Resilience of cold-water coral holobionts to thermal stress.

Cold-water corals are threatened by global warming, especially in the Mediterranean Sea where they live close to their upper known thermal limit (i.e. 13°C), yet their response to rising temperatures is not well known. Here, temperature effects on Lophelia pertusa and Madrepora oculata holobionts (i.e. the host and its associated microbiome) were investigated. We found that at warmer seawater temperature (+2°C), L. pertusa showed a modification of its microbiome prior to a change in behaviour, leading to lower energy reserves and skeletal growth, whereas M. oculata was more resilient. At extreme temperature (+4°C), both species quickly lost their specific bacterial signature followed by lower physiological activity prior to death. In addition, our results showing the holobionts' negative response to colder temperatures (-3°C), suggest that Mediterranean corals live close to their thermal optimum. The species-specific response to temperature change highlights that global warming may affect dramatically the main deep-sea reef-builders, which would alter the associated biodiversity and related ecosystem services.

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.

Local Variability in Microbiome Composition and Growth Suggests Habitat Preferences for Two Reef-Building Cold-Water Coral Species.

Cold-water coral (CWC) ecosystems provide niches and nurseries for many deep-sea species. Lophelia pertusa and Madrepora oculata, two cosmopolitan species forming three dimensional structures, are found in cold waters under specific hydrological regimes that provide food and reoxygenation. There is now more information about their feeding, their growth and their associated microbiome, however, little is known about the influence of their habitat on their physiology, or on the composition of their bacterial community. The goal of this study was to test if the habitat of L. pertusa and M. oculata influenced the hosts associated bacterial communities, the corals' survival and their skeletal growth along the slope of a submarine canyon. A transplant experiment was used, based on sampling and cross-redeployment of coral fragments at two contrasted sites, one deeper and one shallower. Our results show that M. oculata had significantly higher skeletal growth rates in the shallower site and that it had a specific microbiome that did not change between sites. Inversely, L. pertusa had the same growth rates at both sites, but its bacterial community compositions differed between locations. Additionally, transplanted L. pertusa acquired the microbial signature of the local corals. Thus, our results suggest that M. oculata prefer the shallower habitat.

Diet shapes cold-water corals bacterial communities.

Different cold-water coral (CWC) species harbour distinct microbial communities and the community composition is thought to be linked to the ecological strategies of the host. Here we test whether diet shapes the composition of bacterial communities associated with CWC. We compared the microbiomes of two common CWC species in aquaria, Lophelia pertusa and Madrepora oculata, when they were either starved, or fed respectively with a carnivorous diet, two different herbivorous diets, or a mix of the 3. We targeted both the standing stock (16S rDNA) and the active fraction (16S rRNA) of the bacterial communities and showed that in both species, the corals' microbiome was specific to the given diet. A part of the microbiome remained, however, species-specific, which indicates that the microbiome's plasticity is framed by the identity of the host. In addition, the storage lipid content of the coral tissue showed that different diets had different effects on the corals' metabolisms. The combined results suggest that L. pertusa may be preying preferentially on zooplankton while M. oculata may in addition use phytoplankton and detritus. The results cast a new light on coral microbiomes as they indicate that a portion of the CWC's bacterial community could represent a food influenced microbiome.

Long-term aquaria study suggests species-specific responses of two cold-water corals to macro-and microplastics exposure.

Plastic pollution has been identified as a major threat for coastal marine life and ecosystems. Here, we test if the feeding behaviour and growth rate of the two most common cold-water coral species, Lophelia pertusa and Madrepora oculata, are affected by micro- or macroplastic exposures. Low-density polyethylene microplastics impair prey capture and growth rates of L. pertusa after five months of exposure. Macroplastic films, mimicking plastic bags trapped on deep-sea reefs, had however a limited impact on L. pertusa growth. This was due to an avoidance behaviour illustrated by the formation of skeletal 'caps' that changed the polyp orientation and allowed its access to food supply. On the contrary, M. oculata growth and feeding were not affected by plastic exposure. Such a species-specific response has the potential to induce a severe change in coral community composition and the associated biodiversity in deep-sea environments.

The Effect of Captivity on the Dynamics of Active Bacterial Communities Differs Between Two Deep-Sea Coral Species.

Microbes play a crucial role in sustaining the coral holobiont's functions and in particular under the pressure of environmental stressors. The effect of a changing environment on coral health is now a major branch of research that relies heavily on aquarium experiments. However, the effect of captivity on the coral microbiome remains poorly known. Here we show that different cold-water corals species have different microbiome responses to captivity. For both the DNA and the RNA fraction, Madrepora oculata bacterial communities were maintained for at least 6 months of aquarium rearing, while Lophelia pertusa bacteria changed within a day. Interestingly, bacteria from the genus Endozoicomonas, a ubiquitous symbiont of numerous marine hosts, were resilient and remained active in M. oculata for several months. Our results demonstrate that a good knowledge of the coral microbiome and an understanding of the ecological strategy of the holobiont is needed before designing aquarium experiments.

Co-occurring nematodes and bacteria in submarine canyon sediments.

In submarine canyon sediments, bacteria and nematodes dominate the benthic biomass and play a key role in nutrient cycling and energy transfer. The diversity of these communities remains, however, poorly studied. This work aims at describing the composition of bacteria and nematode communities in the Lacaze-Duthiers submarine canyon in the north-western Mediterranean Sea. We targeted three sediment depths for two consecutive years and investigated the communities using nuclear markers (18S rRNA and 16S rRNA genes). High throughput sequencing combined to maximal information coefficient (MIC) statistical analysis allowed us to identify, for the first time, at the same small scale, the community structures and the co-occurrence of nematodes and bacteria Operational Taxonomic Units across the sediment cores. The associations detected by MIC revealed marked patterns of co-occurrences between the bacteria and nematodes in the sediment of the canyon and could be linked to the ecological requirements of individual bacteria and nematodes. For the bacterial community, Delta- and Gammaproteobacteria sequences were the most abundant, as seen in some canyons earlier, although Acidobacteria, Actinobacteria and Planctomycetes have been prevalent in other canyon sediments. The 20 identified nematode genera included bacteria feeders as Terschellingia, Eubostrichus, Geomonhystera, Desmoscolex and Leptolaimus. The present study provides new data on the diversity of bacterial and nematodes communities in the Lacaze-Duthiers canyon and further highlights the importance of small-scale sampling for an accurate vision of deep-sea communities.

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.

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.

Disturbance Increases Microbial Community Diversity and Production in Marine Sediments.

Disturbance strongly impacts patterns of community diversity, yet the shape of the diversity-disturbance relationship remains a matter of debate. The topic has been of interest in theoretical ecology for decades as it has practical implications for the understanding of ecosystem services in nature. One of these processes is the remineralization of organic matter by microorganisms in coastal marine sediments, which are periodically impacted by disturbances across the sediment-water interface. Here we set up an experiment to test the hypothesis that disturbance impacts microbial diversity and function during the anaerobic degradation of organic matter in coastal sediments. We show that during the first 3 weeks of the experiment, disturbance increased both microbial production, derived from the increase in microbial abundance, and diversity of the active fraction of the community. Both community diversity and phylogenetic diversity increased, which suggests that disturbance promoted the cohabitation of ecologically different microorganisms. Metagenome analysis also showed that disturbance increased the relative abundance of genes diagnostic of metabolism associated with the sequential anaerobic degradation of organic matter. However, community composition was not impacted in a systematic way and changed over time. In nature, we can hypothesize that moderate storm disturbances, which impact coastal sediments, promote diverse, and productive communities. These events, rather than altering the decomposition of organic matter, may increase the substrate turnover and, ultimately, remineralization rates.