Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus.

Diatoms, the main eukaryotic phytoplankton of the polar marine regions, are essential for the maintenance of food chains specific to Arctic and Antarctic ecosystems, and are experiencing major disturbances under current climate change. As such, it is fundamental to understand the physiological mechanisms and associated molecular basis of their endurance during the long polar night. Here, using the polar diatom Fragilariopsis cylindrus, we report an integrative analysis combining transcriptomic, microscopic and biochemical approaches to shed light on the strategies used to survive the polar night. We reveal that in prolonged darkness, diatom cells enter a state of quiescence with reduced metabolic and transcriptional activity, during which no cell division occurs. We propose that minimal energy is provided by respiration and degradation of protein, carbohydrate and lipid stores and that homeostasis is maintained by autophagy in prolonged darkness. We also report internal structural changes that manifest the morphological acclimation of cells to darkness, including the appearance of a large vacuole. Our results further show that immediately following a return to light, diatom cells are able to use photoprotective mechanisms and rapidly resume photosynthesis, demonstrating the remarkable robustness of polar diatoms to prolonged darkness at low temperature.

Contrasting sea ice conditions shape microbial food webs in Hudson Bay (Canadian Arctic).

The transition from ice-covered to open water is a recurring feature of the Arctic and sub-Arctic, but microbial diversity and cascading effects on the microbial food webs is poorly known. Here, we investigated microbial eukaryote, bacterial and archaeal communities in Hudson Bay (sub-Arctic, Canada) under sea-ice cover and open waters conditions. Co-occurrence networks revealed a <3 µm pico‒phytoplankton-based food web under the ice and a >3 µm nano‒microphytoplankton-based food web in the open waters. The ice-edge communities were characteristic of post-bloom conditions with high proportions of the picophytoplankton Micromonas and Bathycoccus. Nano‒ to micro‒phytoplankton and ice associated diatoms were detected throughout the water column, with the sympagic Melosira arctica exclusive to ice-covered central Hudson Bay and Thalassiosira in open northwestern Hudson Bay. Heterotrophic microbial eukaryotes and prokaryotes also differed by ice-state, suggesting a linkage between microbes at depth and surface phytoplankton bloom state. The findings suggest that a longer open water season may favor the establishment of a large phytoplankton-based food web at the subsurface chlorophyll maxima (SCM), increasing carbon export from pelagic diatoms to deeper waters and affect higher trophic levels in the deep Hudson Bay.

Genomic data support management of anadromous Arctic Char fisheries in Nunavik by highlighting neutral and putatively adaptive genetic variation.

Distinguishing neutral and adaptive genetic variation is one of the main challenges in investigating processes shaping population structure in the wild, and landscape genomics can help identify signatures of adaptation to contrasting environments. Arctic Char (Salvelinus alpinus) is an anadromous salmonid and the most harvested fish species by Inuit people, including in Nunavik (Québec, Canada), one of the most recently deglaciated regions in the world. Unlike many other anadromous salmonids, Arctic Char occupy coastal habitats near their natal rivers during their short marine phase restricted to the summer ice-free period. Our main objective was to document putatively neutral and adaptive genomic variation in anadromous Arctic Char populations from Nunavik and bordering regions to inform local fisheries management. We used genotyping by sequencing (GBS) to genotype 18,112 filtered single nucleotide polymorphisms (SNP) in 650 individuals from 23 sampling locations along >2000 km of coastline. Our results reveal a hierarchical genetic structure, whereby neighboring hydrographic systems harbor distinct populations grouped by major oceanographic basins: Hudson Bay, Hudson Strait, Ungava Bay, and Labrador Sea. We found genetic diversity and differentiation to be consistent both with the expected postglacial recolonization history and with patterns of isolation-by-distance reflecting contemporary gene flow. Results from three gene-environment association methods supported the hypothesis of local adaptation to both freshwater and marine environments (strongest associations with sea surface and air temperatures during summer and salinity). Our results support a fisheries management strategy at a regional scale, and other implications for hatchery projects and adaptation to climate change are discussed.

Marine DNA Viral Macro- and Microdiversity from Pole to Pole.

Microbes drive most ecosystems and are modulated by viruses that impact their lifespan, gene flow, and metabolic outputs. However, ecosystem-level impacts of viral community diversity remain difficult to assess due to classification issues and few reference genomes. Here, we establish an ∼12-fold expanded global ocean DNA virome dataset of 195,728 viral populations, now including the Arctic Ocean, and validate that these populations form discrete genotypic clusters. Meta-community analyses revealed five ecological zones throughout the global ocean, including two distinct Arctic regions. Across the zones, local and global patterns and drivers in viral community diversity were established for both macrodiversity (inter-population diversity) and microdiversity (intra-population genetic variation). These patterns sometimes, but not always, paralleled those from macro-organisms and revealed temperate and tropical surface waters and the Arctic as biodiversity hotspots and mechanistic hypotheses to explain them. Such further understanding of ocean viruses is critical for broader inclusion in ecosystem models.

Need for focus on microbial species following ice melt and changing freshwater regimes in a Janus Arctic Gateway.

Oceanic gateways are sensitive to climate driven processes. By connecting oceans, they have a global influence on marine biological production and biogeochemical cycles. The furthest north of these gateways is Nares Strait at the top of the North Water between Greenland and Ellesmere Island (Canada). This gateway is globally beneficial, first by supporting high local mammal and bird populations and second with the outflow of phosphate-rich Arctic waters fueling the North Atlantic spring bloom. Both sides of the North Water are hydrologically distinct with counter currents that make this Arctic portal a Janus gateway, after Janus, the Roman god of duality. We examined oceanographic properties and differences in phytoplankton and other protist communities from the eastern and western sides of the North Water (latitude 76.5°N) and found that species differed markedly due to salinity stratification regimes and local hydrography. Typical Arctic communities were associated with south flowing currents along the Canadian side, while potentially noxious Pseudo-nitzschia spp. were dominant on the Greenland side and associated with greater surface freshening from ice melt. This susceptibility of the Greenland side to Pseudo-nitzschia spp. blooms suggest that monitoring species responses to climate mediated changes is needed.

Archaeal amoA and ureC genes and their transcriptional activity in the Arctic Ocean.

Thaumarchaeota and the gene encoding for a subunit of ammonia monooxygenase (amoA) are ubiquitous in Polar Seas, and some Thaumarchaeota also have a gene coding for ureC, diagnostic for urease. Using quantitative PCR we investigated the occurrence of genes and transcripts of ureC and amoA in Arctic samples from winter, spring and summer. AmoA genes, ureC genes and amoA transcripts were always present, but ureC transcripts were rarely detected. Over a 48 h light manipulation experiment amoA transcripts persisted under light and dark conditions, but not ureC transcripts. In addition, maxima for amoA transcript were nearer the surface compared to amoA genes. Clone libraries using DNA template recovered shallow and deep amoA clades but only the shallow clade was recovered from cDNA (from RNA). These results imply environmental control of amoA expression with direct or indirect light effects, and rare ureC expression despite its widespread occurrence in the Arctic Ocean.

Role for urea in nitrification by polar marine Archaea.

Despite the high abundance of Archaea in the global ocean, their metabolism and biogeochemical roles remain largely unresolved. We investigated the population dynamics and metabolic activity of Thaumarchaeota in polar environments, where these microorganisms are particularly abundant and exhibit seasonal growth. Thaumarchaeota were more abundant in deep Arctic and Antarctic waters and grew throughout the winter at surface and deeper Arctic halocline waters. However, in situ single-cell activity measurements revealed a low activity of this group in the uptake of both leucine and bicarbonate (<5% Thaumarchaeota cells active), which is inconsistent with known heterotrophic and autotrophic thaumarchaeal lifestyles. These results suggested the existence of alternative sources of carbon and energy. Our analysis of an environmental metagenome from the Arctic winter revealed that Thaumarchaeota had pathways for ammonia oxidation and, unexpectedly, an abundance of genes involved in urea transport and degradation. Quantitative PCR analysis confirmed that most polar Thaumarchaeota had the potential to oxidize ammonia, and a large fraction of them had urease genes, enabling the use of urea to fuel nitrification. Thaumarchaeota from Arctic deep waters had a higher abundance of urease genes than those near the surface suggesting genetic differences between closely related archaeal populations. In situ measurements of urea uptake and concentration in Arctic waters showed that small-sized prokaryotes incorporated the carbon from urea, and the availability of urea was often higher than that of ammonium. Therefore, the degradation of urea may be a relevant pathway for Thaumarchaeota and other microorganisms exposed to the low-energy conditions of dark polar waters.

Arctic Ocean microbial community structure before and after the 2007 record sea ice minimum.

Increasing global temperatures are having a profound impact in the Arctic, including the dramatic loss of multiyear sea ice in 2007 that has continued to the present. The majority of life in the Arctic is microbial and the consequences of climate-mediated changes on microbial marine food webs, which are responsible for biogeochemical cycling and support higher trophic levels, are unknown. We examined microbial communities over time by using high-throughput sequencing of microbial DNA collected between 2003 and 2010 from the subsurface chlorophyll maximum (SCM) layer of the Beaufort Sea (Canadian Arctic). We found that overall this layer has freshened and concentrations of nitrate, the limiting nutrient for photosynthetic production in Arctic seas, have decreased. We compared microbial communities from before and after the record September 2007 sea ice minimum and detected significant differences in communities from all three domains of life. In particular, there were significant changes in species composition of Eukarya, with ciliates becoming more common and heterotrophic marine stramenopiles (MASTs) accounting for a smaller proportion of sequences retrieved after 2007. Within the Archaea, Marine Group I Thaumarchaeota, which earlier represented up to 60% of the Archaea sequences in this layer, have declined to <10%. Bacterial communities overall were less diverse after 2007, with a significant decrease of the Bacteroidetes. These significant shifts suggest that the microbial food webs are sensitive to physical oceanographic changes such as those occurring in the Canadian Arctic over the past decade.