Katherine R. M. Mackey

Toxicity of atmospheric aerosols on marine phytoplankton

Atmospheric aerosol deposition is an important source of nutrients and trace metals to the open ocean that can enhance ocean productivity and carbon sequestration and thus influence atmospheric carbon dioxide concentrations and climate. Using aerosol samples from different back trajectories in incubation experiments with natural communities, we demonstrate that the response of phytoplankton growth to aerosol additions depends on specific components in aerosols and differs across phytoplankton species. Aerosol additions enhanced growth by releasing nitrogen and phosphorus, but not all aerosols stimulated growth. Toxic effects were observed with some aerosols, where the toxicity affected picoeukaryotes and Synechococcus but not Prochlorococcus. We suggest that the toxicity could be due to high copper concentrations in these aerosols and support this by laboratory copper toxicity tests preformed with Synechococcus cultures. However, it is possible that other elements present in the aerosols or unknown synergistic effects between these elements could have also contributed to the toxic effect. Anthropogenic emissions are increasing atmospheric copper deposition sharply, and based on coupled atmosphere–ocean calculations, we show that this deposition can potentially alter patterns of marine primary production and community structure in high aerosol, low chlorophyll areas, particularly in the Bay of Bengal and downwind of South and East Asia.

Alternative photosynthetic electron flow to oxygen in marine Synechococcus

Cyanobacteria dominate the worlds oceans where iron is often barely detectable. One manifestation of low iron adaptation in the oligotrophic marine environment is a decrease in levels of iron-rich photosynthetic components, including the reaction center of photosystem I and the cytochrome b6f complex [R.F. Strzepek and P.J. Harrison, Photosynthetic architecture differs in coastal and oceanic diatoms, Nature 431 (2004) 689-692.]. These thylakoid membrane components have well characterised roles in linear and cyclic photosynthetic electron transport and their low abundance creates potential impediments to photosynthetic function. Here we show that the marine cyanobacterium Synechococcus WH8102 exhibits significant alternative electron flow to O2, a potential adaptation to the low iron environment in oligotrophic oceans. This alternative electron flow appears to extract electrons from the intersystem electron transport chain, prior to photosystem I. Inhibitor studies demonstrate that a propyl gallate-sensitive oxidase mediates this flow of electrons to oxygen, which in turn alleviates excessive photosystem II excitation pressure that can often occur even at relatively low irradiance. These findings are also discussed in the context of satisfying the energetic requirements of the cell when photosystem I abundance is low.

Influence of atmospheric nutrients on primary productivity in a coastal upwelling region

[1] Atmospheric deposition is an important source of nutrients to the coastal and open ocean; however, its role in highly productive upwelling regions like coastal California has not been determined. Approximately 0.1%–0.2% of new production is attributable to atmospheric deposition of nitrogen (N) annually, but if the estimate is expanded to encompass the effects of iron (Fe), aerosols may support 1%–2% of new production on average, and up to 5% on days with high deposition fluxes. Laboratory culture and in situ incubation experiments confirm the bioavailability of N from dry deposition in this region. A significant positive relationship between aerosol optical thickness and chlorophyll a derived from the Moderate Resolution Imaging Spectroradiometer is observed for the summer months and is stronger offshore than near the coast. Moreover, the portion of productivity supported by atmospheric deposition is higher on days without upwelling and during El Nino periods when nutrient input from upwelling is suppressed, a phenomenon that could become more prevalent due to climate warming. Expanding the results from California, we estimate that dry deposition could increase productivity in other major coastal upwelling regions by up to 8% and suggest that aerosols could stimulate productivity by providing N, Fe, and other nutrients that are essential for cell growth but relatively deplete in upwelled water.

Rapid and gradual modes of aerosol trace metal dissolution in seawater.

Atmospheric deposition is a major source of trace metals in marine surface waters and supplies vital micronutrients to phytoplankton, yet measured aerosol trace metal solubility values are operationally defined, and there are relatively few multi-element studies on aerosol-metal solubility in seawater. Here we measure the solubility of aluminum (Al), cadmium (Cd), cobalt (Co), copper (Cu), iron (Fe), manganese (Mn), nickel (Ni), lead (Pb), and zinc (Zn) from natural aerosol samples in seawater over a 7 days period to (1) evaluate the role of extraction time in trace metal dissolution behavior and (2) explore how the individual dissolution patterns could influence biota. Dissolution behavior occurs over a continuum ranging from rapid dissolution, in which the majority of soluble metal dissolved immediately upon seawater exposure (Cd and Co in our samples), to gradual dissolution, where metals dissolved slowly over time (Zn, Mn, Cu, and Al in our samples). Additionally, dissolution affected by interactions with particles was observed in which a decline in soluble metal concentration over time occurred (Fe and Pb in our samples). Natural variability in aerosol chemistry between samples can cause metals to display different dissolution kinetics in different samples, and this was particularly evident for Ni, for which samples showed a broad range of dissolution rates. The elemental molar ratio of metals in the bulk aerosols was 23,189Fe: 22,651Al: 445Mn: 348Zn: 71Cu: 48Ni: 23Pb: 9Co: 1Cd, whereas the seawater soluble molar ratio after 7 days of leaching was 11Fe: 620Al: 205Mn: 240Zn: 20Cu: 14Ni: 9Pb: 2Co: 1Cd. The different kinetics and ratios of aerosol metal dissolution have implications for phytoplankton nutrition, and highlight the need for unified extraction protocols that simulate aerosol metal dissolution in the surface ocean.

Divergent responses of Atlantic coastal and oceanic Synechococcus to iron limitation

Significance Conventional knowledge suggests that coastal phytoplankton are less able to adapt to Fe limitation than open ocean species. Here we show that in contrast to the established paradigm, coastal Synechococcus from the New England shelf is capable of dynamic, multitiered Fe adaptation that allows it to thrive over a broad range of Fe concentrations by partitioning Fe among different uptake and storage proteins. This protein-based response is beneficial in high nitrogen (N) waters with low and variable Fe:N ratios. An oceanic Atlantic Synechococcus isolate lacks this adaptive response, suggesting the small yet significant N cost of retaining Fe response proteins offsets the benefit of Fe adaptability in the southern Sargasso Sea, where N is chronically scarce and Fe:N ratios are high. Marine Synechococcus are some of the most diverse and ubiquitous phytoplankton, and iron (Fe) is an essential micronutrient that limits productivity in many parts of the ocean. To investigate how coastal and oceanic Atlantic Synechococcus strains acclimate to Fe availability, we compared the growth, photophysiology, and quantitative proteomics of two Synechococcus strains from different Fe regimes. Synechococcus strain WH8102, from a region in the southern Sargasso Sea that receives substantial dust deposition, showed impaired growth and photophysiology as Fe declined, yet used few acclimation responses. Coastal WH8020, from the dynamic, seasonally variable New England shelf, displayed a multitiered, hierarchical cascade of acclimation responses with different Fe thresholds. The multitiered response included changes in Fe acquisition, storage, and photosynthetic proteins, substitution of flavodoxin for ferredoxin, and modified photophysiology, all while maintaining remarkably stable growth rates over a range of Fe concentrations. Modulation of two distinct ferric uptake regulator (Fur) proteins that coincided with the multitiered proteome response was found, implying the coastal strain has different regulatory threshold responses to low Fe availability. Low nitrogen (N) and phosphorus (P) availability in the open ocean may favor the loss of Fe response genes when Fe availability is consistent over time, whereas these genes are retained in dynamic environments where Fe availability fluctuates and N and P are more abundant.

A PERSPECTIVE ON PHOTOSYNTHESIS IN THE OLIGOTROPHIC OCEANS: HYPOTHESES CONCERNING ALTERNATE ROUTES OF ELECTRON FLOW1

Many regions of the open, oligotrophic oceans are depleted of nutrients, especially nitrogen and iron. The biogenesis and the functioning of the photosynthetic apparatus may be specialized and tailored to the various marine habitats. In this minireview, we discuss some new findings with respect to photosynthetic processes in the oceans. We focus on findings that suggest that some cyanobacteria may route electrons derived from the splitting of H2O to the reduction of O2 and H+ in a water‐to‐water cycle, and that other cyanobacteria that fix nitrogen during the day are likely missing PSII and enzymes involved in the fixation of inorganic carbon. Both of these proposed “variant” forms of photosynthetic electron flow provide new insights into ways in which marine phytoplankton satisfy their energetic and nutritive requirements.

Phytoplankton responses to atmospheric metal deposition in the coastal and open-ocean Sargasso Sea

This study investigated the impact of atmospheric metal deposition on natural phytoplankton communities at open-ocean and coastal sites in the Sargasso Sea during the spring bloom. Locally collected aerosols with different metal contents were added to natural phytoplankton assemblages from each site, and changes in nitrate, dissolved metal concentration, and phytoplankton abundance and carbon content were monitored. Addition of aerosol doubled the concentrations of cadmium (Cd), cobalt (Co), copper (Cu), iron (Fe), manganese (Mn), and nickel (Ni) in the incubation water. Over the 3-day experiments, greater drawdown of dissolved metals occurred in the open ocean water, whereas little metal drawdown occurred in the coastal water. Two populations of picoeukaryotic algae and Synechococcus grew in response to aerosol additions in both experiments. Particulate organic carbon increased and was most sensitive to changes in picoeukaryote abundance. Phytoplankton community composition differed depending on the chemistry of the aerosol added. Enrichment with aerosol that had higher metal content led to a 10-fold increase in Synechococcus abundance in the oceanic experiment but not in the coastal experiment. Enrichment of aerosol-derived Co, Mn, and Ni were particularly enhanced in the oceanic experiment, suggesting the Synechococcus population may have been fertilized by these aerosol metals. Cu-binding ligand concentrations were in excess of dissolved Cu in both experiments, and increased with aerosol additions. Bioavailable free hydrated Cu2+ concentrations were below toxicity thresholds throughout both experiments. These experiments show (1) atmospheric deposition contributes biologically important metals to seawater, (2) these metals are consumed over time scales commensurate with cell growth, and (3) growth responses can differ between distinct Synechococcus or eukaryotic algal populations despite their relatively close geographic proximity and taxonomic similarity.

Phosphorus Cycling in the Red Tide Incubator Region of Monterey Bay in Response to Upwelling

This study explores the cycling of phosphorus (P) in the euphotic zone following upwelling in northeastern Monterey Bay (the Red Tide Incubator region) of coastal California, with particular emphasis on how bacteria and phytoplankton that form harmful algal blooms mediate and respond to changes in P availability. In situ measurements of nutrient concentrations, phytoplankton community composition, and cell-specific alkaline phosphatase (AP) activity (determined via enzyme-labeled fluorescence assay) were measured during three cruises. Upwelling led to a 10-fold increase in dissolved inorganic (DIP) in surface waters, reaching ∼0.5 μmol L−1. This DIP was drawn down rapidly as upwelling relaxed over a period of 1 week. Ratios of nitrate to DIP drawdown (∼5:1, calculated as the change in nitrate divided by the change in DIP) were lower than the Redfield ratio of 16:1, suggesting that luxury P uptake was occurring as phytoplankton bloomed. Dissolved organic (DOP) remained relatively constant (∼0.3 μmol L−1) before and immediately following upwelling, but doubled as upwelling relaxed, likely due to phytoplankton excretion and release during grazing. This transition from a relatively high DIP:DOP ratio to lower DIP:DOP ratio was accompanied by a decline in the abundance of diatoms, which had low AP activity, toward localized, spatially heterogeneous blooms of dinoflagellates in the genera Prorocentrum, Ceratium, Dinophysis, Alexandrium, and Scrippsiella that showed high AP activity regardless of ambient DIP levels. A nutrient addition incubation experiment showed that phytoplankton growth was primarily limited by nitrate, followed by DIP and DOP, suggesting that P regulates phytoplankton physiology and competition, but is not a limiting nutrient in this region. AP activity was observed in bacteria associated with lysed cell debris and aggregates of particulate organic material, where it may serve to facilitate P regeneration, as well as affixed to the surfaces of intact phytoplankton cells, possibly indicative of close, beneficial phytoplankton–bacteria interactions.

Diel cycling of DNA staining and nifH gene regulation in the unicellular cyanobacterium Crocosphaera watsonii strain WH 8501 (Cyanophyta)

Crocosphaera watsonii WH 8501 is a marine unicellular cyanobacterium that fixes nitrogen primarily during the dark phase of a light-dark (LD) cycle. Circadian clocks modulate gene transcription and cellular activity in many, if not all, cyanobacteria. A model for circadian control has been proposed in cyanobacteria, called the oscilloid model, which is based on topological changes of nucleoid DNA which in turn regulates gene transcription. In this study, the marine unicellular diazotrophic cyanobacteria C. watsonii WH 8501 and Cyanothece sp. ATCC 51142 were found to have daily fluctuations in DNA staining using Hoechst 33342 and SYBR I Green fluorescent dyes. Up to 20-fold decreases in DNA fluorescence of Hoechst-stained cells were observed during the dark phase when cultures were grown with a 12:12 LD cycle or under continuous light (LL). The variation in DNA staining was consistent with changes in DNA topology proposed in the oscilloid model. The abundance of nifH transcripts in C. watsonii WH 8501 was rhythmic under LD and LL cycles, consistent with a circadian rhythm. Cycles of DNA fluorescence and photosynthetic efficiency were disrupted when cultures were shifted into an early dark phase; however, nifH transcripts predictably increased in abundance following the premature transition from light to darkness. Thus, nifH gene expression in C. watsonii WH 8501 appears to be influenced by both circadian and environmental factors.

Nutrient Loading through Submarine Groundwater Discharge and Phytoplankton Growth in Monterey Bay, CA.

We quantified groundwater discharge and associated nutrient fluxes to Monterey Bay, California, during the wet and dry seasons using excess (224)Ra as a tracer. Bioassay incubation experiments were conducted to document the response of bloom-forming phytoplankton to submarine groundwater discharge (SGD) input. Our data indicate that the high nutrient content (nitrate and silica) in groundwater can stimulate the growth of bloom-forming phytoplankton. The elevated concentrations of nitrate in groundwater around Monterey Bay are consistent with agriculture, landfill, and rural housing, which are the primary land-uses in the area surrounding the study site. These findings indicate that SGD acts as a continual source of nutrients that can feed bloom-forming phytoplankton at our study site, constituting a nonpoint source of anthropogenic nutrients to Monterey Bay.