Kilauea lava fuels phytoplankton bloom in the North Pacific Ocean.

From June to August 2018, the eruption of Kilauea volcano on the island of Hawai'i injected millions of cubic meters of molten lava into the nutrient-poor waters of the North Pacific Subtropical Gyre. The lava-impacted seawater was characterized by high concentrations of metals and nutrients that stimulated phytoplankton growth, resulting in an extensive plume of chlorophyll a that was detectable by satellite. Chemical and molecular evidence revealed that this biological response hinged on unexpectedly high concentrations of nitrate, despite the negligible quantities of nitrogen in basaltic lava. We hypothesize that the high nitrate was caused by buoyant plumes of nutrient-rich deep waters created by the substantial input of lava into the ocean. This large-scale ocean fertilization was therefore a unique perturbation event that revealed how marine ecosystems respond to exogenous inputs of nutrients.

Climate-driven oscillation of phosphorus and iron limitation in the North Pacific Subtropical Gyre.

The supply of nutrients is a fundamental regulator of ocean productivity and carbon sequestration. Nutrient sources, sinks, residence times, and elemental ratios vary over broad scales, including those resulting from climate-driven changes in upper water column stratification, advection, and the deposition of atmospheric dust. These changes can alter the proximate elemental control of ecosystem productivity with cascading ecological effects and impacts on carbon sequestration. Here, we report multidecadal observations revealing that the ecosystem in the eastern region of the North Pacific Subtropical Gyre (NPSG) oscillates on subdecadal scales between inorganic phosphorus (P i ) sufficiency and limitation, when P i concentration in surface waters decreases below 50-60 nmol⋅kg-1 In situ observations and model simulations suggest that sea-level pressure changes over the northwest Pacific may induce basin-scale variations in the atmospheric transport and deposition of Asian dust-associated iron (Fe), causing the eastern portion of the NPSG ecosystem to shift between states of Fe and P i limitation. Our results highlight the critical need to include both atmospheric and ocean circulation variability when modeling the response of open ocean pelagic ecosystems under future climate change scenarios.

Coupling carbon and energy fluxes in the North Pacific Subtropical Gyre.

The major biogeochemical cycles of marine ecosystems are driven by solar energy. Energy that is initially captured through photosynthesis is transformed and transported to great ocean depths via complex, yet poorly understood, energy flow networks. Herein we show that the chemical composition and specific energy (Joules per unit mass or organic carbon) of sinking particulate matter collected in the North Pacific Subtropical Gyre reveal dramatic changes in the upper 500 m of the water column as particles sink and age. In contrast to these upper water column processes, particles reaching the deep sea (4000 m) are energy-replete with organic carbon-specific energy values similar to surface phytoplankton. These enigmatic results suggest that the particles collected in the abyssal zone must be transported by rapid sinking processes. These fast-sinking particles control the pace of deep-sea benthic communities that live a feast-or-famine existence in an otherwise energy-depleted habitat.

The influence of abrupt increases in seawater pCO2 on plankton productivity in the subtropical North Pacific Ocean.

We conducted a series of experiments to examine short-term (2-5 days) effects of abrupt increases in the partial pressure of carbon dioxide (pCO2) in seawater on rates of primary and bacterial production at Station ALOHA (22°45' N, 158° W) in the North Pacific Subtropical Gyre (NPSG). The majority of experiments (8 of 10 total) displayed no response in rates of primary production (measured by 14C-bicarbonate assimilation; 14C-PP) under elevated pCO2 (~1100 µatm) compared to ambient pCO2 (~387 µatm). In 2 of 10 experiments, rates of 14C-PP decreased significantly (~43%) under elevated pCO2 treatments relative to controls. Similarly, no significant differences between treatments were observed in 6 of 7 experiments where bacterial production was measured via incorporation of 3H-leucine (3H-Leu), while in 1 experiment, rates of 3H-Leu incorporation measured in the dark (3H-LeuDark) increased more than 2-fold under high pCO2 conditions. We also examined photoperiod-length, depth-dependent (0-125 m) responses in rates of 14C-PP and 3H-Leu incorporation to abrupt pCO2 increases (to ~750 µatm). In the majority of these depth-resolved experiments (4 of 5 total), rates of 14C-PP demonstrated no consistent response to elevated pCO2. In 2 of 5 depth-resolved experiments, rates of 3H-LeuDark incorporation were lower (10% to 15%) under elevated pCO2 compared to controls. Our results revealed that rates of 14C-PP and bacterial production in this persistently oligotrophic habitat generally demonstrated no or weak responses to abrupt changes in pCO2. We postulate that any effects caused by changes in pCO2 may be masked or outweighed by the role that nutrient availability and temperature play in controlling metabolism in this ecosystem.

Corrigendum: Microbiome of Trichodesmium Colonies from the North Pacific Subtropical Gyre.

[This corrects the article on p. 1122 in vol. 8, PMID: 28729854.].

Microbiome of Trichodesmium Colonies from the North Pacific Subtropical Gyre.

Filamentous diazotrophic Cyanobacteria of the genus Trichodesmium, often found in colonial form, provide an important source of new nitrogen to tropical and subtropical marine ecosystems. Colonies are composed of several clades of Trichodesmium in association with a diverse community of bacterial and eukaryotic epibionts. We used high-throughput 16S rRNA and nifH gene sequencing, carbon (C) and dinitrogen (N2) fixation assays, and metagenomics to describe the diversity and functional potential of the microbiome associated with Trichodesmium colonies collected from the North Pacific Subtropical Gyre (NPSG). The 16S rRNA and nifH gene sequences from hand-picked colonies were predominantly (>99%) from Trichodesmium Clade I (i.e., T. thiebautii), which is phylogenetically and ecologically distinct from the Clade III IMS101 isolate used in most laboratory studies. The bacterial epibiont communities were dominated by Bacteroidetes, Alphaproteobacteria, and Gammaproteobacteria, including several taxa with a known preference for surface attachment, and were relatively depleted in the unicellular Cyanobacteria and small photoheterotrophic bacteria that dominate NPSG surface waters. Sequencing the nifH gene (encoding a subcomponent of the nitrogenase enzyme) identified non-Trichodesmium diazotrophs that clustered predominantly among the Cluster III nifH sequence-types that includes putative anaerobic diazotrophs. Trichodesmium colonies may represent an important habitat for these Cluster III diazotrophs, which were relatively rare in the surrounding seawater. Sequence analyses of nifH gene transcripts revealed several cyanobacterial groups, including heterocystous Richelia, associated with the colonies. Both the 16S rRNA and nifH datasets indicated strong differences between Trichodesmium epibionts and picoplankton in the surrounding seawater, and also between the epibionts inhabiting Trichodesmium puff and tuft colony morphologies. Metagenomic and 16S rRNA gene sequence analyses suggested that lineages typically associated with a copiotrophic lifestyle comprised a large fraction of colony-associated epibionts, in contrast to the streamlined genomes typical of bacterioplankton in these oligotrophic waters. Additionally, epibiont metagenomes were enriched in specific genes involved in phosphate and iron acquisition and denitrification pathways relative to surface seawater metagenomes. We propose that the unique microbial consortium inhabiting colonies has a significant impact on the biogeochemical functioning of Trichodesmium colonies in pelagic environments.

Phenology of particle size distributions and primary productivity in the North Pacific subtropical gyre (Station ALOHA).

The particle size distribution (PSD) is a critical aspect of the oceanic ecosystem. Local variability in the PSD can be indicative of shifts in microbial community structure and reveal patterns in cell growth and loss. The PSD also plays a central role in particle export by influencing settling speed. Satellite-based models of primary productivity (PP) often rely on aspects of photophysiology that are directly related to community size structure. In an effort to better understand how variability in particle size relates to PP in an oligotrophic ecosystem, we collected laser diffraction-based depth profiles of the PSD and pigment-based classifications of phytoplankton functional types (PFTs) on an approximately monthly basis at the Hawaii Ocean Time-series Station ALOHA, in the North Pacific subtropical gyre. We found a relatively stable PSD in the upper water column. However, clear seasonality is apparent in the vertical distribution of distinct particle size classes. Neither laser diffraction-based estimations of relative particle size nor pigment-based PFTs was found to be significantly related to the rate of 14C-based PP in the light-saturated upper euphotic zone. This finding indicates that satellite retrievals of particle size, based on particle scattering or ocean color would not improve parameterizations of present-day bio-optical PP models for this region. However, at depths of 100-125 m where irradiance exerts strong control on PP, we do observe a significant linear relationship between PP and the estimated carbon content of 2-20 µm particles.

Physiological response of Crocosphaera watsonii to enhanced and fluctuating carbon dioxide conditions.

We investigated the effects of elevated pCO2 on cultures of the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH8501. Using CO2-enriched air, cultures grown in batch mode under high light intensity were exposed to initial conditions approximating current atmospheric CO2 concentrations (∼ 400 ppm) as well as CO2 levels corresponding to low- and high-end predictions for the year 2100 (∼ 750 and 1000 ppm). Following acclimation to CO2 levels, the concentrations of particulate carbon (PC), particulate nitrogen (PN), and cells were measured over the diurnal cycle for a six-day period spanning exponential and early stationary growth phases. High rates of photosynthesis and respiration resulted in biologically induced pCO2 fluctuations in all treatments. Despite this observed pCO2 variability, and consistent with previous experiments conducted under stable pCO2 conditions, we observed that elevated mean pCO2 enhanced rates of PC production, PN production, and growth. During exponential growth phase, rates of PC and PN production increased by ∼ 1.2- and ∼ 1.5-fold in the mid- and high-CO2 treatments, respectively, when compared to the low-CO2 treatment. Elevated pCO2 also enhanced PC and PN production rates during early stationary growth phase. In all treatments, PC and PN cellular content displayed a strong diurnal rhythm, with particulate C:N molar ratios reaching a high of 22:1 in the light and a low of 5.5:1 in the dark. The pCO2 enhancement of metabolic rates persisted despite pCO2 variability, suggesting a consistent positive response of Crocosphaera to elevated and fluctuating pCO2 conditions.

Microbial oceanography of anoxic oxygen minimum zones.

Vast expanses of oxygen-deficient and nitrite-rich water define the major oxygen minimum zones (OMZs) of the global ocean. They support diverse microbial communities that influence the nitrogen economy of the oceans, contributing to major losses of fixed nitrogen as dinitrogen (N(2)) and nitrous oxide (N(2)O) gases. Anaerobic microbial processes, including the two pathways of N(2) production, denitrification and anaerobic ammonium oxidation, are oxygen-sensitive, with some occurring only under strictly anoxic conditions. The detection limit of the usual method (Winkler titrations) for measuring dissolved oxygen in seawater, however, is much too high to distinguish low oxygen conditions from true anoxia. However, new analytical technologies are revealing vanishingly low oxygen concentrations in nitrite-rich OMZs, indicating that these OMZs are essentially anoxic marine zones (AMZs). Autonomous monitoring platforms also reveal previously unrecognized episodic intrusions of oxygen into the AMZ core, which could periodically support aerobic metabolisms in a typically anoxic environment. Although nitrogen cycling is considered to dominate the microbial ecology and biogeochemistry of AMZs, recent environmental genomics and geochemical studies show the presence of other relevant processes, particularly those associated with the sulfur and carbon cycles. AMZs correspond to an intermediate state between two "end points" represented by fully oxic systems and fully sulfidic systems. Modern and ancient AMZs and sulfidic basins are chemically and functionally related. Global change is affecting the magnitude of biogeochemical fluxes and ocean chemical inventories, leading to shifts in AMZ chemistry and biology that are likely to continue well into the future.

Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation.

The atmospheric and deep sea reservoirs of carbon dioxide are linked via physical, chemical, and biological processes. The last of these include photosynthesis, particle settling, and organic matter remineralization, and are collectively termed the "biological carbon pump." Herein, we present results from a 13-y (1992-2004) sediment trap experiment conducted in the permanently oligotrophic North Pacific Subtropical Gyre that document a large, rapid, and predictable summertime (July 15-August 15) pulse in particulate matter export to the deep sea (4,000 m). Peak daily fluxes of particulate matter during the summer export pulse (SEP) average 408, 283, 24.1, 1.1, and 67.5 µmol·m(-2)·d(-1) for total carbon, organic carbon, nitrogen, phosphorus (PP), and biogenic silica, respectively. The SEP is approximately threefold greater than mean wintertime particle fluxes and fuels more efficient carbon sequestration because of low remineralization during downward transit that leads to elevated total carbon/PP and organic carbon/PP particle stoichiometry (371:1 and 250:1, respectively). Our long-term observations suggest that seasonal changes in the microbial assemblage, namely, summertime increases in the biomass and productivity of symbiotic nitrogen-fixing cyanobacteria in association with diatoms, are the main cause of the prominent SEP. The recurrent SEP is enigmatic because it is focused in time despite the absence of any obvious predictable stimulus or habitat condition. We hypothesize that changes in day length (photoperiodism) may be an important environmental cue to initiate aggregation and subsequent export of organic matter to the deep sea.

USING A NONANALYTICAL APPROACH TO MODEL NONLINEAR DYNAMICS IN PHOTOSYNTHESIS AT THE PHOTOSYSTEM LEVEL(1).

Nonlinear dynamics in photon capture and uptake at the photosystem level may have a strong effect on photosynthetic yield. However, the magnitude of such effects is difficult to estimate theoretically because nonlinear systems often cannot be represented accurately using equations. A nonanalytical simulation was developed that used a simple decision tree and Monte Carlo methods, instead of equations, to model how a population of photosystems absorbs and utilizes photons from an ambient light field. This simulation replicated realistic kinetics in the closure and variable fluorescence yield of PSII on the single-turnover timescale, as well as the saturating behavior in light-driven electron flow that is observed in nature with increasing irradiance. This simulation indicated that the transfer of absorbed photon energy among PSII units can introduce strong nonlinear enhancement in light-driven electron flow. However, this effect was seen only in populations with particular photosynthetic states as determined by physiological properties of PSII. Other populations with the same degree of energy transfer but with different photosynthetic states exhibited little enhancement in electron flow and, in some cases, a reduction. This nonanalytical approach provides a simple means to quantify theoretically how nonlinear dynamics in photosynthesis arise at the photosystem level and how these dynamics may act to enhance or constrain photosynthetic rates and yields. Such simulations can provide quantitative insight into different physiological bases of nonlinear light-harvesting dynamics and identify those that would have the strongest theoretical influence and thus warrant closer experimental examination.

Nitrogen fixation in an anticyclonic eddy in the oligotrophic North Pacific Ocean.

Mesoscale physical processes (for example eddies, frontal meanders and planetary waves) can play important roles in controlling ocean biogeochemistry. We examined spatial variations in upper ocean (0-100 m) nutrient inventories, N(2) fixing microorganism diversity and abundance, and rates of N(2) fixation in an anticyclonic eddy near Station ALOHA (22 degrees 45' N, 158 degrees 00' W) in the North Pacific Subtropical Gyre (NPSG). In July 2005, satellite-based sea surface altimetry and ocean color observation revealed an anticyclonic eddy with enhanced chlorophyll in the upper ocean in the vicinity of Station ALOHA. Within the eddy, near-surface ocean chlorophyll concentrations were approximately 5-fold greater than in the surrounding waters. Inventories of nitrate and phosphate in the eddy were similar to the concentrations historically observed at Station ALOHA, while silicic acid inventories were significantly depleted (one-way analysis of variance, P<0.01). Quantitative PCR determinations of nifH gene copies revealed relatively high abundances of several N(2) fixing cyanobacteria, including Trichodesmium spp., Crocosphaera watsonii and Richelia intracellularis. Reverse transcriptase PCR (RT-PCR) amplified nitrogenase (nifH) gene transcripts were cloned and sequenced to examine the diversity of active N(2) fixing microorganisms; these clone libraries were dominated by sequence-types 97%-99% identical to the filamentous cyanobacteria Trichodesmium spp. Near-surface ocean rates of N(2) fixation were 2-18 times greater (averaging 8.6+/-5.6 nmol N per l per day) than previously reported measurements at Station ALOHA. These results suggest that mesoscale physical variability can play an important role in modifying the abundances of N(2) fixing microorganisms and associated rates of N(2) fixation in open ocean ecosystems.

Using lasers to probe the transient light absorption by proteorhodopsin in marine bacterioplankton.

We constructed an experimental apparatus that used lasers to provide the probe beams for measuring the transient absorption kinetics of bacterioplankton that contain proteorhodopsin, a microbial protein that binds retinal and is analogous to animal rhodopsin. With this approach we were able to observe photocycles characteristic of functioning retinylidene ion pumps. Using light from lasers instead of broadband sources as transmittance probe beams can be advantageous when examining optically dense, highly scattering samples such as concentrated microbial cultures. Such a laser-based approach may prove useful in shipboard studies for identifying proteorhodopsin in whole cell suspensions concentrated from seawater.

Jet stream intraseasonal oscillations drive dominant ecosystem variations in Oregon's summertime coastal upwelling system.

Summertime wind stress along the coast of the northwestern United States typically exhibits intraseasonal oscillations (ISOs) with periods from approximately 15 to 40 days, as well as fluctuations on the 2- to 6-day "weather-band" and 1-day diurnal time scales. Coastal upwelling of cool, nutrient-rich water is driven by extended periods of equatorward alongshore winds, and we show that the approximately 20-day ISOs in alongshore wind stress dominated the upwelling process during summer 2001 off Oregon. These wind stress ISOs resulted from north-south positional ISOs of the atmospheric jet stream (JS). Upper-ocean temperature, phytoplankton, and zooplankton varied principally on the approximately 20-day time scale as well, and these correlated with the ISOs in alongshore wind stress and JS position, even though there also were weather-band stress fluctuations of comparable magnitude. Such wind stress ISOs are typical along Oregon in the summer upwelling season, occurring in 10 of 12 years examined, including 2001. We present a previously unreported direct connection from the atmospheric JS to oceanic primary and secondary production on the intraseasonal time scale and show the leading importance of ISOs in driving this coastal upwelling ecosystem during a typical summer.

Climate-driven trends in contemporary ocean productivity.

Contributing roughly half of the biosphere's net primary production (NPP), photosynthesis by oceanic phytoplankton is a vital link in the cycling of carbon between living and inorganic stocks. Each day, more than a hundred million tons of carbon in the form of CO2 are fixed into organic material by these ubiquitous, microscopic plants of the upper ocean, and each day a similar amount of organic carbon is transferred into marine ecosystems by sinking and grazing. The distribution of phytoplankton biomass and NPP is defined by the availability of light and nutrients (nitrogen, phosphate, iron). These growth-limiting factors are in turn regulated by physical processes of ocean circulation, mixed-layer dynamics, upwelling, atmospheric dust deposition, and the solar cycle. Satellite measurements of ocean colour provide a means of quantifying ocean productivity on a global scale and linking its variability to environmental factors. Here we describe global ocean NPP changes detected from space over the past decade. The period is dominated by an initial increase in NPP of 1,930 teragrams of carbon a year (Tg C yr(-1)), followed by a prolonged decrease averaging 190 Tg C yr(-1). These trends are driven by changes occurring in the expansive stratified low-latitude oceans and are tightly coupled to coincident climate variability. This link between the physical environment and ocean biology functions through changes in upper-ocean temperature and stratification, which influence the availability of nutrients for phytoplankton growth. The observed reductions in ocean productivity during the recent post-1999 warming period provide insight on how future climate change can alter marine food webs.

Validation of Terra-MODIS phytoplankton chlorophyll fluorescence line height. I. Initial airborne lidar results.

The Moderate Resolution Imaging Spectroradiometer (MODIS) aboard the Terra spacecraft contains spectral bands that allow retrieval of solar-induced phytoplankton chlorophyll fluorescence emission radiance. Concurrent airborne laser-induced (and water-Raman normalized) phytoplankton chlorophyll fluorescence data is used to successfully validate the MODIS chlorophyll fluorescence line height (FLH) retrievals within Gulf Stream, continental slope, shelf, and coastal waters of the Middle Atlantic Bight portion of the western North Atlantic Ocean for 11 March 2002. Over the entire approximately 480-km flight line a correlation coefficient of r2 = 0.85 results from regression of the airborne laser data against the MODIS FLH. It is also shown that the MODIS FLH product is not influenced by blue-absorbing chromophoric dissolved organic matter absorption. These regional results strongly suggest that the FLH methodology is equally valid within similar oceanic provinces of global oceans.