Metal contaminations impact archaeal community composition, abundance and function in remote alpine lakes.

Using the 16S rRNA and mcrA genes, we investigated the composition, abundance and activity of sediment archaeal communities within 18 high-mountain lakes under contrasted metal levels from different origins (bedrock erosion, past-mining activities and atmospheric depositions). Bathyarchaeota, Euryarchaeota and Woesearchaeota were the major phyla found at the meta-community scale, representing 48%, 18.3% and 15.2% of the archaeal community respectively. Metals were equally important as physicochemical variables in explaining the assemblage of archaeal communities and their abundance. Methanogenesis appeared as a process of central importance in the carbon cycle within sediments of alpine lakes as indicated by the absolute abundance of methanogen 16S rRNA and mcrA gene transcripts (105 to 109 copies g-1 ). We showed that methanogen abundance and activity were significantly reduced with increasing concentrations of Pb and Cd, two indicators of airborne metal contaminations. Considering the ecological importance of methanogenesis in sediment habitats, these metal contaminations may have system wide implications even in remote area such as alpine lakes. Overall, this work was pioneer in integrating the effect of long-range atmospheric depositions on archaeal communities and indicated that metal contamination might significantly compromise the contribution of Archaea to the carbon cycling of the mountain lake sediments.

Ultrarare marine microbes contribute to key sulphur-related ecosystem functions.

The description of a rare biosphere within microbial communities has created great interest because microbes play a fundamental role in the functioning of all ecosystems on earth. Despite recent progress in understanding the ecology of the rare biosphere, the concept itself is still discussed, and fundamental questions remain. Here, we target the seed bank compartment of the rare biosphere, assess the level of rarity at which micro-organisms are still able to colonize an ecosystem and investigate whether rare species are functionally redundant. Using an original experimental design where wood in aquaria was inoculated with increasingly diluted coastal seawater, we show that bacteria that represented as few as 0.00000002% of the cells in the environment (or 1 cell in 10 L of seawater) were still able to grow and play key roles within the ecosystem. Our experiment further showed that some bacteria can be replaced by others that have the potential to fulfil the same metabolic tasks. This finding suggests some functional redundancy within bacterial species. However, when ultrarare bacteria were progressively removed, productivity was reduced, and below a certain threshold some processes were lost, and the function of the ecosystem was altered. Overall the study shows that bacteria that are not detected by high-throughput sequencing approaches are nevertheless viable and able to colonize new ecosystems, suggesting the need to consider ultrarare microbes in the marine environment.

Dense water plumes modulate richness and productivity of deep sea microbes.

Growing evidence indicates that dense water formation and flow over the continental shelf is a globally relevant oceanographic process, potentially affecting microbial assemblages down to the deep ocean. However, the extent and consequences of this influence have yet to be investigated. Here it is shown that dense water propagation to the deep ocean increases the abundance of prokaryotic plankton, and stimulates carbon production and organic matter degradation rates. Dense waters spilling off the shelf modifies community composition of deep sea microbial assemblages, leading to the increased relevance of taxa likely originating from the sea surface and the seafloor. This phenomenon can be explained by a combination of factors that interplay during the dense waters propagation, such as the transport of surface microbes to the ocean floor (delivering in our site 0.1 megatons of C), the stimulation of microbial metabolism due to increased ventilation and nutrients availability, the sediment re-suspension, and the mixing with ambient waters along the path. Thus, these results highlight a hitherto unidentified role for dense currents flowing over continental shelves in influencing deep sea microbes. In light of climate projections, this process will affect significantly the microbial functioning and biogeochemical cycling of large sectors of the ocean interior.

Ecosystem productivity is associated with bacterial phylogenetic distance in surface marine waters.

Understanding the link between community diversity and ecosystem function is a fundamental aspect of ecology. Systematic losses in biodiversity are widely acknowledged but the impact this may exert on ecosystem functioning remains ambiguous. There is growing evidence of a positive relationship between species richness and ecosystem productivity for terrestrial macro-organisms, but similar links for marine micro-organisms, which help drive global climate, are unclear. Community manipulation experiments show both positive and negative relationships for microbes. These previous studies rely, however, on artificial communities and any links between the full diversity of active bacterial communities in the environment, their phylogenetic relatedness and ecosystem function remain hitherto unexplored. Here, we test the hypothesis that productivity is associated with diversity in the metabolically active fraction of microbial communities. We show in natural assemblages of active bacteria that communities containing more distantly related members were associated with higher bacterial production. The positive phylogenetic diversity-productivity relationship was independent of community diversity calculated as the Shannon index. From our long-term (7-year) survey of surface marine bacterial communities, we also found that similarly, productive communities had greater phylogenetic similarity to each other, further suggesting that the traits of active bacteria are an important predictor of ecosystem productivity. Our findings demonstrate that the evolutionary history of the active fraction of a microbial community is critical for understanding their role in ecosystem functioning.

Historical contingency impacts on community assembly and ecosystem function in chemosynthetic marine ecosystems.

Predicting ecosystem functioning requires an understanding of the mechanisms that drive microbial community assembly. Many studies have explored microbial diversity extensively and environmental factors are thought to be the principal drivers of community composition. Community assembly is, however, also influenced by past conditions that might affect present-day assemblages. Historical events, called legacy effects or historical contingencies, remain poorly studied in the sea and their impact on the functioning of the communities is not known. We tested the influence, if any, of historical contingencies on contemporary community assembly and functions in a marine ecosystem. To do so, we verified if different inoculum communities colonizing the same substrate led to communities with different compositions. We inoculated wood with sea water microbes from different marine environments that differ in ecological and evolutionary history. Using 16S rRNA and metagenomic sequencing, it was demonstrated that historical contingencies change the composition and potential metabolisms of contemporary communities. The effect of historical events was transient, dominated by environmental selection as, over time, species sorting was a more important driver of community assembly. Our study shows not only that historical contingencies affect marine ecosystems but takes the analysis a step further by characterizing this effect as strong but transient.

The Impact of Methane on Microbial Communities at Marine Arctic Gas Hydrate Bearing Sediment.

Cold seeps are characterized by high biomass, which is supported by the microbial oxidation of the available methane by capable microorganisms. The carbon is subsequently transferred to higher trophic levels. South of Svalbard, five geological mounds shaped by the formation of methane gas hydrates, have been recently located. Methane gas seeping activity has been observed on four of them, and flares were primarily concentrated at their summits. At three of these mounds, and along a distance gradient from their summit to their outskirt, we investigated the eukaryotic and prokaryotic biodiversity linked to 16S and 18S rDNA. Here we show that local methane seepage and other environmental conditions did affect the microbial community structure and composition. We could not demonstrate a community gradient from the summit to the edge of the mounds. Instead, a similar community structure in any methane-rich sediments could be retrieved at any location on these mounds. The oxidation of methane was largely driven by anaerobic methanotrophic Archaea-1 (ANME-1) and the communities also hosted high relative abundances of sulfate reducing bacterial groups although none demonstrated a clear co-occurrence with the predominance of ANME-1. Additional common taxa were observed and their abundances were likely benefiting from the end products of methane oxidation. Among these were sulfide-oxidizing Campilobacterota, organic matter degraders, such as Bathyarchaeota, Woesearchaeota, or thermoplasmatales marine benthic group D, and heterotrophic ciliates and Cercozoa.

Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake.

Permafrost thawing results in the formation of thermokarst lakes, which are biogeochemical hotspots in northern landscapes and strong emitters of greenhouse gasses to the atmosphere. Most studies of thermokarst lakes have been in summer, despite the predominance of winter and ice-cover over much of the year, and the microbial ecology of these waters under ice remains poorly understood. Here we first compared the summer versus winter microbiomes of a subarctic thermokarst lake using DNA- and RNA-based 16S rRNA amplicon sequencing and qPCR. We then applied comparative metagenomics and used genomic bin reconstruction to compare the two seasons for changes in potential metabolic functions in the thermokarst lake microbiome. In summer, the microbial community was dominated by Actinobacteria and Betaproteobacteria, with phototrophic and aerobic pathways consistent with the utilization of labile and photodegraded substrates. The microbial community was strikingly different in winter, with dominance of methanogens, Planctomycetes, Chloroflexi and Deltaproteobacteria, along with various taxa of the Patescibacteria/Candidate Phyla Radiation (Parcubacteria, Microgenomates, Omnitrophica, Aminicenantes). The latter group was underestimated or absent in the amplicon survey, but accounted for about a third of the metagenomic reads. The winter lineages were associated with multiple reductive metabolic processes, fermentations and pathways for the mobilization and degradation of complex organic matter, along with a strong potential for syntrophy or cross-feeding. The results imply that the summer community represents a transient stage of the annual cycle, and that carbon dioxide and methane production continue through the prolonged season of ice cover via a taxonomically distinct winter community and diverse mechanisms of permafrost carbon transformation.

Bacteria alone establish the chemical basis of the wood-fall chemosynthetic ecosystem in the deep-sea.

Wood-fall ecosystems host chemosynthetic bacteria that use hydrogen sulfide as an electron donor. The production of hydrogen sulfide from decaying wood in the deep-sea has long been suspected to rely on the activity of wood-boring bivalves, Xylophaga spp. However, recent mesocosm experiments have shown hydrogen sulfide production in the absence of wood borers. Here, we combined in situ chemical measurements, amplicon sequencing and metagenomics to test whether the presence of Xylophaga spp.-affected hydrogen sulfide production and wood microbial community assemblages. During a short-term experiment conducted in a deep-sea canyon, we found that wood-fall microbial communities could produce hydrogen sulfide in the absence of Xylophaga spp. The presence of wood borers had a strong impact on the microbial community composition on the wood surface but not in the wood centre, where communities were observed to be homogeneous among different samples. When wood borers were excluded, the wood centre community did not have the genetic potential to degrade cellulose or hemicellulose but could use shorter carbohydrates such as sucrose. We conclude that wood centre communities produce fermentation products that can be used by the sulfate-reducing bacteria detected near the wood surface. We thus demonstrate that microorganisms alone could establish the chemical basis essential for the recruitment of chemolithotrophic organisms in deep-sea wood falls.

Ecological succession leads to chemosynthesis in mats colonizing wood in sea water.

Chemosynthetic mats involved in cycling sulfur compounds are often found in hydrothermal vents, cold seeps and whale falls. However, there are only few records of wood fall mats, even though the presence of hydrogen sulfide at the wood surface should create a perfect niche for sulfide-oxidizing bacteria. Here we report the growth of microbial mats on wood incubated under conditions that simulate the Mediterranean deep-sea temperature and darkness. We used amplicon and metagenomic sequencing combined with fluorescence in situ hybridization to test whether a microbial succession occurs during mat formation and whether the wood fall mats present chemosynthetic features. We show that the wood surface was first colonized by sulfide-oxidizing bacteria belonging to the Arcobacter genus after only 30 days of immersion. Subsequently, the number of sulfate reducers increased and the dominant Arcobacter phylotype changed. The ecological succession was reflected by a change in the metabolic potential of the community from chemolithoheterotrophs to potential chemolithoautotrophs. Our work provides clear evidence for the chemosynthetic nature of wood fall ecosystems and demonstrates the utility to develop experimental incubation in the laboratory to study deep-sea chemosynthetic mats.

Temporal and spatial constraints on community assembly during microbial colonization of wood in seawater.

Wood falls on the ocean floor form chemosynthetic ecosystems that remain poorly studied compared with features such as hydrothermal vents or whale falls. In particular, the microbes forming the base of this unique ecosystem are not well characterized and the ecology of communities is not known. Here we use wood as a model to study microorganisms that establish and maintain a chemosynthetic ecosystem. We conducted both aquaria and in situ deep-sea experiments to test how different environmental constraints structure the assembly of bacterial, archaeal and fungal communities. We also measured changes in wood lipid concentrations and monitored sulfide production as a way to detect potential microbial activity. We show that wood falls are dynamic ecosystems with high spatial and temporal community turnover, and that the patterns of microbial colonization change depending on the scale of observation. The most illustrative example was the difference observed between pine and oak wood community dynamics. In pine, communities changed spatially, with strong differences in community composition between wood microhabitats, whereas in oak, communities changed more significantly with time of incubation. Changes in community assembly were reflected by changes in phylogenetic diversity that could be interpreted as shifts between assemblies ruled by species sorting to assemblies structured by competitive exclusion. These ecological interactions followed the dynamics of the potential microbial metabolisms accompanying wood degradation in the sea. Our work showed that wood is a good model for creating and manipulating chemosynthetic ecosystems in the laboratory, and attracting not only typical chemosynthetic microbes but also emblematic macrofaunal species.

Microbial communities in sunken wood are structured by wood-boring bivalves and location in a submarine canyon.

The cornerstones of sunken wood ecosystems are microorganisms involved in cellulose degradation. These can either be free-living microorganisms in the wood matrix or symbiotic bacteria associated with wood-boring bivalves such as emblematic species of Xylophaga, the most common deep-sea woodborer. Here we use experimentally submerged pine wood, placed in and outside the Mediterranean submarine Blanes Canyon, to compare the microbial communities on the wood, in fecal pellets of Xylophaga spp. and associated with the gills of these animals. Analyses based on tag pyrosequencing of the 16S rRNA bacterial gene showed that sunken wood contained three distinct microbial communities. Wood and pellet communities were different from each other suggesting that Xylophaga spp. create new microbial niches by excreting fecal pellets into their burrows. In turn, gills of Xylophaga spp. contain potential bacterial symbionts, as illustrated by the presence of sequences closely related to symbiotic bacteria found in other wood eating marine invertebrates. Finally, we found that sunken wood communities inside the canyon were different and more diverse than the ones outside the canyon. This finding extends to the microbial world the view that submarine canyons are sites of diverse marine life.