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Shi, XG, Lin X, Li L, Li MZ, Palenik B, Lin SJ.  2017.  Transcriptomic and microRNAomic profiling reveals multi-faceted mechanisms to cope with phosphate stress in a dinoflagellate. Isme Journal. 11:2209-2218.   10.1038/ismej.2017.81   AbstractWebsite

Although gene regulation can occur at both transcriptional and epigenetic (microRNA) levels, combined transcriptomic and microRNAomic responses to environmental stress are still largely unexplored for marine plankton. Here, we conducted transcriptome and microRNAome sequencing for Prorocentrum donghaiense to understand the molecular mechanisms by which this dinoflagellate copes with phosphorus (P) deficiency. Under P-depleted conditions, G1/S specific cyclin gene was markedly downregulated, consistent with growth inhibition, and genes related to dissolved organic phosphorus (DOP) hydrolysis, carbon fixation, nitrate assimilation, glycolysis, and cellular motility were upregulated. The elevated expression of ATP-generating genes (for example, rhodopsin) and ATP-consuming genes suggests some metabolic reconfiguration towards accelerated ATP recycling under P deficiency. MicroRNAome sequencing revealed 17 microRNAs, potentially regulating 3268 protein-coding genes. Functional enrichment analysis of these microRNA-targeted genes predicted decreases in sulfatide (sulfolipid) catabolism under P deficiency. Strikingly, we detected a significant increase in sulfolipid sulfatide content (but not in sulphoquinovosyldiacylglycerol content) and its biosynthesis gene expression, indicating a different sulfolipid-substituting-phospholipid mechanism in this dinoflagellate than other phytoplankters studied previously. Taken together, our integrative transcriptomic and microRNAomic analyses show that enhanced DOP utilization, accelerated ATP cycling and repressed sulfolipid degradation constitute a comprehensive strategy to cope with P deficiency in a model dinoflagellate.

Jones, GJ, Palenik BP, Morel FMM.  1987.  Trace-Metal Reduction by Phytoplankton - the Role of Plasmalemma Redox Enzymes. Journal of Phycology. 23:237-244.   10.1111/j.1529-8817.1987.tb04131.x   AbstractWebsite

The phytoplankton cell surface reduces external copper(II) and iron(III) complexes and redox dyes. This reductive activity appears to be mediated by one or more plasmalemma redox enzymes. Trace metal complexes are directly reduced by the redox enzyme, therefore the reduction rate is not regulated by the metal free ion activity in solution. This is in direct contrast to previous measurements of trace metal interactions with the phytoplankton cell membrane. Half-saturation constants for the reduction of Cu(II) complexes with carbonate, phenanthroline and bathocuproinedisulfonate are in the range 2.3–14.7 μM, which suggests that trace metal complexes are not the main electron acceptor in natural waters. In the diatom Thalassiosira weissflogii there is additional reductive activity associated with the cell wall.

Palenik, B, Grimwood J, Aerts A, Rouze P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, Zhou K, Otillar R, Merchant SS, Podell S, Gaasterland T, Napoli C, Gendler K, Manuell A, Tai V, Vallon O, Piganeau G, Jancek S, Heijde M, Jabbari K, Bowler C, Lohr M, Robbens S, Werner G, Dubchak I, Pazour GJ, Ren Q, Paulsen I, Delwiche C, Schmutz J, Rokhsar D, Van de Peer Y, Moreau H, Grigoriev IV.  2007.  The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proceedings of the National Academy of Sciences of the United States of America. 104:7705-7710.   10.1073/pnas.0611046104   AbstractWebsite

The smallest known eukaryotes, at approximate to 1-mu m diameter, are ostreococcus tauri and related species of marine phytoplankton. The genome of Ostreococcus lucimarinus has been completed and compared with that of O. tauri. This comparison reveals surprising differences across orthologous chromosomes in the two species from highly syntenic chromosomes in most cases to chromosomes with almost no similarity. Species divergence in these phytoplankton is occurring through multiple mechanisms acting differently on different chromosomes and likely including acquisition of new genes through horizontal gene transfer. We speculate that this latter process may be involved in altering the cell-surface characteristics of each species. In addition, the genome of O. lucimarinus provides insights into the unique metal metabolism of these organisms, which are predicted to have a large number of selenocysteine-containing proteins. Selenoenzymes are more catalytically active than similar enzymes lacking selenium, and thus the cell may require less of that protein. As reported here, selenoenzymes, novel fusion proteins, and loss of some major protein families including ones associated with chromatin are likely important adaptations for achieving a small cell size.

Tai, V, Palenik B.  2009.  Temporal variation of Synechococcus clades at a coastal Pacific Ocean monitoring site. Isme Journal. 3:903-915.   10.1038/ismej.2009.35   AbstractWebsite

Marine cyanobacteria from the genus Synechococcus are found throughout the world's oceans and are important contributors to global primary productivity and carbon cycling. Cultured isolates and environmental DNA clone libraries of Synechococcus have demonstrated the diversity of these microbes. However, the natural distribution of this diversity through space and time and the ecological significance of their distribution are still poorly understood. To understand the seasonal dynamics of Synechococcus diversity, we have developed a quantitative PCR strategy using the gene encoding as a subunit of DNA-dependent RNA polymerase (rpoC1) and applied it to a 3-year time series of surface samples from the Scripps Institution of Oceanography pier (La Jolla, CA, USA), a coastal site in the northeastern Pacific Ocean. Synechococcus from clades I and IV were dominant throughout the time series and correlated with total Synechococcus abundance. The relative abundance of these two dominant clades showed evidence of a seasonal cycle. Synechococcus from clade IV were typically more abundant, but those from clade I dominated during periods just before the annual spring bloom of Synechococcus. Synechococcus from clades II and III were absent during spring and early summer, but appeared at low abundances in late summer and winter possibly due to changes in circulation in the Southern California Bight. As the first long-term time series describing Synechococcus population diversity, these temporal dynamics were used to interpret the genetic/genomic diversity observed in the environment and the potential factors regulating their distribution. The ISME Journal (2009) 3, 903-915; doi: 10.1038/ismej.2009.35; published online 9 April 2009

Nagarkar, M, Countway PD, Du Yoo Y, Daniels E, Poulton NJ, Palenik B.  2018.  Temporal dynamics of eukaryotic microbial diversity at a coastal Pacific site. The ISME Journal.   10.1038/s41396-018-0172-3   Abstract

High-throughput sequencing of ocean biomes has revealed vast eukaryotic microbial diversity, a significant proportion of which remains uncharacterized. Here we use a temporal approach to understanding eukaryotic diversity at the Scripps Pier, La Jolla, California, USA, via high-throughput amplicon sequencing of the 18S rRNA gene, the abundances of both Synechococcus and Synechococcus grazers, and traditional oceanographic parameters. We also exploit our ability to track operational taxonomic units (OTUs) temporally to evaluate the ability of 18S sequence-based OTU assignments to meaningfully reflect ecological dynamics. The eukaryotic community is highly dynamic in terms of both species richness and composition, although proportional representation of higher-order taxa remains fairly consistent over time. Synechococcus abundance fluctuates throughout the year. OTUs unique to dates of Synechococcus blooms and crashes or enriched in Synechococcus addition incubation experiments suggest that the prasinophyte Tetraselmis sp. and Gymnodinium-like dinoflagellates are likely Synechococcus grazers under certain conditions, and may play an important role in their population fluctuations.

Tai, V, Burton RS, Palenik B.  2011.  Temporal and spatial distributions of marine Synechococcus in the Southern California Bight assessed by hybridization to bead-arrays. Marine Ecology-Progress Series. 426:133-U164.   10.3354/meps09030   AbstractWebsite

Marine Synechococcus diversity has been previously described using multi-locus gene sequence phylogenies and the identification of distinct clades. Synechococcus from Clades I, II, III, and IV and from sub-clades within Clades I and IV were enumerated from environmental samples by developing a hybridization assay to liquid bead-arrays (Luminex). Oligonucleotide probes targeting a gene encoding a subunit of RNA polymerase (rpoC1) were used simultaneously in multiplexed assays to track Synechococcus diversity from a Pacific Ocean coastal monitoring site and along a coastal to open-ocean transect in the Southern California Bight. The Luminex assay demonstrated that Synechococcus from Clades I and IV were the dominant types at the coastal site throughout the year. Synechococcus from Clades II and III were not detected except during the late summer or early winter. Within the dominant Clades I and IV, rpoC1-defined sub-clades of Synechococcus showed distinct spatial distributions along the coastal to open-ocean transect, coinciding with changes in the nitricline, thermocline, and fluorescence (chlorophyll) maximum depths. In coastal waters, Synechococcus targeted by 2 sub-clade IV probes were dominant at the surface, whereas 2 sub-clade I probes and a third sub-clade IV probe had increased signals in deeper water near the fluorescence maximum. In mesotrophic waters, this third sub-clade IV probe dominated at the fluorescence maximum (depth of 50 to 70 m), whereas all other sub-clade probes were below detection limits. The differing distributions of sub-clades within the dominant Synechococcus clades indicate that the sub-clades likely have adapted to distinct ecological niches found within the Southern California Bight.