The Outsized Role of Salps in Carbon Export in the Subarctic Northeast Pacific Ocean.

Periodic blooms of salps (pelagic tunicates) can result in high export of organic matter, leading to an "outsized" role in the ocean's biological carbon pump (BCP). However, due to their episodic and patchy nature, salp blooms often go undetected and are rarely included in measurements or models of the BCP. We quantified salp-mediated export processes in the northeast subarctic Pacific Ocean in summer of 2018 during a bloom of Salpa aspera. Salps migrated from 300 to 750 m during the day into the upper 100 m at night. Salp fecal pellet production comprised up to 82% of the particulate organic carbon (POC) produced as fecal pellets by the entire epipelagic zooplankton community. Rapid sinking velocities of salp pellets (400-1,200 m d-1) and low microbial respiration rates on pellets (<1% of pellet C respired day-1) led to high salp pellet POC export from the euphotic zone-up to 48% of total sinking POC across the 100 m depth horizon. Salp active transport of carbon by diel vertical migration and carbon export from sinking salp carcasses was usually <10% of the total sinking POC flux. Salp-mediated export markedly increased BCP efficiency, increasing by 1.5-fold the proportion of net primary production exported as POC across the base of the euphotic zone and by 2.6-fold the proportion of this POC flux persisting 100 m below the euphotic zone. Salps have unique and important effects on ocean biogeochemistry and, especially in low flux settings, can dramatically increase BCP efficiency and thus carbon sequestration.

A Visual Tour of Carbon Export by Sinking Particles.

To better quantify the ocean's biological carbon pump, we resolved the diversity of sinking particles that transport carbon into the ocean's interior, their contribution to carbon export, and their attenuation with depth. Sinking particles collected in sediment trap gel layers from four distinct ocean ecosystems were imaged, measured, and classified. The size and identity of particles was used to model their contribution to particulate organic carbon (POC) flux. Measured POC fluxes were reasonably predicted by particle images. Nine particle types were identified, and most of the compositional variability was driven by the relative contribution of aggregates, long cylindrical fecal pellets, and salp fecal pellets. While particle composition varied across locations and seasons, the entire range of compositions was measured at a single well-observed location in the subarctic North Pacific over one month, across 500 m of depth. The magnitude of POC flux was not consistently associated with a dominant particle class, but particle classes did influence flux attenuation. Long fecal pellets attenuated most rapidly with depth whereas certain other classes attenuated little or not at all with depth. Small particles (<100 µm) consistently contributed ∼5% to total POC flux in samples with higher magnitude fluxes. The relative importance of these small particle classes (spherical mini pellets, short oval fecal pellets, and dense detritus) increased in low flux environments (up to 46% of total POC flux). Imaging approaches that resolve large variations in particle composition across ocean basins, depth, and time will help to better parameterize biological carbon pump models.

The evolution of silicon transporters in diatoms.

Diatoms are highly productive single-celled algae that form an intricately patterned silica cell wall after every cell division. They take up and utilize silicic acid from seawater via silicon transporter (SIT) proteins. This study examined the evolution of the SIT gene family to identify potential genetic adaptations that enable diatoms to thrive in the modern ocean. By searching for sequence homologs in available databases, the diversity of organisms found to encode SITs increased substantially and included all major diatom lineages and other algal protists. A bacterial-encoded gene with homology to SIT sequences was also identified, suggesting that a lateral gene transfer event occurred between bacterial and protist lineages. In diatoms, the SIT genes diverged and diversified to produce five distinct clades. The most basal SIT clades were widely distributed across diatom lineages, while the more derived clades were lineage-specific, which together produced a distinct repertoire of SIT types among major diatom lineages. Differences in the predicted protein functional domains encoded among SIT clades suggest that the divergence of clades resulted in functional diversification among SITs. Both laboratory cultures and natural communities changed transcription of each SIT clade in response to experimental or environmental growth conditions, with distinct transcriptional patterns observed among clades. Together, these data suggest that the diversification of SITs within diatoms led to specialized adaptations among diatoms lineages, and perhaps their dominant ability to take up silicic acid from seawater in diverse environmental conditions.

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.

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 ( approximately 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.

Direct observations of microbial community succession on sinking marine particles.

Microbial community dynamics on sinking particles control the amount of carbon that reaches the deep ocean and the length of time that carbon is stored, with potentially profound impacts on Earth's climate. A mechanistic understanding of the controls on sinking particle distributions has been hindered by limited depth- and time-resolved sampling and methods that cannot distinguish individual particles. Here, we analyze microbial communities on nearly 400 individual sinking particles in conjunction with more conventional composite particle samples to determine how particle colonization and community assembly might control carbon sequestration in the deep ocean. We observed community succession with corresponding changes in microbial metabolic potential on the larger sinking particles transporting a significant fraction of carbon to the deep sea. Microbial community richness decreased as particles aged and sank; however, richness increased with particle size and the attenuation of carbon export. This suggests that the theory of island biogeography applies to sinking marine particles. Changes in POC flux attenuation with time and microbial community composition with depth were reproduced in a mechanistic ecosystem model that reflected a range of POC labilities and microbial growth rates. Our results highlight microbial community dynamics and processes on individual sinking particles, the isolation of which is necessary to improve mechanistic models of ocean carbon uptake.

Unveiling a phytoplankton hotspot at a narrow boundary between coastal and offshore waters.

In terrestrial ecosystems, transitional areas between different plant communities (ecotones) are formed by steep environmental gradients and are commonly characterized by high species diversity and primary productivity, which in turn influences the foodweb structure of these regions. Whether comparable zones of elevated diversity and productivity characterize ecotones in the oceans remains poorly understood. Here we describe a previously hidden hotspot of phytoplankton diversity and productivity in a narrow but seasonally persistent transition zone at the intersection of iron-poor, nitrate-rich offshore waters and iron-rich, nitrate-poor coastal waters of the Northeast Pacific Ocean. Novel continuous measurements of phytoplankton cell abundance and composition identified a complex succession of blooms of five distinct size classes of phytoplankton populations within a 100-km-wide transition zone. The blooms appear to be fueled by natural iron enrichment of offshore communities as they are transported toward the coast. The observed succession of phytoplankton populations is likely driven by spatial gradients in iron availability or time since iron enrichment. Regardless of the underlying mechanism, the resulting communities have a strong impact on the regional biogeochemistry as evidenced by the low partial pressure of CO(2) and the nearly complete depletion of nutrients. Enhanced phytoplankton productivity and diversity associated with steep environmental gradients are expected wherever water masses with complementary nutrient compositions mix to create a region more favorable for phytoplankton growth. The ability to detect and track these important but poorly characterized marine ecotones is critical for understanding their impact on productivity and ecosystem structure in the oceans.

Tracing the path of carbon export in the ocean though DNA sequencing of individual sinking particles.

Surface phytoplankton communities were linked with the carbon they export into the deep ocean by comparing 18 S rRNA gene sequence communities from surface seawater and individually isolated sinking particles. Particles were collected in sediment traps deployed at locations in the North Pacific subtropical gyre and the California Current. DNA was isolated from individual particles, bulk-collected trap particles, and the surface seawater. The relative sequence abundance of exported phytoplankton taxa in the surface water varied across functional groups and ecosystems. Of the sequences detected in sinking particles, about half were present in large (>300 µm), individually isolated particles and primarily belonged to taxa with small cell sizes (<50 µm). Exported phytoplankton taxa detected only in bulk trap samples, and thus presumably packaged in the smaller sinking size fraction, contained taxa that typically have large cell sizes (>500 µm). The effect of particle degradation on the detectable 18 S rRNA gene community differed across taxa, and differences in community composition among individual particles from the same location largely reflected differences in relative degradation state. Using these data and particle imaging, we present an approach that incorporates genetic diversity into mechanistic models of the ocean's biological carbon pump, which will lead to better quantification of the ocean's carbon cycle.

Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses.

Formation of complex inorganic structures is widespread in nature. Diatoms create intricately patterned cell walls of inorganic silicon that are a biomimetic model for design and generation of three-dimensional silica nanostructures. To date, only relatively simple silica structures can be generated in vitro through manipulation of known diatom phosphoproteins (silaffins) and long-chain polyamines. Here, we report the use of genome-wide transcriptome analyses of the marine diatom Thalassiosira pseudonana to identify additional candidate gene products involved in the biological manipulation of silicon. Whole-genome oligonucleotide tiling arrays and tandem mass spectrometry identified transcripts for >8,000 genes, approximately 3,000 of which were not previously described and included noncoding and antisense RNAs. Gene-specific expression profiles detected a set of 75 genes induced only under low concentrations of silicon but not under low concentrations of nitrogen or iron, alkaline pH, or low temperatures. Most of these induced gene products were predicted to contain secretory signals and/or transmembrane domains but displayed no homology to known proteins. Over half of these genes were newly discovered, identified only through the use of tiling arrays. Unexpectedly, a common set of 84 genes were induced by both silicon and iron limitations, suggesting that biological manipulation of silicon may share pathways in common with iron or, alternatively, that iron may serve as a required cofactor for silicon processes. These results provide insights into the transcriptional and translational basis for the biological generation of elaborate silicon nanostructures by these ecologically important microbes.

Chitin in diatoms and its association with the cell wall.

Chitin is a globally abundant polymer widely distributed throughout eukaryotes that has been well characterized in only a few lineages. Diatoms are members of the eukaryotic lineage of stramenopiles. Of the hundreds of diatom genera, two produce long fibers of chitin that extrude through their cell walls of silica. We identify and describe here genes encoding putative chitin synthases in a variety of additional diatom genera, indicating that the ability to produce chitin is more widespread and likely plays a more central role in diatom biology than previously considered. Diatom chitin synthases fall into four phylogenetic clades. Protein domain predictions and differential gene expression patterns provide evidence that chitin synthases have multiple functions within a diatom cell. Thalassiosira pseudonana possesses six genes encoding three types of chitin synthases. Transcript abundance of the gene encoding one of these chitin synthase types increases when cells resume division after short-term silicic acid starvation and during short-term limitation by silicic acid or iron, two nutrient conditions connected in the environment and known to affect the cell wall. During long-term silicic acid starvation transcript abundance of this gene and one additional chitin synthase gene increased at the same time a chitin-binding lectin localized to the girdle band region of the cell wall. Together, these results suggest that the ability to produce chitin is more widespread in diatoms than previously thought and that a subset of the chitin produced by diatoms is associated with the cell wall.

Prevalence and analysis of Renibacterium salmoninarum infection among juvenile Chinook salmon Oncorhynchus tshawytscha in North Puget Sound.

Renibacterium salmoninarum causes bacterial kidney disease (BKD), a chronic and sometimes fatal disease of salmon and trout that could lower fitness in populations with high prevalences of infection. Prevalence of R. salmoninarum infection among juvenile Chinook salmon Oncorhynchus tshawytscha inhabiting neritic marine habitats in North Puget Sound, Washington, USA, was assessed in 2002 and 2003. Fish were collected by monthly surface trawl at 32 sites within 4 bays, and kidney infections were detected by a quantitative fluorescent antibody technique (qFAT). The sensitivity of the qFAT was within an order of magnitude of the quantitative real-time PCR (qPCR) sensitivity. Prevalence of infection was classified by fish origin (marked/hatchery vs. unmarked/likely natural spawn), month of capture, capture location and stock origin. The highest percentages of infected fish (63.5 to 63.8%) and the greatest infection severity were observed for fish collected in Bellingham Bay. The lowest percentages were found in Skagit Bay (11.4 to 13.5%); however, there was no difference in prevalence between marked and unmarked fish among the capture locations. The optimal logistic regression model of infection probabilities identified the capture location of Bellingham Bay as the strongest effect, and analysis of coded wire tagged (CWT) fish revealed that prevalence of infection was associated with the capture location and not with the originating stock. These results suggest that infections can occur during the early marine life stages of Chinook salmon that may be due to common reservoirs of infection or horizontal transmission among fish stocks.