Exploration of the Types of Rarity in the Arctic Ocean from the Perspective of Multiple Methodologies.

The Arctic Ocean is facing rapid environmental changes with cascading effects on the entire Arctic marine ecosystem. However, we have a limited understanding of the consequences such changes have on bacteria and archaea (prokaryotes) at the base of the marine food web. In this study, we show how the prokaryotic rare biosphere behaves over a range of highly heterogeneous environmental conditions using 16S rRNA gene reads from amplicon and metagenome sequencing data from seawater samples collected during the Norwegian young sea ICE expedition between late winter and early summer. The prokaryotic rare biosphere was analyzed using different approaches: amplicon sequence variants and operational taxonomic units from the 16S rRNA gene amplicons and operational taxonomic units from the 16S rRNA genes of the metagenomes. We found that prokaryotic rare biosphere communities are specific to certain water masses, and that the majority of the rare taxa identified were always rare and disappeared in at least one sample under changing conditions, suggesting their high sensitivity to environmental heterogeneity. In addition, our methodological comparison revealed a good performance of 16S rRNA gene amplicon sequencing in describing rare biosphere patterns, while the metagenome-derived data were better to capture a significant diversity of so-far uncultivated rare taxa. Our analysis on the dynamics of the rare prokaryotic biosphere, by combining different methodological approaches, improves the description of the types of rarity predicted from Community Assembly theory in the Arctic Ocean.

Diversity and Composition of Pelagic Prokaryotic and Protist Communities in a Thin Arctic Sea-Ice Regime.

One of the most prominent manifestations of climate change is the changing Arctic sea-ice regime with a reduction in the summer sea-ice extent and a shift from thicker, perennial multiyear ice towards thinner, first-year ice. These changes in the physical environment are likely to impact microbial communities, a key component of Arctic marine food webs and biogeochemical cycles. During the Norwegian young sea ICE expedition (N-ICE2015) north of Svalbard, seawater samples were collected at the surface (5 m), subsurface (20 or 50 m), and mesopelagic (250 m) depths on 9 March, 27 April, and 16 June 2015. In addition, several physical and biogeochemical data were recorded to contextualize the collected microbial communities. Through the massively parallel sequencing of the small subunit ribosomal RNA amplicon and metagenomic data, this work allows studying the Arctic's microbial community structure during the late winter to early summer transition. Results showed that, at compositional level, Alpha- (30.7%) and Gammaproteobacteria (28.6%) are the most frequent taxa across the prokaryotic N-ICE2015 collection, and also the most phylogenetically diverse. Winter to early summer trends were quite evident since there was a high relative abundance of thaumarchaeotes in the under-ice water column in late winter while this group was nearly absent during early summer. Moreover, the emergence of Flavobacteria and the SAR92 clade in early summer might be associated with the degradation of a spring bloom of Phaeocystis. High relative abundance of hydrocarbonoclastic bacteria, particularly Alcanivorax (54.3%) and Marinobacter (6.3%), was also found. Richness showed different patterns along the depth gradient for prokaryotic (highest at mesopelagic depth) and protistan communities (higher at subsurface depths). The microbial N-ICE2015 collection analyzed in the present study provides comprehensive new knowledge about the pelagic microbiota below drifting Arctic sea-ice. The higher microbial diversity found in late winter/early spring communities reinforces the need to continue with further studies to properly characterize the winter microbial communities under the pack-ice.

Deep carbon export from a Southern Ocean iron-fertilized diatom bloom.

Fertilization of the ocean by adding iron compounds has induced diatom-dominated phytoplankton blooms accompanied by considerable carbon dioxide drawdown in the ocean surface layer. However, because the fate of bloom biomass could not be adequately resolved in these experiments, the timescales of carbon sequestration from the atmosphere are uncertain. Here we report the results of a five-week experiment carried out in the closed core of a vertically coherent, mesoscale eddy of the Antarctic Circumpolar Current, during which we tracked sinking particles from the surface to the deep-sea floor. A large diatom bloom peaked in the fourth week after fertilization. This was followed by mass mortality of several diatom species that formed rapidly sinking, mucilaginous aggregates of entangled cells and chains. Taken together, multiple lines of evidence-although each with important uncertainties-lead us to conclude that at least half the bloom biomass sank far below a depth of 1,000 metres and that a substantial portion is likely to have reached the sea floor. Thus, iron-fertilized diatom blooms may sequester carbon for timescales of centuries in ocean bottom water and for longer in the sediments.

Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current.

Diatoms of the iron-replete continental margins and North Atlantic are key exporters of organic carbon. In contrast, diatoms of the iron-limited Antarctic Circumpolar Current sequester silicon, but comparatively little carbon, in the underlying deep ocean and sediments. Because the Southern Ocean is the major hub of oceanic nutrient distribution, selective silicon sequestration there limits diatom blooms elsewhere and consequently the biotic carbon sequestration potential of the entire ocean. We investigated this paradox in an in situ iron fertilization experiment by comparing accumulation and sinking of diatom populations inside and outside the iron-fertilized patch over 5 wk. A bloom comprising various thin- and thick-shelled diatom species developed inside the patch despite the presence of large grazer populations. After the third week, most of the thinner-shelled diatom species underwent mass mortality, formed large, mucous aggregates, and sank out en masse (carbon sinkers). In contrast, thicker-shelled species, in particular Fragilariopsis kerguelensis, persisted in the surface layers, sank mainly empty shells continuously, and reduced silicate concentrations to similar levels both inside and outside the patch (silica sinkers). These patterns imply that thick-shelled, hence grazer-protected, diatom species evolved in response to heavy copepod grazing pressure in the presence of an abundant silicate supply. The ecology of these silica-sinking species decouples silicon and carbon cycles in the iron-limited Southern Ocean, whereas carbon-sinking species, when stimulated by iron fertilization, export more carbon per silicon. Our results suggest that large-scale iron fertilization of the silicate-rich Southern Ocean will not change silicon sequestration but will add carbon to the sinking silica flux.

Wind-driven upwelling of iron sustains dense blooms and food webs in the eastern Weddell Gyre.

The Southern Ocean is a major sink of anthropogenic CO2 and an important foraging area for top trophic level consumers. However, iron limitation sets an upper limit to primary productivity. Here we report on a considerably dense late summer phytoplankton bloom spanning 9000 km2 in the open ocean of the eastern Weddell Gyre. Over its 2.5 months duration, the bloom accumulated up to 20 g C m-2 of organic matter, which is unusually high for Southern Ocean open waters. We show that, over 1997-2019, this open ocean bloom was likely driven by anomalies in easterly winds that push sea ice southwards and favor the upwelling of Warm Deep Water enriched in hydrothermal iron and, possibly, other iron sources. This recurring open ocean bloom likely facilitates enhanced carbon export and sustains high standing stocks of Antarctic krill, supporting feeding hot spots for marine birds and baleen whales.

A Winter-to-Summer Transition of Bacterial and Archaeal Communities in Arctic Sea Ice.

The Arctic is warming 2-3 times faster than the global average, leading to a decrease in Arctic sea ice extent, thickness, and associated changes in sea ice structure. These changes impact sea ice habitat properties and the ice-associated ecosystems. Sea-ice algal blooms provide various algal-derived carbon sources for the bacterial and archaeal communities within the sea ice. Here, we detail the transition of these communities from winter through spring to early summer during the Norwegian young sea ICE (N-ICE2015) expedition. The winter community was dominated by the archaeon Candidatus Nitrosopumilus and bacteria belonging to the Gammaproteobacteria (Colwellia, Kangiellaceae, and Nitrinocolaceae), indicating that nitrogen-based metabolisms, particularly ammonia oxidation to nitrite by Cand. Nitrosopumilus was prevalent. At the onset of the vernal sea-ice algae bloom, the community shifted to the dominance of Gammaproteobacteria (Kangiellaceae, Nitrinocolaceae) and Bacteroidia (Polaribacter), while Cand. Nitrosopumilus almost disappeared. The bioinformatically predicted carbohydrate-active enzymes increased during spring and summer, indicating that sea-ice algae-derived carbon sources are a strong driver of bacterial and archaeal community succession in Arctic sea ice during the change of seasons. This implies a succession from a nitrogen metabolism-based winter community to an algal-derived carbon metabolism-based spring/ summer community.

Secondary metabolite biosynthetic diversity in Arctic Ocean metagenomes.

Polyketide synthases (PKSs) and non-ribosomal peptide synthetases (NRPSs) are mega enzymes responsible for the biosynthesis of a large fraction of natural products (NPs). Molecular markers for biosynthetic genes, such as the ketosynthase (KS) domain of PKSs, have been used to assess the diversity and distribution of biosynthetic genes in complex microbial communities. More recently, metagenomic studies have complemented and enhanced this approach by allowing the recovery of complete biosynthetic gene clusters (BGCs) from environmental DNA. In this study, the distribution and diversity of biosynthetic genes and clusters from Arctic Ocean samples (NICE-2015 expedition), was assessed using PCR-based strategies coupled with high-throughput sequencing and metagenomic analysis. In total, 149 KS domain OTU sequences were recovered, 36 % of which could not be assigned to any known BGC. In addition, 74 bacterial metagenome-assembled genomes were recovered, from which 179 BGCs were extracted. A network analysis identified potential new NP families, including non-ribosomal peptides and polyketides. Complete or near-complete BGCs were recovered, which will enable future heterologous expression efforts to uncover the respective NPs. Our study represents the first report of biosynthetic diversity assessed for Arctic Ocean metagenomes and highlights the potential of Arctic Ocean planktonic microbiomes for the discovery of novel secondary metabolites. The strategy employed in this study will enable future bioprospection, by identifying promising samples for bacterial isolation efforts, while providing also full-length BGCs for heterologous expression.

A red tide in the pack ice of the Arctic Ocean.

In the Arctic Ocean ice algae constitute a key ecosystem component and the ice algal spring bloom a critical event in the annual production cycle. The bulk of ice algal biomass is usually found in the bottom few cm of the sea ice and dominated by pennate diatoms attached to the ice matrix. Here we report a red tide of the phototrophic ciliate Mesodinium rubrum located at the ice-water interface of newly formed pack ice of the high Arctic in early spring. These planktonic ciliates are not able to attach to the ice. Based on observations and theory of fluid dynamics, we propose that convection caused by brine rejection in growing sea ice enabled M. rubrum to bloom at the ice-water interface despite the relative flow between water and ice. We argue that red tides of M. rubrum are more likely to occur under the thinning Arctic sea ice regime.

Winter storms accelerate the demise of sea ice in the Atlantic sector of the Arctic Ocean.

A large retreat of sea-ice in the 'stormy' Atlantic Sector of the Arctic Ocean has become evident through a series of record minima for the winter maximum sea-ice extent since 2015. Results from the Norwegian young sea ICE (N-ICE2015) expedition, a five-month-long (Jan-Jun) drifting ice station in first and second year pack-ice north of Svalbard, showcase how sea-ice in this region is frequently affected by passing winter storms. Here we synthesise the interdisciplinary N-ICE2015 dataset, including independent observations of the atmosphere, snow, sea-ice, ocean, and ecosystem. We build upon recent results and illustrate the different mechanisms through which winter storms impact the coupled Arctic sea-ice system. These short-lived and episodic synoptic-scale events transport pulses of heat and moisture into the Arctic, which temporarily reduce radiative cooling and henceforth ice growth. Cumulative snowfall from each sequential storm deepens the snow pack and insulates the sea-ice, further inhibiting ice growth throughout the remaining winter season. Strong winds fracture the ice cover, enhance ocean-ice-atmosphere heat fluxes, and make the ice more susceptible to lateral melt. In conclusion, the legacy of Arctic winter storms for sea-ice and the ice-associated ecosystem in the Atlantic Sector lasts far beyond their short lifespan.

Particle availability controls agglutination in pelagic tintinnids in the Southern Ocean.

Mechanisms of particle selectivity controlling agglutination within the agglomerated tintinnid genus Stenosemella spp. Jörgensen were studied during two iron fertilisation experiments (EisenEx and EIFEX) conducted in the Southern Ocean in austral spring 2000 and late austral summer to early autumn 2004. Representative SEM pictures of Stenosemella spp. loricae were taken on the day of fertilisation, during the middle and at the end of both experiments. Whereas during EisenEx particles used for agglutination were unambiguously dominated by coccoliths of Emiliania huxleyi (Lohmann) Hay & Mohle, agglutinated particles during EIFEX mainly consisted of broken diatom frustules (BF) of heavily silicified species. This observation is supported by the ratio of E. huxleyi (Eh)/BF abundances in the water column during both experiments. During EisenEx we observed an Eh/BF ratio which was an order-of-magnitude higher compared to the EIFEX experiment. Thus, our results clearly indicated that particle availability seems to be the driving mechanism in the agglutination of Southern Ocean tintinnids. Furthermore, possible implications for the vertical flux of agglutinated biogenic particles to deep ocean waters and sediments are discussed.

Leads in Arctic pack ice enable early phytoplankton blooms below snow-covered sea ice.

The Arctic icescape is rapidly transforming from a thicker multiyear ice cover to a thinner and largely seasonal first-year ice cover with significant consequences for Arctic primary production. One critical challenge is to understand how productivity will change within the next decades. Recent studies have reported extensive phytoplankton blooms beneath ponded sea ice during summer, indicating that satellite-based Arctic annual primary production estimates may be significantly underestimated. Here we present a unique time-series of a phytoplankton spring bloom observed beneath snow-covered Arctic pack ice. The bloom, dominated by the haptophyte algae Phaeocystis pouchetii, caused near depletion of the surface nitrate inventory and a decline in dissolved inorganic carbon by 16 ± 6 g C m-2. Ocean circulation characteristics in the area indicated that the bloom developed in situ despite the snow-covered sea ice. Leads in the dynamic ice cover provided added sunlight necessary to initiate and sustain the bloom. Phytoplankton blooms beneath snow-covered ice might become more common and widespread in the future Arctic Ocean with frequent lead formation due to thinner and more dynamic sea ice despite projected increases in high-Arctic snowfall. This could alter productivity, marine food webs and carbon sequestration in the Arctic Ocean.

Stable composition of the nano- and picoplankton community during the ocean iron fertilization experiment LOHAFEX.

The iron fertilization experiment LOHAFEX was conducted in a cold-core eddy in the Southern Atlantic Ocean during austral summer. Within a few days after fertilization, a phytoplankton bloom developed dominated by nano- and picoplankton groups. Unlike previously reported for other iron fertilization experiments, a diatom bloom was prevented by iron and silicate co-limitation. We used 18S rRNA gene tag pyrosequencing to investigate the diversity of these morphologically similar cell types within the nano- and picoplankton and microscopically enumerated dominant clades after catalyzed reported deposition fluorescence in situ hybridization (CARD-FISH) with specific oligonucleotide probes. In addition to Phaeocystis, members of Syndiniales group II, clade 10-11, and the Micromonas clades ABC and E made up a major fraction of the tag sequences of the nano- and picoplankton community within the fertilized patch. However, the same clades were also dominant before the bloom and outside the fertilized patch. Furthermore, only little changes in diversity could be observed over the course of the experiment. These results were corroborated by CARD-FISH analysis which confirmed the presence of a stable nano- and picoplankton community dominated by Phaeocystis and Micromonas during the entire course of the experiment. Interestingly, although Syndiniales dominated the tag sequences, they could hardly be detected by CARD-FISH, possibly due to the intracellular parasitic life style of this clade. The remarkable stability of the nano- and picoplankton community points to a tight coupling of the different trophic levels within the microbial food web during LOHAFEX.

Floating ice-algal aggregates below melting arctic sea ice.

During two consecutive cruises to the Eastern Central Arctic in late summer 2012, we observed floating algal aggregates in the melt-water layer below and between melting ice floes of first-year pack ice. The macroscopic (1-15 cm in diameter) aggregates had a mucous consistency and were dominated by typical ice-associated pennate diatoms embedded within the mucous matrix. Aggregates maintained buoyancy and accumulated just above a strong pycnocline that separated meltwater and seawater layers. We were able, for the first time, to obtain quantitative abundance and biomass estimates of these aggregates. Although their biomass and production on a square metre basis was small compared to ice-algal blooms, the floating ice-algal aggregates supported high levels of biological activity on the scale of the individual aggregate. In addition they constituted a food source for the ice-associated fauna as revealed by pigments indicative of zooplankton grazing, high abundance of naked ciliates, and ice amphipods associated with them. During the Arctic melt season, these floating aggregates likely play an important ecological role in an otherwise impoverished near-surface sea ice environment. Our findings provide important observations and measurements of a unique aggregate-based habitat during the 2012 record sea ice minimum year.

Morphological adaptation of a planktonic diatom to growth in Antarctic sea ice.

Chaetoceros dichaeta Ehrenberg is one of the most important planktonic diatom species in the Southern Ocean, making a significant contribution to the total biomass in the region. Our observations on both field and culture material have revealed the existence of a specialized form of C. dichaeta adapted to living in sea ice. This sea ice form differs from the planktonic form by the shape and orientation of the setae and the aperture length between sibling cells. Thus, the diameter of the chain is equivalent to the apical axes of the cells and is accompanied by a two order of magnitude decrease in minimal space requirement. Here, we report for the first time on the extraordinary overwintering strategy of a planktonic diatom in sea ice facilitated by its rapid morphological adaptation to changing environmental conditions. This morphological plasticity enables it to thrive in the confined space of the sea ice brine matrix and retain its numerical dominance in recurrent growing seasons and has likely evolved to optimally exploit the dynamic ecosystem of the seasonally ice-covered seas of the Southern Ocean.

MORPHOLOGICAL VARIABILITY AND LIFE CYCLE TRAITS OF THE TYPE SPECIES OF THE DIATOM GENUS CHAETOCEROS, C. DICHAETA(1).

Chaetoceros dichaeta Ehrenb. is the type species of the genus Chaetoceros and is one of the dominant planktonic diatom species of the Southern Ocean. A number of varieties and forms have been described for C. dichaeta, which prompted us to investigate the morphological variability in clonal cultures to achieve a better circumscription of the morphological features of this species. We studied eight clonal cultures obtained from the type locality by sequencing the D1-D3 hypervariable domains of the LSU to assess their genetic identity, following cell-size reduction and sexual reproduction, and examining the morphological features of cells at different stages of the size reduction process using both LM and EM. Observation of sexual reproduction within clonal strains demonstrated that C. dichaeta is homothallic. The size and morphology of the cells vary considerably during size reduction: cell volume is reduced by over an order of magnitude, and the gradual diminution of the apical axis is accompanied by the elongation of the pervalvar axis. All forms and varieties described for C. dichaeta can be ascribed to the species, with the exception of C. dichaeta f. tenuiformis L. Mangin.