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Increasing contributions of prymnesiophytes such as Phaeocystis pouchetii and Emiliania huxleyi to Barents Sea (BS) phytoplankton production have been suggested based on in situ observations of phytoplankton community composition, but the scattered and discontinuous nature of these records confounds simple inference of community change or its relationship to salient environmental variables. However, provided that meaningful assessments of phytoplankton community composition can be inferred based on their optical characteristics, ocean-colour records offer a potential means to develop a synthesis between sporadic in situ observations. Existing remote-sensing algorithms to retrieve phytoplankton functional types based on chlorophyll-a ( chl-a ) concentration or indices of pigment packaging may, however, fail to distinguish Phaeocystis from other blooms of phytoplankton with high pigment packaging, such as diatoms. We develop a novel algorithm to distinguish major phytoplankton functional types in the BS and apply it to the MODIS-Aqua ocean-colour record, to study changes in the composition of BS phytoplankton blooms in July, between 2002 and 2018, creating time series of the spatial distribution and intensity of coccolithophore, diatom and Phaeocystis blooms. We confirm a north-eastward expansion in coccolithophore bloom distribution, identified in previous studies, and suggest an inferred increase in chl-a concentrations, reported by previous researchers, may be partly explained by increasing frequencies of Phaeocystis blooms. This article is part of the theme issue ‘The changing Arctic Ocean: consequences for biological communities, biogeochemical processes and ecosystem functioning’.

Measures to reduce eutrophication have often led to a more effective decline of phosphorus (P) than nitrogen (N) concentrations. The resultant changes in riverine nutrient loads can cause an increase in the N : P ratios of coastal waters. During four research cruises along a 450 km transect, we investigated how reductions in nutrient inputs during the past 25 yr have affected nutrient limitation patterns in the North Sea. This revealed a strong offshore gradient of dissolved inorganic N : P ratios in spring, from 375 : 1 nearshore toward 1 : 1 in the central North Sea. This gradient was reflected in high nearshore N : P and C : P ratios of particulate organic matter (mainly phytoplankton), indicative of severe P deficiency of coastal phytoplankton, which may negatively affect higher trophic levels in the food web. Nutrient enrichment bioassays performed on-board showed P and Si limitation of phytoplankton growth nearshore, co-limitation of N and P in a transitional region, and N limitation in the outer-shore waters, confirming the existence of an offshore gradient from P to N limitation. Different species were limited by different nutrients, indicating that further reductions of P loads without concomitant reductions of N loads will suppress colonial Phaeocystis blooms, but will be less effective in diminishing harmful algal blooms by dino- and nanoflagellates. Hence, our results provide evidence that de-eutrophication efforts in northwestern Europe have led to a large imbalance in the N : P stoichiometry of coastal waters of the North Sea, with major consequences for the growth, species composition, and nutritional quality of marine phytoplankton communities.

Iron and light are recognized as limiting factors controlling Southern Ocean phytoplankton growth. Recent field-based evidence suggests, however, that manganese availability may also play a role. Here we examine the influence of iron and manganese on protein expression and physiology in Phaeocystis antarctica , a key Antarctic primary producer. We provide taxon-specific proteomic evidence to show that in-situ Southern Ocean Phaeocystis populations regularly experience stress due to combined low manganese and iron availability. In culture, combined low iron and manganese induce large-scale changes in the Phaeocystis proteome and result in reorganization of the photosynthetic apparatus. Natural Phaeocystis populations produce protein signatures indicating late-season manganese and iron stress, consistent with concurrently observed stimulation of chlorophyll production upon additions of manganese or iron. These results implicate manganese as an important driver of Southern Ocean productivity and demonstrate the utility of peptide mass spectrometry for identifying drivers of incomplete macronutrient consumption. Low manganese availability could be a major control of phytoplankton growth in the Southern Ocean. Here the authors identify proteomic signatures of low manganese and iron availability in phytoplankton cultures and detect those signatures in Antarctic field samples.

Light-dependent growth of phytoplankton is a fundamental process in marine ecosystems, but we lack a comprehensive view of how light utilization traits vary across genotypes and species, and how this variation is structured by cell size, taxonomy, and environmental gradients. Here, we compile 308 growth-irradiance experiments performed on 119 species of marine phytoplankton from all major functional groups, and characterize growth-irradiance relationships in terms of the initial slope of the growth-irradiance curve (a), the optimal irradiance above which growth declines (I opt), and the maximum growth rate (μ max). We find that a declines with increasing cell size, although cell size appears to be a weak constraint on this trait. There are significant differences across taxa in α and μ max, with dinoflagellates, raphidophytes, and diazotrophs having the lowest values for both traits, and Phaeocystis spp. and diatoms having relatively high values. I opt does not vary among taxonomic groups, and all traits exhibit large variation within most groups. Open-ocean isolates tend to have higher α, lower I opt, and lower μ max than coastal isolates, implying adaptation to low light and low productivity. The three traits are correlated across species such that α and I opt are negatively related while μ max is positively correlated with both of these traits. There is some evidence that high a carries a cost of high N demand even when nitrogen (not light) is limiting. The results elucidate contrasting light-related ecological strategies across phytoplankton and should help improve the parameterization of major functional groups in biogeochemical models.

In the future, temperature and iron availability are predicted to change in the coastal polynyas of Antarctica, which are the most biologically productive regions of the Southern Ocean. We examined the individual and combined effects of iron addition (+500 nM) and temperature increase (4°C) on Phaeocystis antarctica and several dominant diatom species isolated from the McMurdo Sound sector of the Ross Sea. Iron addition increased growth, carbon fixation, iron uptake rates, cellular carbon quota, and cell size of almost all tested species, while temperature increase only affected certain species. Concurrent increases in temperature and iron synergistically stimulated the growth rates of some species, particularly Pseudo-nitzschia subcurvata. The diversified responses of these phytoplankton to iron and temperature may help explain the current spatial and temporal distributions of diatoms and prymnesiophytes in the Ross Sea. In the future, potential temperature and iron increases may promote the growth of the diatoms Chaetoceros sp., Fragilariopsis cylindrus, and especially P. subcurvata. In contrast, growth rates of P. antarctica did not increase at higher temperatures, suggesting that a shift in community composition toward diatoms may occur under warmer conditions in this biologically and biogeochemically important Southern Ocean polynya region.

We report results of laboratory studies examining the effect of low levels of iron (Fe) availability on the intracellular Fe concentrations and specific growth rates in Southern Ocean diatoms (Fragilariopsis kerguelensis, Eucampia antarctica, Proboscia inermis, and Thalassiosira antarctica) and Phaeocystis antarctica. All species grew on Fe complexed to the siderophore desferrioxamine B (DFB). Concentrations of DFB up to 100-fold in excess of Fe were required to limit growth rates by ≥ 50%. Southern Ocean phytoplankton also grew on Fe complexed by ≥ 10-fold excess concentrations of the siderophores ferrichrome, enterobactin, or aerobactin, whereas the temperate coastal diatoms Thalassiosira weissflogii and Thalassiosira pseudonana did not. Intracellular Fe concentrations and Fe : C ratios of all Southern Ocean species were exceptionally low and decreased with decreasing Fe availability. However, large diatoms had significantly lower cell-volume–normalized Fe content and Fe : C ratios than Phaeocystis. Short-term Fe uptake and extracellular Fe(II) production measurements provided evidence that Phaeocystis possesses a reductive Fe transport pathway. Our findings demonstrate that the large-diatom Fe requirements are at least 2-fold lower than currently reported for oceanic algal species and suggest that bioreduction may enable resident phytoplankton to directly use Fe bound to strong organic ligands.

Increasing contributions of prymnesiophytes such as Phaeocystis pouchetii and Emiliania huxleyi to Barents Sea (BS) phytoplankton production have been suggested based on in situ observations of phytoplankton community composition, but the scattered and discontinuous nature of these records confounds simple inference of community change or its relationship to salient environmental variables. However, provided that meaningful assessments of phytoplankton community composition can be inferred based on their optical characteristics, ocean-colour records offer a potential means to develop a synthesis between sporadic in situ observations. Existing remote-sensing algorithms to retrieve phytoplankton functional types based on chlorophyll-a (chl-a) concentration or indices of pigment packaging may, however, fail to distinguish Phaeocystis from other blooms of phytoplankton with high pigment packaging, such as diatoms. We develop a novel algorithm to distinguish major phytoplankton functional types in the BS and apply it to the MODIS-Aqua ocean-colour record, to study changes in the composition of BS phytoplankton blooms in July, between 2002 and 2018,creating time series of the spatial distribution and intensity of coccolithophore, diatom and Phaeocystis blooms. We confirm a north-eastward expansion in coccolithophore bloom distribution, identified in previous studies, and suggest an inferred increase in chl-a concentrations, reported by previous researchers, may be partly explained by increasing frequencies of Phaeocystis blooms. This article is part of the theme issue ‘The changing Arctic Ocean: consequences for biological communities, biogeochemical processes and ecosystem functioning’.

Massive phytoplankton blooms, like the recurrent Phaeocystis proliferation observed every year in the Eastern English Channel (EEC), have a significant influence on the overall planktonic community structure and their food web dynamics. As well as being an important area for local fisheries, the EEC is an ideal ecosystem for work on microbial diversity. This is because, although its environmental context is relatively complex, it is reasonably well understood due to several years of monitoring and morphological observations of its planktonic organisms. The objective of our study was to better understand the under-explored microbial eukaryotic diversity relative to the Phaeocystis bloom. The community structure of microplankton (diatoms, haptophytes, ciliates and dinoflagellates) was studied through morphological observations and tag pyrosequencing. During the annual Phaeocystis spring bloom, the phytoplankton biomass increased by 34-fold, while the microzooplankton biomass showed a 4-fold increase, representing on average about 4.6% of the biomass of their phytoplankton prey. Tag pyrosequencing unveiled an extensive diversity of Gymnodiniaceae, with G. spirale and G. fusiformis representing the most abundant reads. An extended diversity of Phaeocystales, with partial 18S rDNA genes sequence identity as low as 85% was found, with taxa corresponding to P. globosa, but also to unknown Phaeocystaceae. Morphological analyses and pyrosequencing were generally in accordance with capturing frequency shifts of abundant taxa. Tag pyrosequencing allowed highlighting the maintenance of microplankton diversity during the Phaeocystis bloom and the increase of the taxa presenting low number of reads (minor taxa) along with the dominant ones in response to biotic and/or abiotic changing conditions. Although molecular approaches have enhanced our perception on diversity, it has come to light that the challenge of modelling and predicting ecological change requires the use of different complementary approaches, to link taxonomic data with the functional roles of microbes in biogeochemical cycles.

Phaeocystis antarctica is an important phytoplankter of the Ross Sea where it dominates the early season bloom after sea ice retreat and is a major contributor to carbon export. The factors that influence Phaeocystis colony formation and the resultant Ross Sea bloom initiation have been of great scientific interest, yet there is little known about the underlying mechanisms responsible for these phenomena. Here, we present laboratory and field studies on Phaeocystis antarctica grown under multiple iron conditions using a coupled proteomic and transcriptomic approach. P. antarctica had a lower iron limitation threshold than a Ross Sea diatom Chaetoceros sp., and at increased iron nutrition (> 120 pM Fe') a shift from flagellate cells to a majority of colonial cells in P. antarctica was observed, implying a role for iron as a trigger for colony formation. Proteome analysis revealed an extensive and coordinated shift in proteome structure linked to iron availability and life cycle transitions with 327 and 436 proteins measured as significantly different between low and high iron in strains 1871 and 1374, respectively. The enzymes flavodoxin and plastocyanin that can functionally replace iron metalloenzymes were observed at low iron treatments consistent with cellular iron-sparing strategies, with plastocyanin having a larger dynamic range. The numerous isoforms of the putative iron-starvation-induced protein (ISIP) group (ISIP2A and ISIP3) had abundance patterns coinciding with that of either low or high iron (and coincident flagellate or the colonial cell types in strain 1871), implying that there may be specific iron acquisition systems for each life cycle type. The proteome analysis also revealed numerous structural proteins associated with each cell type: within flagellate cells actin and tubulin from flagella and haptonema structures as well as a suite of calcium-binding proteins with EF domains were observed. In the colony-dominated samples a variety of structural proteins were observed that are also often found in multicellular organisms including spondins, lectins, fibrillins, and glycoproteins with von Willebrand domains. A large number of proteins of unknown function were identified that became abundant at either high or low iron availability. These results were compared to the first metaproteomic analysis of a Ross Sea Phaeocystis bloom to connect the mechanistic information to the in situ ecology and biogeochemistry. Proteins associated with both flagellate and colonial cells were observed in the bloom sample consistent with the need for both cell types within a growing bloom. Bacterial iron storage and B12 biosynthesis proteins were also observed consistent with chemical synergies within the colony microbiome to cope with the biogeochemical conditions. Together these responses reveal a complex, highly coordinated effort by P. antarctica to regulate its phenotype at the molecular level in response to iron and provide a window into the biology, ecology, and biogeochemistry of this group.

Phaeocystis is a cosmopolitan, bloom-forming phytoplankton genus that contributes significantly to global carbon and sulfur cycles. During blooms, Phaeocystis species produce large carbon-rich colonies, creating a unique interface for bacterial interactions. While bacteria are known to interact with phytoplankton— e.g ., they promote growth by producing phytohormones and vitamins—such interactions have not been shown for Phaeocystis . Therefore, we investigated the composition and function of P. globosa microbiomes. Specifically, we tested whether microbiome compositions are consistent across individual colonies from four P. globosa strains, whether similar microbiomes are re-recruited after antibiotic treatment, and how microbiomes affect P. globosa growth under limiting conditions. Results illuminated a core colonial P. globosa microbiome—including bacteria from the orders Alteromonadales , Burkholderiales , and Rhizobiales —that was re-recruited after microbiome disruption. Consistent microbiome composition and recruitment is indicative that P. globosa microbiomes are stable-state systems undergoing deterministic community assembly and suggests there are specific, beneficial interactions between Phaeocystis and bacteria. Growth experiments with axenic and nonaxenic cultures demonstrated that microbiomes allowed continued growth when B-vitamins were withheld, but that microbiomes accelerated culture collapse when nitrogen was withheld. In sum, this study reveals symbiotic and opportunistic interactions between Phaeocystis colonies and microbiome bacteria that could influence large-scale phytoplankton bloom dynamics and biogeochemical cycles.