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.

A genome catalogue of lake bacterial diversity and its drivers at continental scale.

Lakes are heterogeneous ecosystems inhabited by a rich microbiome whose genomic diversity is poorly defined. We present a continental-scale study of metagenomes representing 6.5 million km2 of the most lake-rich landscape on Earth. Analysis of 308 Canadian lakes resulted in a metagenome-assembled genome (MAG) catalogue of 1,008 mostly novel bacterial genomospecies. Lake trophic state was a leading driver of taxonomic and functional diversity among MAG assemblages, reflecting the responses of communities profiled by 16S rRNA amplicons and gene-centric metagenomics. Coupling the MAG catalogue with watershed geomatics revealed terrestrial influences of soils and land use on assemblages. Agriculture and human population density were drivers of turnover, indicating detectable anthropogenic imprints on lake bacteria at the continental scale. The sensitivity of bacterial assemblages to human impact reinforces lakes as sentinels of environmental change. Overall, the LakePulse MAG catalogue greatly expands the freshwater genomic landscape, advancing an integrative view of diversity across Earth's microbiomes.

Geospatial analysis reveals a hotspot of fecal bacteria in Canadian prairie lakes linked to agricultural non-point sources.

Lakes are sentinels of environmental changes within their watersheds including those induced by a changing climate and anthropogenic activities. In particular, contamination originating from point or non-point sources (NPS) within watersheds might be reflected in changes in the bacterial composition of lake water. We assessed the abundance of potentially pathogenic bacteria (PPB) sampled in 413 lakes within 8 southern Canadian ecozones that represent a wide diversity of lakes and watershed land use. The study objectives were (1) to explore the diversity of PPB; (2) to build a fecal multi-indicator from a cluster of co-occurring PPB; and (3) to predict the fecal multi-indicator over thousands of lakes. We identified bacterial taxa based on 16S rRNA amplicon sequencing and clustered 33 PPB matching taxa in the Canadian ePATHogen database using a Sørensen dissimilarity index on binary data across the sampled lakes. One cluster contained Erysipelothrix, Desulfovibrio, Bacteroides, Vibrio and Acholeplasma and was related to the NPS fraction of agriculture and pasture within the watershed as its main driver and thus it was determined as the fecal multi-indicator. We subsequently developed a fecal multi-indicator predictive model across 200 212 southern Canadian lakes which explained 55.1% of the deviance. Mapping the predictions showed higher fecal multi-indicator abundances in the Prairies and Boreal Plains compared to the other ecozones. These results represent the first attempt to map a potential fecal multi-indicator at the continental scale, which may be further improved in the future. Lastly, the study demonstrates the capacity of a multi-disciplinary approach leveraging both datasets derived from remote sensing and DNA sequencing to provide mapping information for public health governmental policies.

Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes.

BACKGROUND: The Arctic Ocean receives massive freshwater input and a correspondingly large amount of humic-rich organic matter of terrestrial origin. Global warming, permafrost melt, and a changing hydrological cycle will contribute to an intensification of terrestrial organic matter release to the Arctic Ocean. Although considered recalcitrant to degradation due to complex aromatic structures, humic substances can serve as substrate for microbial growth in terrestrial environments. However, the capacity of marine microbiomes to process aromatic-rich humic substances, and how this processing may contribute to carbon and nutrient cycling in a changing Arctic Ocean, is relatively unexplored. Here, we used a combination of metagenomics and metatranscriptomics to assess the prevalence and diversity of metabolic pathways and bacterial taxa involved in aromatic compound degradation in the salinity-stratified summer waters of the Canada Basin in the western Arctic Ocean. RESULTS: Community-scale meta-omics profiling revealed that 22 complete pathways for processing aromatic compounds were present and expressed in the Canada Basin, including those for aromatic ring fission and upstream funneling pathways to access diverse aromatic compounds of terrestrial origin. A phylogenetically diverse set of functional marker genes and transcripts were associated with fluorescent dissolved organic matter, a component of which is of terrestrial origin. Pathways were common throughout global ocean microbiomes but were more abundant in the Canada Basin. Genome-resolved analyses identified 12 clades of Alphaproteobacteria, including Rhodospirillales, as central contributors to aromatic compound processing. These genomes were mostly restricted in their biogeographical distribution to the Arctic Ocean and were enriched in aromatic compound processing genes compared to their closest relatives from other oceans. CONCLUSION: Overall, the detection of a phylogenetically diverse set of genes and transcripts implicated in aromatic compound processing supports the view that Arctic Ocean microbiomes have the capacity to metabolize humic substances of terrestrial origin. In addition, the demonstration that bacterial genomes replete with aromatic compound degradation genes exhibit a limited distribution outside of the Arctic Ocean suggests that processing humic substances is an adaptive trait of the Arctic Ocean microbiome. Future increases in terrestrial organic matter input to the Arctic Ocean may increase the prominence of aromatic compound processing bacteria and their contribution to Arctic carbon and nutrient cycles. Video Abstract.

Protist Diversity and Metabolic Strategy in Freshwater Lakes Are Shaped by Trophic State and Watershed Land Use on a Continental Scale.

Protists play key roles in aquatic food webs as primary producers, predators, nutrient recyclers, and symbionts. However, a comprehensive view of protist diversity in freshwaters has been challenged by the immense environmental heterogeneity among lakes worldwide. We assessed protist diversity in the surface waters of 366 freshwater lakes across a north temperate to subarctic range covering nearly 8.4 million km2 of Canada. Sampled lakes represented broad gradients in size, trophic state, and watershed land use. Hypereutrophic lakes contained the least diverse and most distinct protist communities relative to nutrient-poor lakes. Greater taxonomic variation among eutrophic lakes was mainly a product of heterotroph and mixotroph diversity, whereas phototroph assemblages were more similar under high-nutrient conditions. Overall, local physicochemical factors, particularly ion and nutrient concentrations, elicited the strongest responses in community structure, far outweighing the effects of geographic gradients. Despite their contrasting distribution patterns, obligate phototroph and heterotroph turnover was predicted by an overlapping set of environmental factors, while the metabolic plasticity of mixotrophs may have made them less predictable. Notably, protist diversity was associated with variation in watershed soil pH and agricultural crop coverage, pointing to human impact on the land-water interface that has not been previously identified in studies on smaller scales. Our study exposes the importance of both within-lake and external watershed characteristics in explaining protist diversity and biogeography, critical information for further developing an understanding of how freshwater lakes and their watersheds are impacted by anthropogenic stressors. IMPORTANCE Freshwater lakes are experiencing rapid changes under accelerated anthropogenic stress and a warming climate. Microorganisms underpin aquatic food webs, yet little is known about how freshwater microbial communities are responding to human impact. Here, we assessed the diversity of protists and their myriad ecological roles in lakes varying in size across watersheds experiencing a range of land use pressures by leveraging data from a continental-scale survey of Canadian lakes. We found evidence of human impact on protist assemblages through an association with lake trophic state and extending to agricultural activity and soil characteristics in the surrounding watershed. Furthermore, trophic state appeared to explain the distributions of phototrophic and heterotrophic protists in contrasting ways. Our findings highlight the vulnerability of lake ecosystems to increased land use and the importance of assessing terrestrial interfaces to elucidate freshwater ecosystem dynamics.

Comparing microscopy and DNA metabarcoding techniques for identifying cyanobacteria assemblages across hundreds of lakes.

Accurately identifying the species present in an ecosystem is vital to lake managers and successful bioassessment programs. This is particularly important when monitoring cyanobacteria, as numerous taxa produce toxins and can have major negative impacts on aquatic ecosystems. Increasingly, DNA-based techniques such as metabarcoding are being used for measuring aquatic biodiversity, as they could accelerate processing time, decrease costs and reduce some of the biases associated with traditional light microscopy. Despite the continuing use of traditional microscopy and the growing use of DNA metabarcoding to identify cyanobacteria assemblages, methodological comparisons between the two approaches have rarely been reported from a wide suite of lake types. Here, we compare planktonic cyanobacteria assemblages generated by inverted light microscopy and DNA metabarcoding from a 379-lake dataset spanning a longitudinal and trophic gradient. We found moderate levels of congruence between methods at the broadest taxonomic levels (i.e., Order, RV=0.40, p < 0.0001). This comparison revealed distinct cyanobacteria communities from lakes of different trophic states, with Microcystis, Aphanizomenon and Dolichospermum dominating with both methods in eutrophic and hypereutrophic sites. This finding supports the use of either method when monitoring eutrophication in lake surface waters. The biggest difference between the two methods was the detection of picocyanobacteria, which are typically underestimated by light microscopy. This reveals that the communities generated by each method currently are complementary as opposed to identical and promotes a combined-method strategy when monitoring a range of trophic systems. For example, microscopy can provide measures of cyanobacteria biomass, which are critical data in managing lakes. Going forward, we believe that molecular genetic methods will be increasingly adopted as reference databases are routinely updated with more representative sequences and will improve as cyanobacteria taxonomy is resolved with the increase in available genetic information.