Giacomo R. DiTullio

Iron and manganese in the Ross Sea, Antarctica: Seasonal iron limitation in Antarctic shelf waters

Dissolved iron and manganese and total dissolvable iron were measured in water column samples collected from the polynya region of the southern Ross Sea during cruises in November–December 1994 (spring 1994) and December 1995 to January 1996 (summer 1995). Iron and manganese addition bottle incubation experiments were also performed during these cruises in order to assess the nutritional sufficiency of ambient iron and manganese concentrations for growth of the phytoplankton community. Generally high dissolved iron concentrations (>0.5 nM) and relatively complex iron and manganese vertical profiles were obtained during the spring 1994 cruise, compared with the summer 1995 data. Dissolved iron concentrations in the upper water column averaged 1.0 nM during spring 1994 and 0.23 nM in summer 1995, excluding two stations where concentrations exceeding 1 nM are attributed to inputs from melting sea ice. The observed differences in the distribution of iron and manganese between spring 1994 and summer 1995 are attributed to seasonal decreases in the up welling of bottom waters and melting of sea ice, which supply these metals into the upper water column, combined with the cumulative removal of iron and manganese from the water column throughout the spring and summer, due to biological uptake, vertical export and scavenging by suspended and sinking particles. Results of the metal addition bottle incubation experiments indicate that ambient dissolved iron concentrations are adequate for phytoplankton growth requirements during the spring and early summer, when algal production is highest and Phaeocystis antarctica dominates the algal community, whereas low dissolved iron concentrations limit algal community growth later in the summer, except in the stratified, iron-enriched waters near melting sea ice, where diatoms are able to bloom. Our observations and the inferred seasonal distributions of P. antarctica and diatoms in these waters suggest that iron availability and vertical mixing (i.e., irradiance) exert the primary controls on phytoplankton growth and community structure in the southern Ross Sea during the spring and summer.

Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea, Antarctica.

The Southern Ocean is very important for the potential sequestration of carbon dioxide in the oceans and is expected to be vulnerable to changes in carbon export forced by anthropogenic climate warming. Annual phytoplankton blooms in seasonal ice zones are highly productive and are thought to contribute significantly to pCO2 drawdown in the Southern Ocean. Diatoms are assumed to be the most important phytoplankton class with respect to export production in the Southern Ocean; however, the colonial prymnesiophyte Phaeocystis antarctica regularly forms huge blooms in seasonal ice zones and coastal Antarctic waters. There is little evidence regarding the fate of carbon produced by P. antarctica in the Southern Ocean, although remineralization in the upper water column has been proposed to be the main pathway in polar waters. Here we present evidence for early and rapid carbon export from P. antarctica blooms to deep water and sediments in the Ross Sea. Carbon sequestration from P. antarctica blooms may influence the carbon cycle in the Southern Ocean, especially if projected climatic changes lead to an alteration in the structure of the phytoplankton community.

Phytoplankton taxonomic variability in nutrient utilization and primary production in the Ross Sea

Patterns of nutrient utilization and primary productivity (PP) in late austral spring and early summer in the southwestern Ross Sea were characterized with respect to phytoplankton taxonomic composition, polynya dynamics, and upper ocean hydrography during the 1996–1997 oceanographic program Research on Ocean-Atmosphere Variability and Ecosystem Response in the Ross Sea. Phytoplankton biomass in the upper 150 m of the water column ranged from 40 to 540 mg chlorophyll a (Chl a) m−2, exceeding 200 mg Chl a m−2 everywhere except the extreme northern and eastern boundaries of the Ross Sea polynya. Diatom biomass was greatest in the shallow mixed layers of Terra Nova Bay, while the more deeply mixed waters of the Ross Sea polynya were dominated by Phaeocystis antarctica. Daily production computed from the disappearance of NO3 (1.14 g C m−2 d−1) and total dissolved inorganic carbon (TDIC, 1.29 g C m−2 d−1) is consistent with estimates made from an algorithm forced with satellite measurements of Chl a (1.25 g C m−2 d−1) and from measurements of 14C uptake (1.33 g C m−2 d−1). Phytoplankton PP in the Ross Sea averaged 100 g C m−2 yr−1 during 1996–1997. Despite the early formation of the Terra Nova Bay polynya the diatom bloom there did not reach its peak PP until middle to late January 1997 (most likely because of more intense wind mixing in November), ∼6 weeks after the P. antarctica bloom in the Ross Sea polynya had reached the same stage of development. From 70 to 100% of the C and N deficits in the upper 150 m could be accounted for by particulate organic matter, indicating that there had been little dissolved organic matter production or export of particulate material prior to our cruise. This suggests that early in the season, PP and zooplankton grazing are decoupled in the southwestern Ross Sea. The NO3∶PO4 disappearance ratio in waters dominated by P. antarctica (19.0±0.61) was significantly greater than in waters where diatoms were most common (9.52±0.33), and both were significantly different from the Redfield N∶P ratio of 16. Vertical profiles of TDIC suggest that P. antarctica took up 110% more CO2 per mole of PO4 removed than did diatoms, an important consideration for climate models that estimate C uptake from the removal of PO4.

Temporal and spatial patterns in the Ross Sea: Phytoplankton biomass, elemental composition, productivity and growth rates

The temporal and spatial patterns of phytoplankton biomass, productivity, and particulate matter composition in the Ross Sea were assessed during cruises in January 1990 and February 1992. Biomass and primary productivity in the southern Ross Sea were greatest during mid-January, with surface chlorophyll concentrations, particulate organic carbon levels, and integrated primary productivity averaging 4.9 μg L−1, 0.54 mg L−1 and 2.63 g C m−2 d−1, respectively. Comparable mean concentrations and rates for February were 1.1 μg L−1, 0.29 mg L−1, and 0.78 g C m−2 d−1 (decreases of 76, 46, and 70%, respectively), indicative of the scale of temporal changes. A distinct south-north transition also was observed both in productivity and phytoplankton biomass, with the lowest values occurring in the northern Ross Sea. East-west gradients in phytoplankton biomass and composition occurred within the southern Ross Sea. The areal productivity of the Ross Sea ranged from 0.15 to 2.85 g C m−2 d−1 and is among the highest found in the entire Antarctic. Carbon:chlorophyll ratios were uniformly high but were highest (150) in 1990 in the diatom-dominated western Ross Sea. Surface growth rates were modest, averaging less than 0.2 day−1 during both seasons. We hypothesize that the marked seasonality in the region provides an environment in which net growth rates, although slow, are maximized through low loss rates and which allows biomass to accumulate in the surface layer. Furthermore, the temporal variations are quantitatively similar to the observed spatial variations. Therefore the dominant determinant of phytoplankton biomass and productivity at any one point on the Ross Sea continental shelf is the stage of the seasonal growth cycle.

Spatial patterns in phytoplankton biomass and pigment distributions in the Ross Sea

The distribution of phytoplankton biomass and pigments was determined in the Ross Sea during late austral summer 1992. Large gradients in biomass were noted both in the east-west and north-south direction, with maximum particulate matter concentrations occurring in the southwest portion of the Ross Sea. Two xanthophyll pigments dominated the profiles, fucoxanthin (indicative of diatoms) and 19′ hexanoyloxyfucoxanthin (hex) (indicative of the prymnesiophyte Phaeocystis antarctica). Fucoxanthin concentrations were greatest near the coast of Victoria Land and within the northern transect, whereas hex concentrations were highest offshore in the SE Ross Sea. Particulate carbon:chlorophyll a (POC:chl) ratios in diatom-dominated waters of the western Ross Sea were relatively high (210). The POC:chl ratio for Phaeocystis antarctica populations from the SE Ross Sea was substantially less (92) than the ratios observed in diatom-dominated waters. Pigment 14C labeling indicated that phytoplankton carbon in the diatom-dominated northern Ross Sea accounted for approximately 30% of the POC, with a phytoplankton C:chl ratio of 130. Short-term (24 hour) vertical fluxes of pigments ranged from 3 to 40 μg chl a m−2 d−1. Diatom-dominated regions had greater fluxes of phaeophorbides, suggesting that metazoans were the most important grazers at these locations. In contrast, the phaeophytin/total phaeopigment ratio was highest in waters dominated by Phaeocystis antarctica. The distribution of phytoplankton biomass and pigments revealed a spatially variable distribution of taxa, one which clearly has important consequences to food-web dynamics, biogeochemical cycles, and vertical flux patterns in the Ross Sea.

Limitation of algal growth by iron deficiency in the Australian Subantarctic region

In March 1998 we measured iron in the upper water column and conducted iron- and nutrient-enrichment bottle-incubation experiments in the open-ocean Subantarctic region southwest of Tasmania, Australia. In the Subtropical Convergence Zone (∼42°S, 142°E), silicic acid concentrations were low (< 1.5 µM) in the upper water column, whereas pronounced vertical gradients in dissolved iron concentration (0.12-0.84 nM) were observed, presumably reflecting the interleaving of Subtropical and Subantarctic waters, and mineral aerosol input. Results of a bottle-incubation experiment performed at this location indicate that phytoplankton growth rates were limited by iron deficiency within the iron-poor layer of the euphotic zone. In the Subantarctic water mass (∼46.8°S, 142°E), low concentrations of dissolved iron (0.05-0.11 nM) and silicic acid (< 1 µM) were measured throughout the upper water column, and our experimental results indicate that algal growth was limited by iron deficiency. These observations suggest that availability of dissolved iron is a primary factor limiting phytoplankton growth over much of the Subantarctic Southern Ocean in the late summer and autumn.

Cobalt and nickel in the Peru upwelling region: A major flux of labile cobalt utilized as a micronutrient

behaved as a micronutrient with correlations with major nutrients (nitrate, phosphate; r 2 = 0.90, 0.96) until depleted to � 50 pM of strongly complexed cobalt. Co:P utilization ratios were an order of magnitude higher than in the North Pacific, comparable to utilization rates of zinc in other oceanic regions. Cobalt speciation measurements showed that available cobalt decreased over 4 orders of magnitude in this region, with shifts in phytoplankton assemblages occurring at transitions between labile and nonlabile cobalt. Only small changes in total dissolved nickel were observed, and nickel was present in a labile chemical form throughout the region. In the Peru upwelling region, cobalt uptake was highest at the surface and decreased with depth, suggesting phytoplankton uptake was a more important removal mechanism than co-oxidation with microbial manganese oxidation. These findings show the importance of cobalt as a micronutrient and that cobalt scarcity and speciation may be important in influencing phytoplankton species composition in this economically important environment. INDEX TERMS: 1030 Geochemistry: Geochemical cycles (0330); 1050 Geochemistry: Marine geochemistry (4835, 4850); 1065 Geochemistry: Trace elements (3670); 4279 Oceanography: General: Upwelling and convergences;

Multiple nutrient stresses at intersecting pacific ocean biomes detected by protein biomarkers

Protein markers of cyanobacterial stress Nutrients including iron, nitrogen, and phosphorus limit primary productivity in the oceans. Determining how abundant cyanobacteria such as Prochlorococcus adapt to nutrient stress across marine settings requires accurate molecular assays. Saito et al. developed a proteomic and metaproteomic approach capable of targeting specific metabolic biomarkers from mixed communities in seawater (see the Perspective by Moore). Prochlorococcus proteins are indicative of a major limiting nutrient across a wide transect in the Pacific Ocean; however, they also show that the limitation of multiple nutrients at overlapping biomes is an additional source of stress. Science, this issue p. 1173; see also p. 1120 The composition of cyanobacterial proteins reflects nutrient stress in central Pacific Ocean ecosystems. [Also see Perspective by Moore] Marine primary productivity is strongly influenced by the scarcity of required nutrients, yet our understanding of these nutrient limitations is informed by experimental observations with sparse geographical coverage and methodological limitations. We developed a quantitative proteomic method to directly assess nutrient stress in high-light ecotypes of the abundant cyanobacterium Prochlorococcus across a meridional transect in the central Pacific Ocean. Multiple peptide biomarkers detected widespread and overlapping regions of nutritional stress for nitrogen and phosphorus in the North Pacific Subtropical Gyre and iron in the equatorial Pacific. Quantitative protein analyses demonstrated simultaneous stress for these nutrients at biome interfaces. This application of proteomic biomarkers to diagnose ocean metabolism demonstrated Prochlorococcus actively and simultaneously deploying multiple biochemical strategies for low-nutrient conditions in the oceans.

Particulate Dimethylsulfoniopropionate Removal and Dimethylsulfide Production by Zooplankton in the Southern Ocean

The influence of Antarctic krill, Euphausia superba, on particulate dimethlysulfoniopropionate (DMSP(p)) and dimethylsulfide (DMS) concentrations in surface waters of the Southern Ocean was investigated by shipboard experiments during austral spring near the Antarctic Peninsula. Chlorophyll concentrations were low in the water column, but substantially higher in sea ice due to the high biomass of ice algae, predominantly pennate diatoms. A comparison of DMSP(p) concentrations and algal accessory pigments indicated that DMSP(p) was associated primarily with diatoms (fucoxanthin) and to a minor extent with Phaeocystis spp. (19’-hexanoyloxyfucoxanthin) in sea ice algae. Maximum DMSP(p) and fucoxanthin concentrations also occurred in the 100-200 μm size fraction. We interpret this to mean that high biomass of diatoms in sea ice contributes significantly to DMSP(p) pools in the Antarctic.

Novel molecular determinants of viral susceptibility and resistance in the lipidome of Emiliania huxleyi.

Viruses play a key role in controlling the population dynamics of algae, including Emiliania huxleyi, a globally distributed haptophyte with calcite coccoliths that comprise ca. 50% of the sinking carbonate flux from the surface ocean. Emiliania huxleyi viruses (EhVs) routinely infect and terminate E. huxleyi blooms. EhVs are surrounded by a lipid envelope, which we found to be comprised largely of glycosphingolipids (GSLs) with lesser amounts of polar glycerolipids. Infection appears to involve membrane fusion between the virus and host, and we hypothesized that specific polar lipids may facilitate virus attachment. We identified three novel intact polar lipids in E. huxleyi strain CCMP 374 and EhV86, including a GSL with a monosaccharide sialic acid headgroup (sGSL); for all 11 E. huxleyi strains we tested, there was a direct relationship between sGSL content and sensitivity to infection by EhV1, EhV86 and EhV163. In mesocosms, the E. huxleyi population with greatest initial sGSL content had the highest rate of virus-induced mortality. We propose potential physiological roles for sGSL that would be beneficial for growth but leave cells susceptible to infection, thus furthering the discussion of Red Queen-based co-evolution and the cost(s) of sensitivity and resistance in the dynamic E. huxleyi-EhV system.