Search

Thaumarchaea are among the most abundant microbial groups in the ocean, but controls on their abundance and the distribution and metabolic potential of different subpopulations are poorly constrained. Here, two ecotypes of ammonia-oxidizing thaumarchaea were quantified using ammonia monooxygenase (amoA) genes across the equatorial Pacific Ocean. The shallow, or water column “A” (WCA), ecotype was the most abundant ecotype at the depths of maximum nitrification rates, and its abundance correlated with other biogeochemical indicators of remineralization such as NO3 : Si and total Hg. Metagenomes contained thaumarchaeal genes encoding for the catalytic subunit of the urease enzyme (ureC) at all depths, suggesting that members of both WCA and the deep, water column “B” (WCB) ecotypes may contain ureC. Coupled urea hydrolysis-ammonia oxidation rates were similar to ammonia oxidation rates alone, suggesting that urea could be an important source of ammonia for mesopelagic ammonia oxidizers. Potential inducement of metal limitation of both ammonia oxidation and urea hydrolysis was demonstrated via additions of a strong metal chelator. The water column inventory of WCA was correlated with the depth-integrated abundance of WCB, with both likely controlled by the flux of sinking particulate organic matter, providing strong evidence of vertical connectivity between the ecotypes. Further, depth-integrated amoA gene abundance and nitrification rates were correlated with particulate organic nitrogen flux measured by contemporaneously deployed sediment traps. Together, the results refine our understanding of the controls on thaumarchaeal distributions in the ocean, and provide new insights on the relationship between material flux and microbial communities in the mesopelagic.

Summary 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.

We present full-depth zonal sections of total dissolved cobalt, iron, manganese, and labile cobalt from the South Atlantic Ocean. A basin-scale plume from the African coast appeared to be a major source of dissolved metals to this region, with high cobalt concentrations in the oxygen minimum zone of the Angola Dome and extending 2500 km into the subtropical gyre. Metal concentrations were elevated along the coastal shelf, likely due to reductive dissolution and resuspension of particulate matter. Linear relationships between cobalt, N2O, and O2, as well as low surface aluminum supported a coastal rather than atmospheric cobalt source. Lateral advection coupled with upwelling, biological uptake, and remineralization delivered these metals to the basin, as evident in two zonal transects with distinct physical processes that exhibited different metal distributions. Scavenging rates within the coastal plume differed for the three metals; iron was removed fastest, manganese removal was 2.5 times slower, and cobalt scavenging could not be discerned from water mass mixing. Because scavenging, biological utilization, and export constantly deplete the oceanic inventories of these three hybrid-type metals, point sources of the scale observed here likely serve as vital drivers of their oceanic cycles. Manganese concentrations were elevated in surface waters across the basin, likely due to coupled redox processes acting to concentrate the dissolved species there. These observations of basin-scale hybrid metal plumes combined with the recent projections of expanding oxygen minimum zones suggest a potential mechanism for effects on ocean primary production and nitrogen fixation via increases in trace metal source inputs.

Primary production in the Ross Sea, one of the most productive areas in the Southern Ocean, has previously been shown to be seasonally limited by iron. In two of three bottle incubation experiments conducted in the austral summer, significantly higher chlorophyll a (Chl a) concentrations were measured upon the addition of iron and B12, relative to iron additions alone. Initial bacterial abundances were significantly lower in the two experiments that showed phytoplankton stimulation upon addition of B12 and iron relative to the experiment that did not show this stimulation. This is consistent with the hypothesis that the bacteria and archaea in the upper water column are an important source of B12 to marine phytoplankton. The addition of iron alone increased the growth of Phaeocystis antarctica relative to diatoms, whereas in an experiment where iron and B12 stimulated total phytoplankton growth, the diatom Pseudonitzschia subcurvata went from comprising approximately 70% of the phytoplankton community to over 90%. Cobalt additions, with and without iron, did not alter Chl a biomass relative to controls and iron additions alone in the Ross Sea. Iron and vitamin B12 plus iron treatments caused reductions in the DMSP (dimethyl sulfoniopropionate) : Chl a ratio relative to the control and B12 treatments, consistent with the notion of an antioxidant function for DMSP. These results demonstrate the importance of a vitamin to phytoplankton growth and community composition in the marine environment.

Phytoplankton community structure in the eastern Equatorial Pacific (EEP) and the Peru upwelling system was determined using ChemTax analysis of pigment data. Photosynthetic efficiencies (F v : F m ), concentrations of macronutrients, iron (Fe), and the redox proteins flavodoxin (Flv) and ferredoxin (Fd) were used to assess the physiological status of the algal communities with respect to Fe. Diel periodicity in F v :F m ratios was observed in Fe-stressed populations of Prochlorococcus and type 4 haptophytes (Phaeocystis) in the EEP with daytime values (0.05-0.30) displaying a distinct noontime minimum. On the Peruvian continental shelf, upwelling of Fe-rich subsurface waters led to massive diatom blooms (reaching chlorophyll a [Chl a] values >45 μg L -1 ) with near-maximal photosynthetic efficiencies (F v : F m >0.6). Assimilation and luxurious uptake of Fe, scavenging processes, and Ek-man transport off the shelf break led to rapid decreases in Fe concentration and dramatic shifts in phytoplankton assemblages. The shelf break region was dominated by cryptophyte populations with relatively high photosynthetic competency (F v :F m = 0.4-0.5). In this region, subnanomolar Fe concentrations limited further diatom growth. As Fe concentrations decreased offshore, haptophyte (coccolithophorids and Phaeocystis) populations contributed approximately 40-80% toward the total Chl a concentration. Haptophyte populations were Fe stressed, as determined by high Flv indices (Flv [Flv + Fd] -1 ) and low photosynthetic efficiencies (F v : F m ∼0.3). The Flv index was very high in regions where Fe concentrations were ≤0.2 nmol L -1 , but it was 0 when Fe levels were >0.4 nmol L -1 . In the Peru upwelling, Fe concentrations between 0.2 and 0.4 nmol L -1 represented a transitional region that marked the threshold switch in community Fd and Flv expression.

Lake Bonney is a permanently ice-covered lake in the McMurdo Dry Valleys, Antarctica. The lake has two chemically stratified lobes (referred to as the east and west lobes), each with distinct biogenic sulfur profiles. Dimethylsulfoniopropionate (DMSPp) and dimethylsulfoxide (DMSOp) exceeded 32 and 2 nmol L 21 , respectively, in the photic surface waters of the lake. Maximum DMSPp levels occurred in the deep-chlorophyll layer of both lobes, a zone dominated by chrysophytes and chlorophytes, which are thought to be the source of dimethylated sulfur in the deep waters of the lake following sedimentation and biogeochemical processing. Waters beneath the chemoclines of both lobes are cold (,08C), saline (.3 times seawater), suboxic, and devoid of phytoplankton biomass and activity. Dimethylsulfide (DMS) levels (.330 nmol L 21 ) in the deep west lobe are among the highest recorded in a natural aquatic ecosystem. In contrast, saline waters of the deep east lobe contain relatively little DMS (,70 nmol L 21 ) but high DMSOd (270 nmol L 21 ), with the latter being the highest observed in any natural aquatic ecosystem. We argue that the differences in the biogenic sulfur profiles between the deep waters of the two lobes arise principally from subtle differences in the redox conditions found in each lobe.

Inputs of low concentrations of new and regenerated forms of nitrogen (≤1 µM) have large impacts on phytoplankton community structure and ocean biogeochemistry in the oligotrophic central gyres. However, current manipulative experimental methods cannot effectively simulate low-level, continuous supplies of nitrate, such as those from upwelling or eddy events, or steady-state inputs of regenerated ammonium and dissolved organic nitrogen from zooplankton grazing. Using a new shipboard continuous culture system based on laboratory chemostat methodology, we compared the effects of a continuous supply of 1 µM nitrate, ammonium, and urea-N at a dilution rate of 0.5 d−1 on algal community composition in the North Atlantic. In the Gulf Stream, continuous inputs of 1 µM nitrate dramatically changed phytoplankton community structure from dominance by cyanobacteria to dominance by diatoms. Equimolar continuous supplies of ammonium resulted in much smaller increases in total phytoplankton biomass, and favored a community co-dominated by diatoms and cyanobacteria, and promoted the growth of pelagophytes. In the Sargasso Sea, continuous 1 µM urea-N inputs greatly increased the biomass and dominance of Synechococcus relative to the initial community and compared with control and 1 µM nitrate additions. The shipboard natural community continuous culture system is uniquely suited for realistically simulating inputs of low levels of limiting nutrients, allowing new types of prognostic enrichment experiments that give novel insights into the processes that control phytoplankton community structure in the ocean.

We investigated phytoplankton Fe limitation using shipboard incubation experiments in the high-nutrient South American eastern boundary current regime. Low ambient Fe concentrations (;0.1 nM) in water collected from the Humboldt and Peru Currents were supplemented with a range of added Fe levels up to 2.5 nM. Phytoplankton chlorophyll a, photosystem II photosynthetic efficiency, and nitrate and phosphate drawdown increased in proportion to the amount of Fe added. The Humboldt Current algal community after Fe additions included colonial and flagellated Phaeocystis globosa and large pennate diatoms, whereas the Peru Upwelling assemblage was dominated by coccolithophorids and small pennate diatoms. Apparent half-saturation constants for growth of the two communities were 0.17 nM Fe (Humboldt Current) and 0.26 nM Fe (Peru Upwelling). Net molar dissolved Si(OH)4 : NO drawdown ratios were low in both experiments (;0.2‐0.7), but net particulate silica to nitrogen production 2 3 ratios were higher. Fe limitation decreased net NO : PO utilization ratios in the Humboldt Current incubation to 2 32 34 well below Redfield values. Phytoplankton community sinking rates were decreased by Fe additions in the Peru Upwelling, suggesting potential Fe effects on carbon export. Our results confirm that primary producers in the Peru Upwelling/Humboldt Current system can be limited by Fe, but the biological and biogeochemical consequences of Fe limitation differ from Fe-limited California coastal upwelling waters that have been previously studied.

Although Fe limitation is well documented in open ocean high -nutrient, low -chlorophyll (HNLC) areas, little is known about the potential for Fe limitation in coastal environments. We present a series of four Fe addition experiments that demonstrate varying degrees of Fe limitation in the central California coastal upwelling area. Fe concentrations vary widely here ( 8.0 nM) because inputs from rivers and resuspended shelf sediments are unevenly distributed. The biological response to Fe availability is also extremely variable. Fe-replete areas experience extensive blooms of large diatoms and almost complete depletion of nutrients. In slightly Fe-stressed areas, Fe limits the growth of large diatoms but does not control nutrient biogeochemistry or growth of other planktonic organisms. In severely Fe-limited waters, Fe exerts a fundamental control on nitrate and silicic acid drawdown, particulate organic carbon production, and the growth of phytoplankton, zooplankton, and bacteria. We propose a four -level classification scheme for Fe limitation in coastal California waters. Each level is characterized by a set of specific biological and biogeochemical responses to Fe. Parameters that show a characteristic response to Fe addition and thus define a region's Fe limitation status include particulate Si:N and Si:C production ratios, NO3− and H2SiO3 drawdown, C fixation, large diatom and picoplankton growth, bacterial production, and zooplankton grazing and biomass. Fe limitation of coastal upwelling regions needs to be recognized as an important biogeochemical process that could profoundly affect global new production and carbon cycling. The physical, chemical, and biological complexity of coastal upwelling regimes requires that Fe limitation effects be addressed with a more sophisticated approach than has generally been used to describe oceanic HNLC regimes.

We investigated biological Fe recycling in plankton communities from two contrasting marine ecosystems, the equatorial Pacific and Monterey Bay, California. Our experiments involved addition of cultured cyanobacteria and diatoms labeled with Fe radiotracer to natural plankton communities. Transfer of label into the natural community was followed by size fractionation and microautoradiography, and intracellular Fe was determined with titanium wash techniques. We documented the transfer of labeled Fe from added cyanobacteria to indigenous large cells in both environments and from large diatoms to indigenous small cells in the equatorial Pacific. Microautoradiography and Ti washing verified that transfer occurred from and into intracellular fractions in Monterey Bay experiments, although substantial amounts of transferred Fe were also found to be surface-adsorbed or associated with detritus. We argue that, as is the case for N, recycling of cellular Fe to support regenerated production could be an important component of marine ecosystem dynamics, especially in areas low in Fe.

A 6-d nutrient enrichment experiment was performed in the tropical North Pacific Ocean at 9”N, 147”W with ultraclean techniques. Changes in phytoplankton biomass, C and N assimilation rates, growth rates, and species composition were monitored with HPLC pigment analyses and flow cytometry techniques, as well as 14C fixation into particulate C, pigments, and protein. Prochlorophyte specific growth rates (from divinyl Chl a labeling) increased from an initial value of 0.15 d -I to 0.96 d-l following macronutrient addition (N, P, and Si). Diatoms, however, were unable to grow without added Fe. Diatom populations were severely colimited by Fe and macronutrients but achieved a specific growth rate of 2.5 d -’ following Fe and macronutrient additions. Results implied that grazing rates (g) on prochlorophytes were stimulated in approximate balance with prochlorophyte growth (p) after 6 d (g : p = O.SS), but that grazing processes were not as efficient (g: p = 0.40) at controlling the diatom standing stock. Our results suggest that grazing processes may be the most important factor regulating procaryotic biomass, but Fc limitation is the proximate control of diatom biomass and hence may limit the utilization of macronutrients in the equatorial Pacific Ocean.

Concentrations of phytoplankton and NO{sub 3} are consistently low and high in surface waters of the oceanic eastern and central equatorial Pacific, and phytoplankton populations are dominated by small solitary phytoplankton. Growth rates of natural phytoplankton populations, needed to assess the relative importance of many of the processes considered in the equatorial Pacific, were estimated by several methods. The growth rates of natural phytoplankton populations were found to be {approximately}0.7 d{sup {minus}1} or 1 biomass doubling d{sup {minus}1} and were similar for all methods. To keep this system in its observed balance requires that loss rates approximate observed growth rates. Grazing rates, measured with a dilution grazing experiment, were high, accounting for a large fraction of the daily production. Additions of various forms of Fe to 5-7-d incubations utilizing ultraclean techniques resulted in significant shifts in autotrophic and heterotrophic assemblages between initial samples, controls, and Fe enrichments, which were presumably due to Fe, grazing by both protistan and metazoan components, and incubation artifacts. Estimated growth rates of small pennate diatoms showed increases in Fe enrichments with respect to controls. The growth rates of the pennate diatoms were similar to those estimated for the larger size fraction of the natural populations.

The feasibility of estimating phytoplankton N uptake in N-limited systems by measuring the rate of 14CO2 incorporation into protein was studied using laboratory cultures and field populations. The accuracy of the method depends on the fact that the N:C ratio in protein is remarkably constant and that under N limitation a rather constant percentage (85%) of phytoplankton N is incorporated into protein. Results showed that incubations of 5–6 h are required to yield accurate estimates of N uptake due to internal cycling of amino acids before that. Estimates of phytoplankton N:C ratios based on field studies implied a positive correlation between distance from land and degree of N limitation.