The Arctic summer microbiome across Fram Strait: Depth, longitude, and substrate concentrations structure microbial diversity in the euphotic zone.

The long-term dynamics of microbial communities across geographic, hydrographic, and biogeochemical gradients in the Arctic Ocean are largely unknown. To address this, we annually sampled polar, mixed, and Atlantic water masses of the Fram Strait (2015-2019; 5-100 m depth) to assess microbiome composition, substrate concentrations, and oceanographic parameters. Longitude and water depth were the major determinants (~30%) of microbial community variability. Bacterial alpha diversity was highest in lower-photic polar waters. Community composition shifted from west to east, with the prevalence of, for example, Dadabacteriales and Thiotrichales in Arctic- and Atlantic-influenced waters, respectively. Concentrations of dissolved organic carbon peaked in the western, compared to carbohydrates in the chlorophyll-maximum of eastern Fram Strait. Interannual differences due to the time of sampling, which varied between early (June 2016/2018) and late (September 2019) phytoplankton bloom stages, illustrated that phytoplankton composition and resulting availability of labile substrates influence bacterial dynamics. We identified 10 species clusters with stable environmental correlations, representing signature populations of distinct ecosystem states. In context with published metagenomic evidence, our microbial-biogeochemical inventory of a key Arctic region establishes a benchmark to assess ecosystem dynamics and the imprint of climate change.

Annual cycle of downward particle fluxes on each side of the Gakkel Ridge in the central Arctic Ocean.

Two mooring arrays carrying sediment traps were deployed from September 2011 to August 2012 at ∼83°N on each side of the Gakkel Ridge in the Nansen and Amundsen Basins to measure downward particle flux below the euphotic zone (approx. 250 m) and approximately 150 m above seafloor at approximately 3500 and 4000 m depth, respectively. In a region that still experiences nearly complete ice cover throughout the year, export fluxes of total particulate matter (TPM), particulate organic carbon (POC), particulate nitrogen (PN), biogenic matter, lithogenic matter, biogenic particulate silica (bPSi), calcium carbonate (CaCO3), protists and biomarkers only slightly decreased with depth. Seasonal variations of particulate matter fluxes were similar on both sides of the Gakkel Ridge. Somewhat higher export rates in the Amundsen Basin and differences in the composition of the sinking TPM and bPSi on each side of the Gakkel Ridge probably reflected the influence of the Lena River/Transpolar Drift in the Amundsen Basin and the influence of Atlantic water in the Nansen Basin. Low variations in particle export with depth revealed a limited influence of lateral advection in the deep barren Eurasian Basin. This article is part of the theme issue 'The changing Arctic Ocean: consequences for biological communities, biogeochemical processes and ecosystem functioning'.

Limited sinking of Phaeocystis during a 12 days sediment trap study.

There is a controversy discussion about the contribution of the genus Phaeocystis to the vertical carbon export with evidence for and against sedimentation of Phaeocystis. So far, the presence of Phaeocystis in sinking matter was investigated with methods depending on morphological features (microscopy) and fast degradable substances (biochemical analyses). In this study, we determine the occurrence and abundance of Phaeocystis antarctica in short-term sediment traps and the overlying water column during a 12-day time period in the Atlantic sector of the Southern Ocean with 454-pyrosequencing and microscopy counting. In the sediment trap samples, we only found few sequences belonging to Phaeocystis, which was not reflecting the situation in the water column above. The cell counts showed the same results. We conclude that Phaeocystis cells are not generally transported downwards by active sinking or other sinking processes.

Picoeukaryote plankton composition off West Spitsbergen at the entrance to the Arctic Ocean.

Investigation of marine eukaryotic picoplankton composition is limited by missing morphological features for appropriate identification. Consequently, molecular methods are required. In this study, we used 454-pyrosequencing to study picoplankton communities at four stations in the West Spitsbergen Current (WSC; Fram Strait). High abundances of Micromonas pusilla were detected in the station situated closest to Spitsbergen, as seen in surveys of picoplankton assemblages in the Beaufort Sea. At the other three stations, other phylotypes, affiliating with Phaeocystis pouchetii and Syndiniales in the phylogenetic tree, were present in high numbers, dominating most of them. The picoplankton community structures at three of the stations, all with similar salinity and temperature, were alike. At the fourth station, the influence of the East Spitsbergen Current, transporting cold water from the Barents Sea around Spitsbergen, causes different abiotic parameters that result in a significantly different picoeukaryote community composition, which is dominated by M. pusilla. This observation is particularly interesting with regard to ongoing environmental changes in the Arctic. Ongoing warming of the WSC could convey a new picoplankton assemblage into the Arctic Ocean, which may come to affect the dominance of M. pusilla.

Release of ballast material during sea-ice melt enhances carbon export in the Arctic Ocean.

Globally, the most intense uptake of anthropogenic carbon dioxide (CO2) occurs in the Atlantic north of 50°N, and it has been predicted that atmospheric CO2 sequestration in the Arctic Ocean will increase as a result of ice-melt and increased primary production. However, little is known about the impact of pan-Arctic sea-ice decline on carbon export processes. We investigated the potential ballasting effect of sea-ice derived material on settling aggregates and carbon export in the Fram Strait by combining 13 years of vertical flux measurements with benthic eDNA analysis, laboratory experiments, and tracked sea-ice distributions. We show that melting sea-ice in the Fram Strait releases cryogenic gypsum and terrigenous material, which ballasts sinking organic aggregates. As a result, settling velocities of aggregates increased ≤10-fold, resulting in ≤30% higher carbon export in the vicinity of the melting ice-edge. Cryogenic gypsum is formed in first-year sea-ice, which is predicted to increase as the Arctic is warming. Simultaneously, less sea-ice forms over the Arctic shelves, which is where terrigenous material is incorporated into sea-ice. Supporting this, we found that terrigenous fluxes from melting sea-ice in the Fram Strait decreased by >80% during our time-series. Our study suggests that terrigenous flux will eventually cease when enhanced sea-ice melt disrupts trans-Arctic sea-ice transport and thus, limit terrigenous-ballasted carbon flux. However, the predicted increase in Arctic primary production and gypsum formation may enhance gypsum-ballasted carbon flux and compensate for lowered terrigenous fluxes. It is thus unclear if sea-ice loss will reduce carbon export in the Arctic Ocean.

Unprecedented insights into extents of biological responses to physical forcing in an Arctic sub-mesoscale filament by combining high-resolution measurement approaches.

In Fram Strait, we combined underway-sampling using the remote-controlled Automated Filtration System for Marine Microbes (AUTOFIM) with CTD-sampling for eDNA analyses, and with high-resolution optical measurements in an unprecedented approach to determine variability in plankton composition in response to physical forcing in a sub-mesoscale filament. We determined plankton composition and biomass near the surface with a horizontal resolution of ~ 2 km, and addressed vertical variability at five selected sites. Inside and near the filament, plankton composition was tightly linked to the hydrological dynamics related to the presence of sea ice. The comprehensive data set indicates that sea-ice melt related stratification near the surface inside the sub-mesoscale filament resulted in increased sequence abundances of sea ice-associated diatoms and zooplankton near the surface. In analogy to the physical data set, the underway eDNA data, complemented with highly sampled phytoplankton pigment data suggest a corridor of 7 km along the filament with enhanced photosynthetic biomass and sequence abundances of sea-ice associated plankton. Thus, based on our data we extrapolated an area of 350 km2 in Fram Strait with enhanced plankton abundances, possibly leading to enhanced POC export in an area that is around a magnitude larger than the visible streak of sea-ice.

Sea-ice melt determines seasonal phytoplankton dynamics and delimits the habitat of temperate Atlantic taxa as the Arctic Ocean atlantifies.

The Arctic Ocean is one of the regions where anthropogenic environmental change is progressing most rapidly and drastically. The impact of rising temperatures and decreasing sea ice on Arctic marine microbial communities is yet not well understood. Microbes form the basis of food webs in the Arctic Ocean, providing energy for larger organisms. Previous studies have shown that Atlantic taxa associated with low light are robust to more polar conditions. We compared to which extent sea ice melt influences light-associated phytoplankton dynamics and biodiversity over two years at two mooring locations in the Fram Strait. One mooring is deployed in pure Atlantic water, and the second in the intermittently ice-covered Marginal Ice Zone. Time-series analysis of amplicon sequence variants abundance over a 2-year period, allowed us to identify communities of co-occurring taxa that exhibit similar patterns throughout the annual cycle. We then examined how alterations in environmental conditions affect the prevalence of species. During high abundance periods of diatoms, polar phytoplankton populations dominated, while temperate taxa were weakly represented. Furthermore, we found that polar pelagic and ice-associated taxa, such as Fragilariopsis cylindrus and Melosira arctica, were more common in Atlantic conditions, while temperate taxa, such as Odontella aurita and Proboscia alata, were less abundant under polar conditions. This suggests that sea ice melt may act as a barrier to the northward expansion of temperate phytoplankton, preventing their dominance in regions still strongly influenced by polar conditions. Our findings highlight the complex interactions between sea ice melt, phytoplankton dynamics, and biodiversity in the Arctic.

Genetic and Structural Diversity of Prokaryotic Ice-Binding Proteins from the Central Arctic Ocean.

Ice-binding proteins (IBPs) are a group of ecologically and biotechnologically relevant enzymes produced by psychrophilic organisms. Although putative IBPs containing the domain of unknown function (DUF) 3494 have been identified in many taxa of polar microbes, our knowledge of their genetic and structural diversity in natural microbial communities is limited. Here, we used samples from sea ice and sea water collected in the central Arctic Ocean as part of the MOSAiC expedition for metagenome sequencing and the subsequent analyses of metagenome-assembled genomes (MAGs). By linking structurally diverse IBPs to particular environments and potential functions, we reveal that IBP sequences are enriched in interior ice, have diverse genomic contexts and cluster taxonomically. Their diverse protein structures may be a consequence of domain shuffling, leading to variable combinations of protein domains in IBPs and probably reflecting the functional versatility required to thrive in the extreme and variable environment of the central Arctic Ocean.

Atlantic water influx and sea-ice cover drive taxonomic and functional shifts in Arctic marine bacterial communities.

The Arctic Ocean is experiencing unprecedented changes because of climate warming, necessitating detailed analyses on the ecology and dynamics of biological communities to understand current and future ecosystem shifts. Here, we generated a four-year, high-resolution amplicon dataset along with one annual cycle of PacBio HiFi read metagenomes from the East Greenland Current (EGC), and combined this with datasets spanning different spatiotemporal scales (Tara Arctic and MOSAiC) to assess the impact of Atlantic water influx and sea-ice cover on bacterial communities in the Arctic Ocean. Densely ice-covered polar waters harboured a temporally stable, resident microbiome. Atlantic water influx and reduced sea-ice cover resulted in the dominance of seasonally fluctuating populations, resembling a process of "replacement" through advection, mixing and environmental sorting. We identified bacterial signature populations of distinct environmental regimes, including polar night and high-ice cover, and assessed their ecological roles. Dynamics of signature populations were consistent across the wider Arctic; e.g. those associated with dense ice cover and winter in the EGC were abundant in the central Arctic Ocean in winter. Population- and community-level analyses revealed metabolic distinctions between bacteria affiliated with Arctic and Atlantic conditions; the former with increased potential to use bacterial- and terrestrial-derived substrates or inorganic compounds. Our evidence on bacterial dynamics over spatiotemporal scales provides novel insights into Arctic ecology and indicates a progressing Biological Atlantification of the warming Arctic Ocean, with consequences for food webs and biogeochemical cycles.

Impact of preservation method and storage period on ribosomal metabarcoding of marine microbes: Implications for remote automated samplings.

Automated sampling technologies can enhance the temporal and spatial resolution of marine microbial observations, particularly in remote and inaccessible areas. A critical aspect of automated microbiome sampling is the preservation of nucleic acids over long-term autosampler deployments. Understanding the impact of preservation method on microbial metabarcoding is essential for implementing genomic observatories into existing infrastructure, and for establishing best practices for the regional and global synthesis of data. The present study evaluates the effect of two preservatives commonly used in autosampler deployments (mercuric chloride and formalin) and two extraction kits (PowerWater and NucleoSpin) on amplicon sequencing of 16S and 18S rRNA gene over 50 weeks of sample storage. Our results suggest the combination of mercuric chloride preservation and PowerWater extraction as most adequate for 16S and 18S rRNA gene amplicon-sequencing from the same seawater sample. This approach provides consistent information on species richness, diversity and community composition in comparison to control samples (nonfixed, filtered and frozen) when stored up to 50 weeks at in situ temperature. Preservation affects the recovery of certain taxa, with specific OTUs becoming overrepresented (SAR11 and diatoms) or underrepresented (Colwellia and pico-eukaryotes) after preservation. In case eukaryotic sequence information is the sole target, formalin preservation and NucleoSpin extraction performed best. Our study contributes to the design of long-term autonomous microbial observations in remote ocean areas, allowing cross-comparison of microbiome dynamics across sampling devices (e.g., water and particle samplers) and marine realms.

Phytoplankton Surveys in the Arctic Fram Strait Demonstrate the Tiny Eukaryotic Alga Micromonas and Other Picoprasinophytes Contribute to Deep Sea Export.

Critical questions exist regarding the abundance and, especially, the export of picophytoplankton (≤2 µm diameter) in the Arctic. These organisms can dominate chlorophyll concentrations in Arctic regions, which are subject to rapid change. The picoeukaryotic prasinophyte Micromonas grows in polar environments and appears to constitute a large, but variable, proportion of the phytoplankton in these waters. Here, we analyze 81 samples from the upper 100 m of the water column from the Fram Strait collected over multiple years (2009−2015). We also analyze sediment trap samples to examine picophytoplankton contributions to export, using both 18S rRNA gene qPCR and V1-V2 16S rRNA Illumina amplicon sequencing to assess the Micromonas abundance within the broader diversity of photosynthetic eukaryotes based on the phylogenetic placement of plastid-derived 16S amplicons. The material sequenced from the sediment traps in July and September 2010 showed that 11.2 ± 12.4% of plastid-derived amplicons are from picoplanktonic prasinophyte algae and other green lineage (Viridiplantae) members. In the traps, Micromonas dominated (83.6 ± 21.3%) in terms of the overall relative abundance of Viridiplantae amplicons, specifically the species Micromonas polaris. Temporal variations in Micromonas abundances quantified by qPCR were also observed, with higher abundances in the late-July traps and deeper traps. In the photic zone samples, four prasinophyte classes were detected in the amplicon data, with Micromonas again being the dominant prasinophyte, based on the relative abundance (89.4 ± 8.0%), but with two species (M. polaris and M. commoda-like) present. The quantitative PCR assessments showed that the photic zone samples with higher Micromonas abundances (>1000 gene copies per mL) had significantly lower standing stocks of phosphate and nitrate, and a shallower average depth (20 m) than those with fewer Micromonas. This study shows that despite their size, prasinophyte picophytoplankton are exported to the deep sea, and that Micromonas is particularly important within this size fraction in Arctic marine ecosystems.

Host-parasitoid associations in marine planktonic time series: Can metabarcoding help reveal them?

In this study, we created a dataset of a continuous three-year 18S metabarcoding survey to identify eukaryotic parasitoids, and potential connections to hosts at the Long-Term Ecological Research station Helgoland Roads. The importance of parasites and parasitoids for food web dynamics has previously been recognized mostly in terrestrial and freshwater systems, while marine planktonic parasitoids have been understudied in comparison to those. Therefore, the occurrence and role of parasites and parasitoids remains mostly unconsidered in the marine environment. We observed high abundances and diversity of parasitoid operational taxonomic units in our dataset all year round. While some parasitoid groups were present throughout the year and merely fluctuated in abundances, we also detected a succession of parasitoid groups with peaks of individual species only during certain seasons. Using co-occurrence and patterns of seasonal occurrence, we were able to identify known host-parasitoid dynamics, however identification of new potential host-parasitoid interactions was not possible due to their high dynamics and variability in the dataset.

The polar night shift: seasonal dynamics and drivers of Arctic Ocean microbiomes revealed by autonomous sampling.

The Arctic Ocean features extreme seasonal differences in daylight, temperature, ice cover, and mixed layer depth. However, the diversity and ecology of microbes across these contrasting environmental conditions remain enigmatic. Here, using autonomous samplers and sensors deployed at two mooring sites, we portray an annual cycle of microbial diversity, nutrient concentrations and physical oceanography in the major hydrographic regimes of the Fram Strait. The ice-free West Spitsbergen Current displayed a marked separation into a productive summer (dominated by diatoms and carbohydrate-degrading bacteria) and regenerative winter state (dominated by heterotrophic Syndiniales, radiolarians, chemoautotrophic bacteria, and archaea). The autumn post-bloom with maximal nutrient depletion featured Coscinodiscophyceae, Rhodobacteraceae (e.g. Amylibacter) and the SAR116 clade. Winter replenishment of nitrate, silicate and phosphate, linked to vertical mixing and a unique microbiome that included Magnetospiraceae and Dadabacteriales, fueled the following phytoplankton bloom. The spring-summer succession of Phaeocystis, Grammonema and Thalassiosira coincided with ephemeral peaks of Aurantivirga, Formosa, Polaribacter and NS lineages, indicating metabolic relationships. In the East Greenland Current, deeper sampling depth, ice cover and polar water masses concurred with weaker seasonality and a stronger heterotrophic signature. The ice-related winter microbiome comprised Bacillaria, Naviculales, Polarella, Chrysophyceae and Flavobacterium ASVs. Low ice cover and advection of Atlantic Water coincided with diminished abundances of chemoautotrophic bacteria while others such as Phaeocystis increased, suggesting that Atlantification alters microbiome structure and eventually the biological carbon pump. These insights promote the understanding of microbial seasonality and polar night ecology in the Arctic Ocean, a region severely affected by climate change.

Selective feeding in Southern Ocean key grazers-diet composition of krill and salps.

Over the past decades, two key grazers in the Southern Ocean (SO), krill and salps, have experienced drastic changes in their distribution and abundance, leading to increasing overlap of their habitats. Both species occupy different ecological niches and long-term shifts in their distributions are expected to have cascading effects on the SO ecosystem. However, studies directly comparing krill and salps are lacking. Here, we provide a direct comparison of the diet and fecal pellet composition of krill and salps using 18S metabarcoding and fatty acid markers. Neither species' diet reflected the composition of the plankton community, suggesting that in contrast to the accepted paradigm, not only krill but also salps are selective feeders. Moreover, we found that krill and salps had broadly similar diets, potentially enhancing the competition between both species. This could be augmented by salps' ability to rapidly reproduce in favorable conditions, posing further risks to krill populations.

Sea-ice derived meltwater stratification slows the biological carbon pump: results from continuous observations.

The ocean moderates the world's climate through absorption of heat and carbon, but how much carbon the ocean will continue to absorb remains unknown. The North Atlantic Ocean west (Baffin Bay/Labrador Sea) and east (Fram Strait/Greenland Sea) of Greenland features the most intense absorption of anthropogenic carbon globally; the biological carbon pump (BCP) contributes substantially. As Arctic sea-ice melts, the BCP changes, impacting global climate and other critical ocean attributes (e.g. biodiversity). Full understanding requires year-round observations across a range of ice conditions. Here we present such observations: autonomously collected Eulerian continuous 24-month time-series in Fram Strait. We show that, compared to ice-unaffected conditions, sea-ice derived meltwater stratification slows the BCP by 4 months, a shift from an export to a retention system, with measurable impacts on benthic communities. This has implications for ecosystem dynamics in the future warmer Arctic where the seasonal ice zone is expected to expand.

Uncovering the intricacies of microbial community dynamics at Helgoland Roads at the end of a spring bloom using automated sampling and 18S meta-barcoding.

In May 2016, the remote-controlled Automated Filtration System for Marine Microbes (AUTOFIM) was implemented in parallel to the Long Term Ecological Research (LTER) observatory Helgoland Roads in the German Bight. We collected samples for characterization of dynamics within the eukaryotic microbial communities at the end of a phytoplankton bloom via 18S meta-barcoding. Understanding consequences of environmental change for key marine ecosystem processes, such as phytoplankton bloom dynamics requires information on biodiversity and species occurrences with adequate temporal and taxonomic resolution via time series observations. Sampling automation and molecular high throughput methods can serve these needs by improving the resolution of current conventional marine time series observations. A technical evaluation based on an investigation of eukaryotic microbes using the partial 18S rRNA gene suggests that automated filtration with the AUTOFIM device and preservation of the plankton samples leads to highly similar 18S community profiles, compared to manual filtration and snap freezing. The molecular data were correlated with conventional microscopic counts. Overall, we observed substantial change in the eukaryotic microbial community structure during the observation period. A simultaneous decline of diatom and ciliate sequences succeeded a peak of Miracula helgolandica, suggesting a potential impact of these oomycete parasites on diatom bloom dynamics and phenology in the North Sea. As oomycetes are not routinely counted at Helgoland Roads LTER, our findings illustrate the benefits of combining automated filtration with metabarcodingto augment classical time series observations, particularly for taxa currently neglected due to methodological constraints.

Chytrid fungi distribution and co-occurrence with diatoms correlate with sea ice melt in the Arctic Ocean.

Global warming is rapidly altering physicochemical attributes of Arctic waters. These changes are predicted to alter microbial networks, potentially perturbing wider community functions including parasite infections and saprotrophic recycling of biogeochemical compounds. Specifically, the interaction between autotrophic phytoplankton and heterotrophic fungi e.g. chytrids (fungi with swimming tails) requires further analysis. Here, we investigate the diversity and distribution patterns of fungi in relation to abiotic variables during one record sea ice minimum in 2012 and explore co-occurrence of chytrids with diatoms, key primary producers in these changing environments. We show that chytrid fungi are primarily encountered at sites influenced by sea ice melt. Furthermore, chytrid representation positively correlates with sea ice-associated diatoms such as Fragilariopsis or Nitzschia. Our findings identify a potential future scenario where chytrid representation within these communities increases as a consequence of ice retreat, further altering community structure through perturbation of parasitic or saprotrophic interaction networks.

Erratum to: Rapid succession drives spring community dynamics of small protists at Helgoland Roads, North Sea.

[This corrects the article DOI: 10.1093/plankt/fbaa017.].

Rapid succession drives spring community dynamics of small protists at Helgoland Roads, North Sea.

The dynamics of diatoms and dinoflagellates have been monitored for many decades at the Helgoland Roads Long-Term Ecological Research site and are relatively well understood. In contrast, small-sized eukaryotic microbes and their community changes are still much more elusive, mainly due to their small size and uniform morphology, which makes them difficult to identify microscopically. By using next-generation sequencing, we wanted to shed light on the Helgoland planktonic community dynamics, including nano- and picoplankton, during a spring bloom. We took samples from March to May 2016 and sequenced the V4 region of the 18S rDNA. Our results showed that mixotrophic and heterotrophic taxa were more abundant than autotrophic diatoms. Dinoflagellates dominated the sequence assemblage, and several small-sized eukaryotic microbes like Haptophyta, Choanoflagellata, Marine Stramenopiles and Syndiniales were identified. A diverse background community including taxa from all size classes was present during the whole sampling period. Five phases with several communities were distinguished. The fastest changes in community composition took place in phase 3, while the communities from phases 1 to 5 were more similar to each other despite contrasting environmental conditions. Synergy effects of next-generation sequencing and traditional methods may be exploited in future long-term observations.

Harmful phytoplankton in the Beagle Channel (South America) as a potential threat to aquaculture activities.

The Beagle Channel is a remote subantarctic environment where mussel aquaculture initiatives have existed since the early 1990s. Here we analyze phytoplankton biomass and composition, and the occurrence of harmful microalgae species and their toxins at three sites during the period 2015-2016. The occurrence of potentially harmful algae was observed throughout the study period, including toxigenic dinoflagellates such as Alexandrium catenella (Group I of the A. tamarense complex), A. ostenfeldii, Dinophysis acuminata, Gonyaulax spinifera, Azadinium sp., and the diatoms Pseudo-nitzschia australis and P. fraudulenta. Toxic dinoflagellates were detected in low densities whereas a Pseudo-nitzschia bloom was observed in late February. Isolates of A. catenella and P. delicatissima sensu stricto were phylogenetically characterized. The toxin profile of A. catenella was dominated by GTX4, while P. delicatissima sensu stricto showed no production of the neurotoxin domoic acid in culture conditions. The results provide base-line information for the management of harmful algal blooms in this little explored subantarctic area.