Michael W. Lomas

Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity

Phosphorus is an obligate requirement for the growth of all organisms; major biochemical reservoirs of phosphorus in marine plankton include nucleic acids and phospholipids. However, eukaryotic phytoplankton and cyanobacteria (that is, ‘phytoplankton’ collectively) have the ability to decrease their cellular phosphorus content when phosphorus in their environment is scarce. The biochemical mechanisms that allow phytoplankton to limit their phosphorus demand and still maintain growth are largely unknown. Here we show that phytoplankton, in regions of oligotrophic ocean where phosphate is scarce, reduce their cellular phosphorus requirements by substituting non-phosphorus membrane lipids for phospholipids. In the Sargasso Sea, where phosphate concentrations were less than 10 nmol l-1, we found that only 1.3 ± 0.6% of phosphate uptake was used for phospholipid synthesis; in contrast, in the South Pacific subtropical gyre, where phosphate was greater than 100 nmol l-1, plankton used 17 ± 6% (ref. 6). Examination of the planktonic membrane lipids at these two locations showed that classes of sulphur- and nitrogen-containing membrane lipids, which are devoid of phosphorus, were more abundant in the Sargasso Sea than in the South Pacific. Furthermore, these non-phosphorus, ‘substitute lipids’ were dominant in phosphorus-limited cultures of all of the phytoplankton species we examined. In contrast, the marine heterotrophic bacteria we examined contained no substitute lipids and only phospholipids. Thus heterotrophic bacteria, which compete with phytoplankton for nutrients in oligotrophic regions like the Sargasso Sea, appear to have a biochemical phosphorus requirement that phytoplankton avoid by using substitute lipids. Our results suggest that phospholipid substitutions are fundamental biochemical mechanisms that allow phytoplankton to maintain growth in the face of phosphorus limitation.

Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus

The Cyanobacteria Prochlorococcus and Synechococcus account for a substantial fraction of marine primary production. Here, we present quantitative niche models for these lineages that assess present and future global abundances and distributions. These niche models are the result of neural network, nonparametric, and parametric analyses, and they rely on >35,000 discrete observations from all major ocean regions. The models assess cell abundance based on temperature and photosynthetically active radiation, but the individual responses to these environmental variables differ for each lineage. The models estimate global biogeographic patterns and seasonal variability of cell abundance, with maxima in the warm oligotrophic gyres of the Indian and the western Pacific Oceans and minima at higher latitudes. The annual mean global abundances of Prochlorococcus and Synechococcus are 2.9 ± 0.1 × 1027 and 7.0 ± 0.3 × 1026 cells, respectively. Using projections of sea surface temperature as a result of increased concentration of greenhouse gases at the end of the 21st century, our niche models projected increases in cell numbers of 29% and 14% for Prochlorococcus and Synechococcus, respectively. The changes are geographically uneven but include an increase in area. Thus, our global niche models suggest that oceanic microbial communities will experience complex changes as a result of projected future climate conditions. Because of the high abundances and contributions to primary production of Prochlorococcus and Synechococcus, these changes may have large impacts on ocean ecosystems and biogeochemical cycles.

COMPARISONS OF NITRATE UPTAKE, STORAGE, AND REDUCTION IN MARINE DIATOMS AND FLAGELLATES

Diatoms, but not flagellates, have been shown to increase rates of nitrogen release after a shift from a low growth irradiance to a much higher experimental irradiance. We compared NO3− uptake kinetics, internal inorganic nitrogen storage, and the temperature dependence of the NO3− reduction enzymes, nitrate (NR) and nitrite reductase (NiR), in nitrogen‐replete cultures of 3 diatoms (Chaetoceros sp., Skeletonema costatum, Thalassiosira weissflogii) and 3 flagellates (Dunaliella tertiolecta, Pavlova lutheri, Prorocentrum minimum) to provide insight into the differences in nitrogen release patterns observed between these species. At NO3− concentrations <40 μmol‐N·L−1, all the diatom species and the dinoflagellate P. minimum exhibited saturating kinetics, whereas the other flagellates, D. tertiolecta and P. lutheri, did not saturate, leading to very high estimated K  s values. Above ∼60 μmol‐N·L−1, NO3− uptake rates of all species tested continued to increase in a linear fashion. Rates of NO3− uptake at 40 μmol‐N·L−1, normalized to cellular nitrogen, carbon, cell number, and surface area, were generally greater for diatoms than flagellates. Diatoms stored significant amounts of NO3− internally, whereas the flagellate species stored significant amounts of NH4+. Half‐saturation concentrations for NR and NiR were similar between all species, but diatoms had significantly lower temperature optima for NR and NiR than did the flagellates tested in most cases. Relative to calculated biosynthetic demands, diatoms were found to have greater NO3− uptake and NO3− reduction rates than flagellates. This enhanced capacity for NO3− uptake and reduction along with the lower optimum temperature for enzyme activity could explain differences in nitrogen release patterns between diatoms and flagellates after an increase in irradiance.

Harmful algal blooms in the Chesapeake and coastal bays of Maryland, USA: Comparison of 1997, 1998, and 1999 events

Harmful algal blooms in the Chesapeake Bay and coastal bays of Maryland, USA, are not a new phenomenon, but may be increasing in frequency and diversity. Outbreaks ofPfiesteria piscicida (Dinophyceae) were observed during 1997 in several Chesapeake Bay tributaries, while in 1998,Pfiesteria-related events were not found but massive blooms ofProrocentrum minimum (Dinophyceae) occurred. In 1999,Aureococcus anophagefferens (Pelagophyceae) developed in the coastal bays in early summer in sufficient densities to cause a brown tide. In 1997, toxicPfiesteria was responsible for fish kills at relatively low cell densities. In 1998 and 1999, the blooms ofP. minimum andA. anophagefferens were not toxic, but reached sufficiently high densities to have ecological consequences. These years differed in the amount and timing of rainfall events and resulting nutrient loading from the largely agricultural watershed. Nutrient loading to the eastern tributaries of Chesapeake Bay has been increasing over the past decade. Much of this nutrient delivery is in organic form. The sites of thePfiesteria outbreaks ranked among those with the highest organic loading of all sites monitored bay-wide. The availability of dissolved organic carbon and phosphorus were also higher at sites experiencingA. anophagefferens blooms than at those without blooms. The ability to supplement photosynthesis with grazing or organic substrates and to use a diversity of organic nutrients may play a role in the development and maintenance of these species. ForP. minimum andA. anophagefferens, urea is used preferentially over nitrate.Pfiesteria is a grazer, but also has the ability to take up nutrients directly. The timing of nutrient delivery may also be of critical importance in determining the success of certain species.

Total dissolved nitrogen analysis : comparisons between the persulfate, UV and high temperature oxidation methods

We compared the persulfate (PO), ultraviolet (UV), and high temperature oxidation (HTO) methods used to analyze total dissolved nitrogen (TDN) concentrations in aquatic samples to determine whether the three methods differed in terms of standard parameters (blanks, limits of detection and linearity, and precision) or in oxidation efficiency of standard compounds and field samples of varying salinity. The TDN concentrations of several N-containing standard compounds, as well as a humic mixture and a suite of field samples collected from the Sargasso Sea, Chesapeake Bay and an aquaculture pond were determined with the three methods. The PO method had the highest percent recoveries for the range of labile and refractory standard compounds tested (93±13). The HTO method yielded recoveries of 87±14; recoveries increased to 91±10 under optimized conditions. The standard UV method, with 30% H2O2 as the oxidant, was found to be highly variable, producing the lowest percent recoveries (71±21); the oxidation efficiency of the UV method increased substantially in subsequent trials (91±12), when the PO reagent was used in place of H2O2. In the field sample comparison, the PO, UV with PO reagent, and HTO method produced similar results (slopes of the Model II regression lines comparing them ranged from 1.00 to 1.05 with r2≥0.99). The standard UV method, however, produced concentrations 5% to 40% lower than the other methods. Analysis of the spectra emitted by the UV lamp used in this study suggests that variations in the UV spectra reaching the sample may have caused the reduced efficiencies. The poor recovery of some standard compounds with each of the methods suggests that concentrations of TDN, and subsequently DON, measured in the field with any of the methods will likely be underestimated to some degree depending on the composition of the TDN pool at that time. With careful attention to detail, however, the PO and HTO methods can provide reproducible results consistent with each other. The standard UV method, however, was found to be highly unpredictable in practice.

Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea

There are an estimated 1030 virioplankton in the world oceans, the majority of which are phages (viruses that infect bacteria). Marine phages encompass enormous genetic diversity, affect biogeochemical cycling of elements, and partially control aspects of prokaryotic production and diversity. Despite their importance, there is a paucity of data describing virioplankton distributions over time and depth in oceanic systems. A decade of high-resolution time-series data collected from the upper 300 m in the northwestern Sargasso Sea revealed recurring temporal and vertical patterns of virioplankton abundance in unprecedented detail. An annual virioplankton maximum developed between 60 and 100 m during periods of summer stratification and eroded during winter convective mixing. The timing and vertical positioning of this seasonal pattern was related to variability in water column stability and the dynamics of specific picophytoplankton and heterotrophic bacterioplankton lineages. Between 60 and 100 m, virioplankton abundance was negatively correlated to the dominant heterotrophic bacterioplankton lineage SAR11, as well as the less abundant picophytoplankton, Synechococcus. In contrast, virioplankton abundance was positively correlated to the dominant picophytoplankton lineage Prochlorococcus, and the less abundant alpha-proteobacteria, Rhodobacteraceae. Seasonally, virioplankton abundances were highly synchronous with Prochlorococcus distributions and the virioplankton to Prochlorococcus ratio remained remarkably constant during periods of water column stratification. The data suggest that a significant fraction of viruses in the mid-euphotic zone of the subtropical gyres may be cyanophages and patterns in their abundance are largely determined by Prochlorococcus dynamics in response to water column stability. This high-resolution, decadal survey of virioplankton abundance provides insight into the possible controls of virioplankton dynamics in the open ocean.

Temporal and Spatial Dynamics of Urea Uptake and Regeneration Rates and Concentrations in Chesapeake Bay

We examined the temporal and spatial variability of urea concentrations and urea uptake and regeneration rates collected on cruises along the longitudinal axis of the Chesapeake Bay between 1972 and 1998. Interannually, mean Bay-wide surface urea concentrations ranged between 0.49 and 0.91 μg-at N l−1 with a nearly 50% decrease in surface concentrations observed between 1988 and 1998. Concentrations of urea from samples collected within ∼1 m of the bottom were generally higher and much more varable than surface samples. Seasonally, two different patterns were observed in mean Bay-wide surface urea concentrations. Urea concentrations from near surface waters exhibited a clear summer peak for 1988 through 1994, while for 1973 and 1996 to 1998 a distinct winter-spring peak in concentration was observed. Urea concentrations from deeper waters showed a similar seasonal trend each year with peak concentrations measured in spring. Spatially, urea concentrations in the surface waters decreased in a conservative-type pattern from 0.91 μg-at N I−1 at the freshwater end member to 0.46 μg-at N I−1 at the ocean end member. Mean Bay-wide surface urea uptake rates displayed a seasonal pattern throughout the data set with maximum uptake rates (up to 0.33 μg-at N I−1 h−1) consistently observed during summer. Mean Bay-wide surface regeneration rates were highest but most variable during fall (1.63±0.82 μg-at N I−1 h−1). Mean urea uptake and regeneration rates displayed opposing spatial trends along the axis of the Bay with uptake rates being lowest in the North Bay where regeneration rates were highest. The average temporal and spatial patterns of urea concentration in Chesapeake Bay appear to reflect a balance between external inputs and internal biological recycling.

Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus

Significance Phosphorus is scarce in many subtropical ocean regions, and phytoplankton in these regions adjust their biochemical composition such that they require less of it. We show here that phytoplankton in the ultra–low-phosphorus Sargasso Sea are enriched in polyphosphate (polyP), a phosphorus molecule hitherto thought of primarily as a luxury storage product in marine phytoplankton. We further show that polyP appears to be more readily recycled in the surface ocean than other phosphorus-containing biochemicals. Thus, the high relative levels, and fast cycling, of polyP in low-phosphorus environments may form a feedback loop that contributes bioavailable phosphorus for primary production, potentially reducing the likelihood of growth limitation by phosphorus. Phytoplankton alter their biochemical composition according to nutrient availability, such that their bulk elemental composition varies across oceanic provinces. However, the links between plankton biochemical composition and variation in biogeochemical cycling of nutrients remain largely unknown. In a survey of phytoplankton phosphorus stress in the western North Atlantic, we found that phytoplankton in the phosphorus-depleted subtropical Sargasso Sea were enriched in the biochemical polyphosphate (polyP) compared with nutrient-rich temperate waters, contradicting the canonical oceanographic view of polyP as a luxury phosphorus storage molecule. The enrichment in polyP coincided with enhanced alkaline phosphatase activity and substitution of sulfolipids for phospholipids, which are both indicators of phosphorus stress. Further, polyP appeared to be liberated preferentially over bulk phosphorus from sinking particles in the Sargasso Sea, thereby retaining phosphorus in shallow waters. Thus, polyP cycling may form a feedback loop that attenuates the export of phosphorus when it becomes scarce, contributes bioavailable P for primary production, and supports the export of carbon and nitrogen via sinking particles.

Impact of ocean phytoplankton diversity on phosphate uptake

Significance Nutrient uptake is a central property of ocean biogeochemistry, but our understanding of this process is based on laboratory cultures or bulk environmental studies. Thus, mathematical descriptions of nutrient uptake, at the heart of most biogeochemical models, must rely on this limited information. Hence, we have little knowledge of how natural phytoplankton populations vary in their abilities to take up key nutrients. Using advanced analytical techniques, this study provides the first comprehensive in situ quantification of nutrient uptake capabilities among dominant phytoplankton groups. Supported by a model that considers plastic ecological responses in an evolutionary context, this work further provides a fundamentally new framework for the integration of microbial diversity to describe and understand the controls of ocean nutrient assimilation. We have a limited understanding of the consequences of variations in microbial biodiversity on ocean ecosystem functioning and global biogeochemical cycles. A core process is macronutrient uptake by microorganisms, as the uptake of nutrients controls ocean CO2 fixation rates in many regions. Here, we ask whether variations in ocean phytoplankton biodiversity lead to novel functional relationships between environmental variability and phosphate (Pi) uptake. We analyzed Pi uptake capabilities and cellular allocations among phytoplankton groups and the whole community throughout the extremely Pi-depleted western North Atlantic Ocean. Pi uptake capabilities of individual populations were well described by a classic uptake function but displayed adaptive differences in uptake capabilities that depend on cell size and nutrient availability. Using an eco-evolutionary model as well as observations of in situ uptake across the region, we confirmed that differences among populations lead to previously uncharacterized relationships between ambient Pi concentrations and uptake. Supported by novel theory, this work provides a robust empirical basis for describing and understanding assimilation of limiting nutrients in the oceans. Thus, it demonstrates that microbial biodiversity, beyond cell size, is important for understanding the global cycling of nutrients.

The counterintuitive effect of summer‐to‐fall mixed layer deepening on eukaryotic new production in the Sargasso Sea

The Sargasso Sea is characterized by strong summertime stratification that is thought to drive oligotrophy, but export production is surprisingly similar to that of high-latitude regions with ample major nutrient supply. Here we use the summer-to-fall progression in the northwestern Sargasso Sea to investigate the relationship between upper ocean stratification and phytoplankton nitrogen (N) uptake. Euphotic zone particles collected in July, October, and December were sorted by flow cytometry, and the 15N/14N of separated prokaryotic and eukaryotic phytoplankton was analyzed. The 15N/14N of Prochlorococcus and Synechococcus was always low, indicating uniform reliance on recycled N. In July and in two fall profiles, the 15N/14N of eukaryotic phytoplankton was high, reflecting consumption of subsurface nitrate. In three other fall profiles, eukaryotic 15N/14N was similar to prokaryote 15N/14N, suggesting a shift toward more complete reliance on recycled N. The progressive deepening of the mixed layer from summer to fall, although reducing the surface-to-deep density contrast, increases the density difference of the euphotic zone as a whole from underlying nutrient-rich waters, which may play a role in the observed decline in euphotic zone nitrate supply into the fall. The apparent summertime nitrate supply to the euphotic zone, when the mixed layer is shallowest, may help to explain the surprisingly high export production of the subtropical and tropical ocean.