A multiyear time series (2004-2012) of bacterial and archaeal community dynamics in a changing Arctic Ocean.

Climate change is profoundly impacting the Arctic, leading to a loss of multiyear sea ice and a warmer, fresher upper Arctic Ocean. The response of microbial communities to these climate-mediated changes is largely unknown. Here, we document the interannual variation in bacterial and archaeal communities across a 9-year time series of the Canada Basin that includes two historic sea ice minima (2007 and 2012). We report an overall loss of bacterial and archaeal community richness and significant shifts in community composition. The magnitude and period of most rapid change differed between the stratified water layers. The most pronounced changes in the upper water layers (surface mixed layer and upper Arctic water) occurred earlier in the time series, while changes in the lower layer (Pacific-origin water) occurred later. Shifts in taxonomic composition across time were subtle, but a decrease in Bacteroidota taxa and increase in Thaumarchaeota and Euryarchaeota taxa were the clearest signatures of change. This time series provides a rare glimpse into the potential influence of climate change on Arctic microbial communities; extension to the present day should contribute to deeper insights into the trajectory of Arctic marine ecosystems in response to warming and freshening.

Drivers of Regional Bacterial Community Structure and Diversity in the Northwest Atlantic Ocean.

The fundamental role of bacteria in global biogeochemical cycles warrants a thorough understanding of the factors controlling bacterial community structure. In this study, the integrated effect of seasonal differences and spatial distribution on bacterial community structure and diversity were investigated at the regional scale. We conducted a comprehensive bacterial survey, with 451 samples of the Scotian Shelf sector of the Northwest Atlantic Ocean during spring and fall of 2014 and 2016, to analyze the effects of physicochemical gradients on bacterial community structure. Throughout the region, Pelagibacteraceae and Rhodobacteraceae were the most common in the free-living fraction, while Flavobacteriia and Deltaproteobacteria were more abundant in the particle-associated fraction. Overall, there was strong covariation of the microbial community diversity from the two size fractions. This relationship existed despite the statistically significant difference in community structure between the free-living and particle-associated size fractions. In both size fractions, distribution patterns of bacterial taxa, and species within taxa, displayed temporal and spatial preferences. Distinct bacterial assemblages specific to season and depth in the water column were identified. These distinct assemblages, consistent for both 2014 and 2016, suggested replicable patterns in microbial communities for spring and fall in this region. Over all sites, temperature and oxygen values were highly correlated with community similarity, and salinity and oxygen values were the most strongly positively- and negatively correlated with alpha diversity, respectively. However, the strengths of these correlations depended on the depth and season sampled. The bathymetry of the Scotian Shelf, the abrupt shelf break to the Scotian Slope and the major ocean currents dominating in the region led to the formation of distinct on-shelf and off-shelf bacterial communities both in spring and fall. The highest species richness was observed at the shelf break, where water masses from the two major currents meet. Our study establishes the baseline for assessing future changes in the bacterial community of the Scotian Shelf waters, a rapidly changing sector of the Atlantic Ocean.

Seasonal assemblages and short-lived blooms in coastal north-west Atlantic Ocean bacterioplankton.

Temperate oceans are inhabited by diverse and temporally dynamic bacterioplankton communities. However, the role of the environment, resources and phytoplankton dynamics in shaping marine bacterioplankton communities at different time scales remains poorly constrained. Here, we combined time series observations (time scales of weeks to years) with molecular analysis of formalin-fixed samples from a coastal inlet of the north-west Atlantic Ocean to show that a combination of temperature, nitrate, small phytoplankton and Synechococcus abundances are best predictors for annual bacterioplankton community variability, explaining 38% of the variation. Using Bayesian mixed modelling, we identified assemblages of co-occurring bacteria associated with different seasonal periods, including the spring bloom (e.g. Polaribacter, Ulvibacter, Alteromonadales and ARCTIC96B-16) and the autumn bloom (e.g. OM42, OM25, OM38 and Arctic96A-1 clades of Alphaproteobacteria, and SAR86, OM60 and SAR92 clades of Gammaproteobacteria). Community variability over spring bloom development was best explained by silicate (32%)--an indication of rapid succession of bacterial taxa in response to diatom biomass--while nanophytoplankton as well as picophytoplankton abundance explained community variability (16-27%) over the transition into and out of the autumn bloom. Moreover, the seasonal structure was punctuated with short-lived blooms of rare bacteria including the KSA-1 clade of Sphingobacteria related to aromatic hydrocarbon-degrading bacteria.

Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton.

In this study, we used comparative metaproteomics to investigate the metabolic activity of microbial plankton inhabiting a seasonally hypoxic basin in the Northwest Atlantic Ocean (Bedford Basin). From winter to spring, we observed a seasonal increase in high-affinity membrane transport proteins involved in scavenging of organic substrates; Rhodobacterales transporters were strongly associated with the spring phytoplankton bloom, whereas SAR11 transporters were abundant in the underlying waters. A diverse array of transporters for organic compounds were similar to the SAR324 clade, revealing an active heterotrophic lifestyle in coastal waters. Proteins involved in methanol oxidation (from the OM43 clade) and carbon monoxide (from a wide variety of bacteria) were identified throughout Bedford Basin. Metabolic niche partitioning between the SUP05 and ARCTIC96BD-19 clades, which together comprise the Gamma-proteobacterial sulfur oxidizers group was apparent. ARCTIC96BD-19 proteins involved in the transport of organic compounds indicated that in productive coastal waters this lineage tends toward a heterotrophic metabolism. In contrast, the identification of sulfur oxidation proteins from SUP05 indicated the use of reduced sulfur as an energy source in hypoxic bottom water. We identified an abundance of Marine Group I Thaumarchaeota proteins in the hypoxic deep layer, including proteins for nitrification and carbon fixation. No transporters for organic compounds were detected among the thaumarchaeal proteins, suggesting a reliance on autotrophic carbon assimilation. In summary, our analyses revealed the spatiotemporal structure of numerous metabolic activities in the coastal ocean that are central to carbon, nitrogen and sulfur cycling in the sea.

Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus.

The Cyanobacteria Prochlorococcus and Synechococcus account for a substantial fraction of marine primary production. Here, we present quantitative niche models for these lineages that assess present and future global abundances and distributions. These niche models are the result of neural network, nonparametric, and parametric analyses, and they rely on >35,000 discrete observations from all major ocean regions. The models assess cell abundance based on temperature and photosynthetically active radiation, but the individual responses to these environmental variables differ for each lineage. The models estimate global biogeographic patterns and seasonal variability of cell abundance, with maxima in the warm oligotrophic gyres of the Indian and the western Pacific Oceans and minima at higher latitudes. The annual mean global abundances of Prochlorococcus and Synechococcus are 2.9 ± 0.1 × 10(27) and 7.0 ± 0.3 × 10(26) cells, respectively. Using projections of sea surface temperature as a result of increased concentration of greenhouse gases at the end of the 21st century, our niche models projected increases in cell numbers of 29% and 14% for Prochlorococcus and Synechococcus, respectively. The changes are geographically uneven but include an increase in area. Thus, our global niche models suggest that oceanic microbial communities will experience complex changes as a result of projected future climate conditions. Because of the high abundances and contributions to primary production of Prochlorococcus and Synechococcus, these changes may have large impacts on ocean ecosystems and biogeochemical cycles.

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.

Planktonic microbes in the Gulf of Maine area.

In the Gulf of Maine area (GoMA), as elsewhere in the ocean, the organisms of greatest numerical abundance are microbes. Viruses in GoMA are largely cyanophages and bacteriophages, including podoviruses which lack tails. There is also evidence of Mimivirus and Chlorovirus in the metagenome. Bacteria in GoMA comprise the dominant SAR11 phylotype cluster, and other abundant phylotypes such as SAR86-like cluster, SAR116-like cluster, Roseobacter, Rhodospirillaceae, Acidomicrobidae, Flavobacteriales, Cytophaga, and unclassified Alphaproteobacteria and Gammaproteobacteria clusters. Bacterial epibionts of the dinoflagellate Alexandrium fundyense include Rhodobacteraceae, Flavobacteriaceae, Cytophaga spp., Sulfitobacter spp., Sphingomonas spp., and unclassified Bacteroidetes. Phototrophic prokaryotes in GoMA include cyanobacteria that contain chlorophyll (mainly Synechococcus), aerobic anoxygenic phototrophs that contain bacteriochlorophyll, and bacteria that contain proteorhodopsin. Eukaryotic microalgae in GoMA include Bacillariophyceae, Dinophyceae, Prymnesiophyceae, Prasinophyceae, Trebouxiophyceae, Cryptophyceae, Dictyochophyceae, Chrysophyceae, Eustigmatophyceae, Pelagophyceae, Synurophyceae, and Xanthophyceae. There are no records of Bolidophyceae, Aurearenophyceae, Raphidophyceae, and Synchromophyceae in GoMA. In total, there are records for 665 names and 229 genera of microalgae. Heterotrophic eukaryotic protists in GoMA include Dinophyceae, Alveolata, Apicomplexa, amoeboid organisms, Labrynthulida, and heterotrophic marine stramenopiles (MAST). Ciliates include Strombidium, Lohmaniella, Tontonia, Strobilidium, Strombidinopsis and the mixotrophs Laboea strobila and Myrionecta rubrum (ex Mesodinium rubra). An inventory of selected microbial groups in each of 14 physiographic regions in GoMA is made by combining information on the depth-dependent variation of cell density and the depth-dependent variation of water volume. Across the entire GoMA, an estimate for the minimum abundance of cell-based microbes is 1.7×10(25) organisms. By one account, this number of microbes implies a richness of 10(5) to 10(6) taxa in the entire water volume of GoMA. Morphological diversity in microplankton is well-described but the true extent of taxonomic diversity, especially in the femtoplankton, picoplankton and nanoplankton--whether autotrophic, heterotrophic, or mixotrophic, is unknown.

Water-column stratification governs the community structure of subtropical marine picophytoplankton.

The increase in the areal extent of the subtropical gyres over the past decade has been attributed to a global tendency towards increased water-column stratification. Here, we examine how vertical stratification governs the community structure of the picophytoplankton that dominate these vast marine ecosystems. We analysed phytoplankton community composition in the three Southern Subtropical basins of the Pacific, Indian and Atlantic Oceans using a variety of methods and show that the distributions of picocyanobacteria and photosynthetic picoeukaryotes (PPEs) are strongly correlated with depth and strength of vertical mixing: the changes in community structure occur at various taxonomic levels. In well-mixed waters, PPEs, in particular haptophytes, dominate, whereas in strongly stratified waters, picocyanobacteria of the genus Prochlorococcus are prevalent, regardless of whether the relative contributions to total biomass are assessed in terms of pigment or of carbon. This ecological diochotomy within the picophytoplankton supports the hypothesis that genomic streamlining provides a selective advantage for Prochlorococcus in highly stable, oligotrophic systems, but may restrict their ability to dominate in regions subject to dynamic mixing.

Smallest algae thrive as the Arctic Ocean freshens.

As climate changes and the upper Arctic Ocean receives more heat and fresh water, it becomes more difficult for mixing processes to deliver nutrients from depth to the surface for phytoplankton growth. Competitive advantage will presumably accrue to small cells because they are more effective in acquiring nutrients and less susceptible to gravitational settling than large cells. Since 2004, we have discerned an increase in the smallest algae and bacteria along with a concomitant decrease in somewhat larger algae. If this trend toward a community of smaller cells is sustained, it may lead to reduced biological production at higher trophic levels.

Coherent assembly of phytoplankton communities in diverse temperate ocean ecosystems.

The annual cycle of phytoplankton cell abundance is coherent across diverse ecosystems in the temperate North Atlantic Ocean. In Bedford Basin, on the Scotian Shelf and in the Labrador Sea, the numerical abundance of phytoplankton is low in spring and high in autumn, thus in phase with the temperature cycle. Temperature aligns abundance on a common basis, effectively adjusting apparent cell discrepancies in waters that are colder or warmer than the regional norm. As an example of holistic simplicity arising from underlying complexity, the variance in a community variable (total abundance) is explained by a single predictor (temperature) to the extent of 75% in the marginal seas. In the estuarine basin, weekly averages of phytoplankton and temperature computed from a 13 year time-series yield a predictive relationship with 91% explained variance. Temperature-directed assembly of individual phytoplankton cells to form communities is statistically robust, consistent with observed biomass changes, amenable to theoretical analysis, and a sentinel for long-term change. Since cell abundance is a community property in the same units for all marine microbes at any trophic level and at any phylogenetic position, it promises to integrate biological oceanography into general ecology and evolution.

Oceanographic basis of the global surface distribution of Prochlorococcus ecotypes.

By using data collected during a continuous circumnavigation of the Southern Hemisphere, we observed clear patterns in the population-genetic structure of Prochlorococcus, the most abundant photosynthetic organism on Earth, between and within the three Southern Subtropical Gyres. The same mechanisms that were previously invoked to account for the vertical distribution of ecotypes at local scales accounted for the global (horizontal) patterns we observed. Basin-scale and seasonal variations in the structure and strength of vertical stratification provide a basis for understanding large-scale horizontal distribution in genetic and physiological traits of Prochlorococcus, and perhaps of marine microbial communities in general.

Coherent sign switching in multiyear trends of microbial plankton.

Since the 1990s, phytoplankton biomass on the continental shelf of Nova Scotia and in the Labrador Sea has undergone sustained changes in the spring and fall, which are accompanied by changes in bacterioplankton that are dampened in amplitude but coherent in the direction of change. A reversal of trend in biomass change, so-called sign switching, occurs both in time and in space. Thus, whenever (spring or fall) and wherever (Scotian Shelf or Labrador Sea) phytoplankton increase or decrease, so also does bacterioplankton. This tandem sign switch indicates coupling of the trophic levels at a multiyear time scale and contributes to an ecological fingerprint of systemwide forcing.