at DDBJ/EMBL/GenBank under the accession number JSUQ00000000.

PMID: 27625991 [PubMed]

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The Mechanism of Diarrhetic Shellfish Poisoning Toxin Production in Prorocentrum spp.: Physiological and Molecular Perspectives.

Toxins (Basel). 2016 09 22;8(10):

Authors: Lee TC, Fong FL, Ho KC, Lee FW

Abstract
Diarrhetic shellfish poisoning (DSP) is a gastrointestinal disorder caused by the consumption of seafood contaminated with okadaic acid (OA) and dinophysistoxins (DTXs). OA and DTXs are potent inhibitors of protein phosphatases 2A, 1B, and 2B, which may promote cancer in the human digestive system. Their expression in dinoflagellates is strongly affected by nutritional and environmental factors. Studies have indicated that the level of these biotoxins is inversely associated with the growth of dinoflagellates at low concentrations of nitrogen or phosphorus, or at extreme temperature. However, the presence of leucine or glycerophosphate enhances both growth and cellular toxin level. Moreover, the presence of ammonia and incubation in continuous darkness do not favor the toxin production. Currently, studies on the mechanism of this biotoxin production are scant. Full genome sequencing of dinoflagellates is challenging because of the massive genomic size; however, current advanced molecular and omics technologies may provide valuable insight into the biotoxin production mechanism and novel research perspectives on microalgae. This review presents a comprehensive analysis on the effects of various nutritional and physical factors on the OA and DTX production in the DSP toxin-producing Prorocentrum spp. Moreover, the applications of the current molecular technologies in the study on the mechanism of DSP toxin production are discussed.

PMID: 27669302 [PubMed – indexed for MEDLINE]