A decadal perspective on north water microbial eukaryotes as Arctic Ocean sentinels

The North Water region, between Greenland and Ellesmere Island, with high populations of marine birds and mammals, is an Arctic icon. Due to climate related changes, seasonal patterns in water column primary production are changing but the implications for the planktonic microbial eukaryote communities that support the ecosystem are unknown. Here we report microbial community phenology in samples collected over 12 years (2005–2018) from July to October and analysed using high throughput 18S rRNA V4 amplicon sequencing. Community composition was tied to seasonality with summer communities more variable than distinct October communities. In summer, sentinel pan- Arctic species, including a diatom in the Chaetoceros socialis-gelidus complex and the picochlorophyte Micromonas polaris dominated phytoplankton and were summer specialists. In autumn, uncultured undescribed open water dinoflagellates were favored, and their ubiquity suggests they are sentinels of arctic autumn conditions. Despite the input of nutrients into surface waters, autumn chlorophyll concentrations remained low, refuting projected scenarios that longer ice-free seasons are synonymous with high autumn production and a diatom dominated bloom. Overall, the summer sentinel microbial taxa are persisting, and a subset oceanic dinoflagellate should be monitored for possible ecosystem shifts as later autumn ice formation becomes prevalent elsewhere

Genomic evidence of functional diversity in DPANN archaea, from oxic species to anoxic vampiristic consortia

DPANN archaea account for half of the archaeal diversity of the biosphere, but with few cultivated representatives, their metabolic potential and environmental functions are poorly understood. The extreme geochemical and environmental conditions in meromictic ice-capped Lake A, in the Canadian High Arctic, provided an isolated, stratified model ecosystem to resolve the distribution and metabolism of uncultured aquatic DPANN archaea living across extreme redox and salinity gradients, from freshwater oxygenated conditions, to saline, anoxic, sulfidic waters. We recovered 28 metagenome-assembled genomes (MAGs) of DPANN archaea that provided genetic insights into their ecological function. Thiosulfate oxidation potential was detected in aerobic Woesearchaeota, whereas diverse metabolic functions were identified in anaerobic DPANN archaea, including degradation and fermentation of cellular compounds, and sulfide and polysulfide reduction. We also found evidence for “vampiristic” metabolism in several MAGs, with genes coding for pore-forming toxins, peptidoglycan degradation, and RNA scavenging. The vampiristic MAGs co-occurred with other DPANNs having complementary metabolic capacities, leading to the possibility that DPANN form interspecific consortia that recycle microbial carbon, nutrients and complex molecules through a DPANN archaeal shunt, adding hidden novel complexity to anaerobic microbial food webs

Size-fractionated microbiome structure in subarctic rivers and a coastal plume across DOC and salinity gradients

Little is known about the microbial diversity of rivers that flow across the changing subarctic landscape. Using amplicon sequencing (rRNA and rRNA genes) combined with HPLC pigment analysis and physicochemical measurements, we investigated the diversity of two size fractions of planktonic Bacteria, Archaea and microbial eukaryotes along environmental gradients in the Great Whale River (GWR), Canada. This large subarctic river drains an extensive watershed that includes areas of thawing permafrost, and discharges into southeastern Hudson Bay as an extensive plume that gradually mixes with the coastal marine waters. The microbial communities differed by size-fraction (separated with a 3-μm filter), and clustered into three distinct environmental groups: (1) the GWR sites throughout a 150-km sampling transect; (2) the GWR plume in Hudson Bay; and (3) small rivers that flow through degraded permafrost landscapes. There was a downstream increase in taxonomic richness along the GWR, suggesting that sub-catchment inputs influence microbial community structure in the absence of sharp environmental gradients. Microbial community structure shifted across the salinity gradient within the plume, with changes in taxonomic composition and diversity. Rivers flowing through degraded permafrost had distinct physicochemical and microbiome characteristics, with allochthonous dissolved organic carbon explaining part of the variation in community structure. Finally, our analyses of the core microbiome indicated that while a substantial part of all communities consisted of generalists, most taxa had a more limited environmental range and may therefore be sensitive to ongoing change

Seasonal changes in planktonic bacterivory rates under the ice-covered coastal Arctic Ocean

Bacterivory was determined in surface waters of Franklin Bay, western Arctic, over a seasonal ice-covered period (winter-spring, 2003-2004). The objectives were to obtain information on the functioning of the microbial food web under the ice, during winter (from 21 December 2003 to 21 March 2004) and during spring (from 22 March 2004 to 29 May 2004), and to test whether bacterial losses would increase after the increase in bacterial production following the spring phytoplankton bloom. Chl a concentrations ranged from 0.04 to 0.36 mu g L(-1), increasing in March and reaching a peak in April. Bacterial biomass showed no consistent trend for the whole period, and protist biomass followed a pattern similar to that of Chl a. Bacterial production increased 1 week after Chl a concentrations started to increase, while bacterivory rates increased very slightly. Average bacterivory rates in winter (0.16 +/- 0.07 mu g C L(-1) d(-1)) were not significantly different from those in spring (0.29 +/- 0.24 mu g C L(-1) d(-1)). Average bacterial production, on the other hand, was similar to bacterivory rates in winter (0.19 +/- 0.38 mu g C L(-1) d(-1)), but higher than bacterivory in spring (0.93 +/- 0.28 mu g C L(-1) d(-1)). Therefore, bacterial production was controlled by grazers during winter and by substrate concentration in spring

Chlorovirus and myovirus diversity in permafrost thaw ponds

Permafrost thaw ponds occur in high abundance across the northern landscape of Canada and are sites of intense microbial activity, resulting in carbon dioxide and methane emissions to the atmosphere. In this study, we focused on viruses as largely unstudied agents of top-down control in these high-latitude microbial ecosystems. Specifically, we compared the diversity of myovirus, chlorovirus and host microbial communities in an organic soil palsa valley pond and a mineral soil lithalsa valley pond. These 2 subarctic permafrost landscapes are both common in northern Québec, Canada. Sequence analysis of ribosomal small subunit RNA genes showed that the community structure of bacteria and microbial eukaryotes differed significantly between the 2 ponds, which both differed from microbial communities in a rock-basin lake (whose formation was not related to permafrost thawing and which we used as a reference pond) in the same region. The viral assemblages included 439 OTUs in the uncultured Myoviridae category and 41 OTUs in the family Phycodnaviridae. Phylogenetic analysis of the latter based on an amino acid sequence alignment revealed a single large clade related to chloroviruses, consistent with the abundant presence of chlorophytes in these waters. As there was for the bacterial and eukaryotic communi-ties, there were also significant differences in the community structure of these viral groups among the 3 ponds. These results suggest that host community composition is influenced by environmental filtering, which in turn contributes to driving viral diversity across landscape types

Genomic evidence for sulfur intermediates as new biogeochemical hubs in a model aquatic microbial ecosystem

Background: The sulfur cycle encompasses a series of complex aerobic and anaerobic transformations of S-containing molecules and plays a fundamental role in cellular and ecosystem-level processes, influencing biological carbon transfers and other biogeochemical cycles. Despite their importance, the microbial communities and metabolic pathways involved in these transformations remain poorly understood, especially for inorganic sulfur compounds of intermediate oxidation states (thiosulfate, tetrathionate, sulfite, polysulfides). Isolated and highly stratified, the extreme geochemical and environmental features of meromictic ice-capped Lake A, in the Canadian High Arctic, provided an ideal model ecosystem to resolve the distribution and metabolism of aquatic sulfur cycling microorganisms along redox and salinity gradients. Results: Applying complementary molecular approaches, we identified sharply contrasting microbial communities and metabolic potentials among the markedly distinct water layers of Lake A, with similarities to diverse fresh, brackish and saline water microbiomes. Sulfur cycling genes were abundant at all depths and covaried with bacterial abundance. Genes for oxidative processes occurred in samples from the oxic freshwater layers, reductive reactions in the anoxic and sulfidic bottom waters and genes for both transformations at the chemocline. Up to 154 different genomic bins with potential for sulfur transformation were recovered, revealing a panoply of taxonomically diverse microorganisms with complex metabolic pathways for biogeochemical sulfur reactions. Genes for the utilization of sulfur cycle intermediates were widespread throughout the water column, co-occurring with sulfate reduction or sulfide oxidation pathways. The genomic bin composition suggested that in addition to chemical oxidation, these intermediate sulfur compounds were likely produced by the predominant sulfur chemo- and photo-oxidisers at the chemocline and by diverse microbial degraders of organic sulfur molecules. Conclusions: The Lake A microbial ecosystem provided an ideal opportunity to identify new features of the biogeochemical sulfur cycle. Our detailed metagenomic analyses across the broad physico-chemical gradients of this permanently stratified lake extend the known diversity of microorganisms involved in sulfur transformations over a wide range of environmental conditions. The results indicate that sulfur cycle intermediates and organic sulfur molecules are major sources of electron donors and acceptors for aquatic and sedimentary microbial communities in association with the classical sulfur cycl

Effects of light and prey availability on Arctic freshwater protist communities examined by high-throughput DNA and RNA sequencing

Abstract Protists in high-latitude lakes are constrained by cold temperatures, low inorganic nutrient supply and low light availability for much of the year due to ice cover and polar darkness. The lengthening ice-free periods in these freshwater ecosystems due to a warming climate results in increased light availability, but the overall impacts on phytoplankton and other protists are unknown. We experimentally investigated protist community responses to changes in light and prey availability in a dilution series in Ward Hunt Lake (latitude 83°05 0 N), in the Canadian High Arctic. The communities at the end of the experiment were characterized using high-throughput pyrosequencing of the V4 region of the 18S rRNA gene as a measure of taxonomic presence, and of 18S rRNA (from RNA converted to cDNA) as a taxon-specific indicator of community response. At the end of the experiment under low irradiance, cDNA reads were dominated by photosynthetic dinoflagellate genera, except at the greatest dilution where Cercozoa were most abundant. In contrast, the cDNA reads in the high light treatments were dominated by chrysophytes. Given the known trophic differences among dinoflagellates, cercozoans and chrysophytes, this apparent environmental selection implies that the rise in underwater irradiance associated with increasing ice-free conditions may affect microbial food web structure and function in polar lakes

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

Arctic microbial ecosystems and impacts of extreme warming during the International Polar Year

As a contribution to the International Polar Year program MERGE (Microbiological and Ecological Responses to Global Environmental change in polar regions), studies were conducted on the terrestrial and aquatic microbial ecosystems of northern Canada (details at: http://www.cen.ulaval.ca/merge/). The habitats included permafrost soils, saline coldwater springs, supraglacial lakes on ice shelves, epishelf lakes in fjords, deep meromictic lakes, and shallow lakes, ponds and streams. Microbiological samples from each habitat were analysed by HPLC pigment assays, light and fluorescence microscopy, and DNA sequencing. The results show a remarkably diverse microflora of viruses, Archaea (including ammonium oxidisers and methanotrophs), Bacteria (including filamentous sulfur-oxidisers in a saline spring and benthic mats of Cyanobacteria in many waterbodies), and protists (including microbial eukaryotes in snowbanks and ciliates in ice-dammed lakes). In summer 2008, we recorded extreme warming at Ward Hunt Island and vicinity, the northern limit of the Canadian high Arctic, with air temperatures up to 20.5 \ub0C. This was accompanied by pronounced changes in microbial habitats: deepening of the permafrost active layer; loss of perennial lake ice and sea ice; loss of ice-dammed freshwater lakes; and 23% loss of total ice shelf area, including complete break-up and loss of the Markham Ice Shelf cryo-ecosystem. These observations underscore the vulnerability of Arctic microbial ecosystems to ongoing climate change.Peer reviewed: YesNRC publication: Ye