Micaela S. Parker

The Phaeodactylum genome reveals the evolutionary history of diatom genomes.

Diatoms are photosynthetic secondary endosymbionts found throughout marine and freshwater environments, and are believed to be responsible for around one-fifth of the primary productivity on Earth. The genome sequence of the marine centric diatom Thalassiosira pseudonana was recently reported, revealing a wealth of information about diatom biology. Here we report the complete genome sequence of the pennate diatom Phaeodactylum tricornutum and compare it with that of T. pseudonana to clarify evolutionary origins, functional significance and ubiquity of these features throughout diatoms. In spite of the fact that the pennate and centric lineages have only been diverging for 90 million years, their genome structures are dramatically different and a substantial fraction of genes (∼40%) are not shared by these representatives of the two lineages. Analysis of molecular divergence compared with yeasts and metazoans reveals rapid rates of gene diversification in diatoms. Contributing factors include selective gene family expansions, differential losses and gains of genes and introns, and differential mobilization of transposable elements. Most significantly, we document the presence of hundreds of genes from bacteria. More than 300 of these gene transfers are found in both diatoms, attesting to their ancient origins, and many are likely to provide novel possibilities for metabolite management and for perception of environmental signals. These findings go a long way towards explaining the incredible diversity and success of the diatoms in contemporary oceans.

Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas.

Picoeukaryotes are a taxonomically diverse group of organisms less than 2 micrometers in diameter. Photosynthetic marine picoeukaryotes in the genus Micromonas thrive in ecosystems ranging from tropical to polar and could serve as sentinel organisms for biogeochemical fluxes of modern oceans during climate change. These broadly distributed primary producers belong to an anciently diverged sister clade to land plants. Although Micromonas isolates have high 18S ribosomal RNA gene identity, we found that genomes from two isolates shared only 90% of their predicted genes. Their independent evolutionary paths were emphasized by distinct riboswitch arrangements as well as the discovery of intronic repeat elements in one isolate, and in metagenomic data, but not in other genomes. Divergence appears to have been facilitated by selection and acquisition processes that actively shape the repertoire of genes that are mutually exclusive between the two isolates differently than the core genes. Analyses of the Micromonas genomes offer valuable insights into ecological differentiation and the dynamic nature of early plant evolution.

A Model for Carbohydrate Metabolism in the Diatom Phaeodactylum tricornutum Deduced from Comparative Whole Genome Analysis

Background Diatoms are unicellular algae responsible for approximately 20% of global carbon fixation. Their evolution by secondary endocytobiosis resulted in a complex cellular structure and metabolism compared to algae with primary plastids. Methodology/Principal Findings The whole genome sequence of the diatom Phaeodactylum tricornutum has recently been completed. We identified and annotated genes for enzymes involved in carbohydrate pathways based on extensive EST support and comparison to the whole genome sequence of a second diatom, Thalassiosira pseudonana. Protein localization to mitochondria was predicted based on identified similarities to mitochondrial localization motifs in other eukaryotes, whereas protein localization to plastids was based on the presence of signal peptide motifs in combination with plastid localization motifs previously shown to be required in diatoms. We identified genes potentially involved in a C4-like photosynthesis in P. tricornutum and, on the basis of sequence-based putative localization of relevant proteins, discuss possible differences in carbon concentrating mechanisms and CO2 fixation between the two diatoms. We also identified genes encoding enzymes involved in photorespiration with one interesting exception: glycerate kinase was not found in either P. tricornutum or T. pseudonana. Various Calvin cycle enzymes were found in up to five different isoforms, distributed between plastids, mitochondria and the cytosol. Diatoms store energy either as lipids or as chrysolaminaran (a β-1,3-glucan) outside of the plastids. We identified various β-glucanases and large membrane-bound glucan synthases. Interestingly most of the glucanases appear to contain C-terminal anchor domains that may attach the enzymes to membranes. Conclusions/Significance Here we present a detailed synthesis of carbohydrate metabolism in diatoms based on the genome sequences of Thalassiosira pseudonana and Phaeodactylum tricornutum. This model provides novel insights into acquisition of dissolved inorganic carbon and primary metabolic pathways of carbon in two different diatoms, which is of significance for an improved understanding of global carbon cycles.

Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria

Interactions between primary producers and bacteria impact the physiology of both partners, alter the chemistry of their environment, and shape ecosystem diversity. In marine ecosystems, these interactions are difficult to study partly because the major photosynthetic organisms are microscopic, unicellular phytoplankton. Coastal phytoplankton communities are dominated by diatoms, which generate approximately 40% of marine primary production and form the base of many marine food webs. Diatoms co-occur with specific bacterial taxa, but the mechanisms of potential interactions are mostly unknown. Here we tease apart a bacterial consortium associated with a globally distributed diatom and find that a Sulfitobacter species promotes diatom cell division via secretion of the hormone indole-3-acetic acid, synthesized by the bacterium using both diatom-secreted and endogenous tryptophan. Indole-3-acetic acid and tryptophan serve as signalling molecules that are part of a complex exchange of nutrients, including diatom-excreted organosulfur molecules and bacterial-excreted ammonia. The potential prevalence of this mode of signalling in the oceans is corroborated by metabolite and metatranscriptome analyses that show widespread indole-3-acetic acid production by Sulfitobacter-related bacteria, particularly in coastal environments. Our study expands on the emerging recognition that marine microbial communities are part of tightly connected networks by providing evidence that these interactions are mediated through production and exchange of infochemicals.

Ferritin is used for iron storage in bloom-forming marine pennate diatoms

Primary productivity in 30–40% of the world’s oceans is limited by availability of the micronutrient iron. Regions with chronically low iron concentrations are sporadically pulsed with new iron inputs by way of dust or lateral advection from continental margins. Addition of iron to surface waters in these areas induces massive phytoplankton blooms dominated primarily by pennate diatoms. Here we provide evidence that the bloom-forming pennate diatoms Pseudo-nitzschia and Fragilariopsis use the iron-concentrating protein, ferritin, to safely store iron. Ferritin has not been reported previously in any member of the Stramenopiles, a diverse eukaryotic lineage that includes unicellular algae, macroalgae and plant parasites. Phylogenetic analyses suggest that ferritin may have arisen in this small subset of diatoms through a lateral gene transfer. The crystal structure and functional assays of recombinant ferritin derived from Pseudo-nitzschia multiseries reveal a maxi-ferritin that exhibits ferroxidase activity and binds iron. The protein is predicted to be targeted to the chloroplast to control the distribution and storage of iron for proper functioning of the photosynthetic machinery. Abundance of Pseudo-nitzschia ferritin transcripts is regulated by iron nutritional status, and is closely tied to the loss and recovery of photosynthetic competence. Enhanced iron storage with ferritin allows the oceanic diatom Pseudo-nitzschia granii to undergo several more cell divisions in the absence of iron than the comparably sized, oceanic centric diatom Thalassiosira oceanica. Ferritin in pennate diatoms probably contributes to their success in chronically low-iron regions that receive intermittent iron inputs, and provides an explanation for the importance of these organisms in regulating oceanic CO2 over geological timescales.

Impacts of climate variability and future climate change on harmful algal blooms and human health.

Anthropogenically-derived increases in atmospheric greenhouse gas concentrations have been implicated in recent climate change, and are projected to substantially impact the climate on a global scale in the future. For marine and freshwater systems, increasing concentrations of greenhouse gases are expected to increase surface temperatures, lower pH, and cause changes to vertical mixing, upwelling, precipitation, and evaporation patterns. The potential consequences of these changes for harmful algal blooms (HABs) have received relatively little attention and are not well understood. Given the apparent increase in HABs around the world and the potential for greater problems as a result of climate change and ocean acidification, substantial research is needed to evaluate the direct and indirect associations between HABs, climate change, ocean acidification, and human health. This research will require a multidisciplinary approach utilizing expertise in climatology, oceanography, biology, epidemiology, and other disciplines. We review the interactions between selected patterns of large-scale climate variability and climate change, oceanic conditions, and harmful algae.

Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability

In vast expanses of the oceans, growth of large phytoplankton such as diatoms is limited by iron availability. Diatoms respond almost immediately to the delivery of iron and rapidly compose the majority of phytoplankton biomass. The molecular bases underlying the subsistence of diatoms in iron-poor waters and the plankton community dynamics that follow iron resupply remain largely unknown. Here we use comparative metatranscriptomics to identify changes in gene expression associated with iron-stimulated growth of diatoms and other eukaryotic plankton. A microcosm iron-enrichment experiment using mixed-layer waters from the northeastern Pacific Ocean resulted in increased proportions of diatom transcripts and reduced proportions of transcripts from most other taxa within 98 h after iron addition. Hundreds of diatom genes were differentially expressed in the iron-enriched community compared with the iron-limited community; transcripts of diatom genes required for synthesis of photosynthesis and chlorophyll components, nitrate assimilation and the urea cycle, and synthesis of carbohydrate storage compounds were significantly overrepresented. Transcripts of genes encoding rhodopsins in eukaryotic phytoplankton were significantly underrepresented following iron enrichment, suggesting rhodopsins help cells cope with low-iron conditions. Oceanic diatoms appear to display a distinctive transcriptional response to iron enrichment that allows chemical reduction of available nitrogen and carbon sources along with a continued dependence on iron-free photosynthetic proteins rather than substituting for iron-containing functional equivalents present within their gene repertoire. This ability of diatoms to divert their newly acquired iron toward nitrate assimilation may underlie why diatoms consistently dominate iron enrichments in high-nitrate, low-chlorophyll regions.

Genomic Insights into Marine Microalgae

Marine eukaryotic photosynthesis is dominated by a diverse group of unicellular organisms collectively called microalgae. Microalgae include cells derived from a primary endosymbiotic event (similar to land plants) and cells derived from subsequent secondary and/or tertiary endosymbiotic events. These latter cells are chimeras of several genomes and dominate primary production in the marine environment. Two consequences of multiple endosymbiotic events include complex targeting mechanisms to allow nuclear-encoded proteins to be imported into the plastid and coordination of enzymes, potentially from disparate originator cells, to form complete metabolic pathways. In this review, we discuss the forces that shaped the genomes of marine microalgae and then discuss some of the metabolic consequences of such a complex evolutionary history. We focus our metabolic discussion on carbon, nitrogen, and iron. We then discuss biomineralization and new evidence for programmed cell death in microalgae. We conclude with a short summary on advances in genetic manipulation of microalgae and thoughts on the future directions of marine algal genomics.

SYNERGISTIC EFFECTS OF LIGHT, TEMPERATURE, AND NITROGEN SOURCE ON TRANSCRIPTION OF GENES FOR CARBON AND NITROGEN METABOLISM IN THE CENTRIC DIATOM THALASSIOSIRA PSEUDONANA (BACILLARIOPHYCEAE)1

The effects of nitrogen source, temperature, and light level on transcription of five genes from three pathways of carbon and nitrogen metabolism were determined for the centric diatom Thalassiosira pseudonana (Hustedt) Hasle et Heimdal. The targeted genes were NR (nitrate reductase) and GSII (glutamine synthetase II), both required for nitrate utilization; PGP (phosphoglycolate phosphatase) and GDCT (glycine decarboxylase T‐protein), both required for photorespiration; and SBP (sedoheptulose 1,7‐bisphosphatase), required for carbon fixation (Calvin cycle). Quantitative reverse transcriptase PCR was used to compare transcript abundances for these genes from T. pseudonana cells grown at two light intensities (50 or 300 μmol photons·m−2·s−1), at two temperatures (12 or 22°C), and on two different nitrogen sources (nitrate or ammonium). Transcript abundance (normalized to 18S rRNA) was higher for all five genes at the higher light intensity. At 12°C, fewer transcripts were detected for the Calvin cycle gene, whereas more transcripts were detected for the photorespiration and nitrate utilization genes. Nitrogen source affected transcript accumulation of the photorespiration and nitrate utilization genes but not the Calvin cycle gene. Extracellular concentrations of glycolate, a photorespiratory‐specific product, were determined under the high light conditions and were found to decrease at 12°C and when cells were grown on ammonium. A hypothetical model is presented to explain the patterns of transcript accumulation and glycolate release in terms of energy balance within the cell.

Centers for Oceans and Human Health: a unified approach to the challenge of harmful algal blooms

BackgroundHarmful algal blooms (HABs) are one focus of the national research initiatives on Oceans and Human Health (OHH) at NIEHS, NOAA and NSF. All of the OHH Centers, from the east coast to Hawaii, include one or more research projects devoted to studying HAB problems and their relationship to human health. The research shares common goals for understanding, monitoring and predicting HAB events to protect and improve human health: understanding the basic biology of the organisms; identifying how chemistry, hydrography and genetic diversity influence blooms; developing analytical methods and sensors for cells and toxins; understanding health effects of toxin exposure; and developing conceptual, empirical and numerical models of bloom dynamics.ResultsIn the past several years, there has been significant progress toward all of the common goals. Several studies have elucidated the effects of environmental conditions and genetic heterogeneity on bloom dynamics. New methods have been developed or implemented for the detection of HAB cells and toxins, including genetic assays for Pseudo-nitzschia and Microcystis, and a biosensor for domoic acid. There have been advances in predictive models of blooms, most notably for the toxic dinoflagellates Alexandrium and Karenia. Other work is focused on the future, studying the ways in which climate change may affect HAB incidence, and assessing the threat from emerging HABs and toxins, such as the cyanobacterial neurotoxin β-N-methylamino-L-alanine.ConclusionAlong the way, many challenges have been encountered that are common to the OHH Centers and also echo those of the wider HAB community. Long-term field data and basic biological information are needed to develop accurate models. Sensor development is hindered by the lack of simple and rapid assays for algal cells and especially toxins. It is also critical to adequately understand the human health effects of HAB toxins. Currently, we understand best the effects of acute toxicity, but almost nothing is known about the effects of chronic, subacute toxin exposure. The OHH initiatives have brought scientists together to work collectively on HAB issues, within and across regions. The successes that have been achieved highlight the value of collaboration and cooperation across disciplines, if we are to continue to advance our understanding of HABs and their relationship to human health.