2021 |
Dittami, S. M., et al. "A community perspective on the concept of marine holobionts: current status, challenges, and future directions." PeerJ. 9 (2021): e10911.
Résumé: Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g., the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. Here we propose that one significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This first step is crucial to decipher the main drivers of the dynamics and evolution of holobionts and to account for the holobiont concept in applied areas, such as the conservation, management, and exploitation of marine ecosystems and resources, where practical solutions to predict and mitigate the impact of human activities are more important than ever.
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Escalas, A., et al. "Ecological Specialization Within a Carnivorous Fish Family Is Supported by a Herbivorous Microbiome Shaped by a Combination of Gut Traits and Specific Diet." Front. Mar. Sci.. 8 (2021): 622883.
Résumé: Animals have been developing key associations with micro-organisms through evolutionary processes and ecological diversification. Hence, in some host clades, phylogenetic distance between hosts is correlated to dissimilarity in microbiomes, a pattern called phylosymbiosis. Teleost fishes, despite being the most diverse and ancient group of vertebrates, have received little attention from the microbiome perspective and our understanding of its determinants is currently limited. In this study, we assessed the gut microbiome of 12 co-occurring species of teleost representing a large breadth of ecological diversity and originating from a single family (i.e., the Sparidae). We tested how host evolutionary history, diet composition and morphological traits are related to fish gut microbiome. Despite fish species having different microbiomes, there is no phylosymbiosis signal in this fish family, but gut length and diet had a strong influence on the microbiome. We revealed that the only species with a specialized herbivorous diet, Sarpa salpa had a 3.3 times longer gut than carnivorous species and such a long gut favor the presence of anaerobic bacteria typical of herbivorous gut microbiomes. Hence, dietary uniqueness is paired with both unique gut anatomy and unique microbiome.
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2020 |
Chiarello, M., et al. "Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes." Proc. R. Soc. B-Biol. Sci.. 287.1927 (2020): 20200642.
Résumé: Coral reefs host hundreds of thousands of animal species that are increasingly threatened by anthropogenic disturbances. These animals host microbial communities at their surface, playing crucial roles for their fitness. However, the diversity of such microbiomes is mostly described in a few coral species and still poorly defined in other invertebrates and vertebrates. Given the diversity of animal microbiomes, and the diversity of host species inhabiting coral reefs, the contribution of such microbiomes to the total microbial diversity of coral reefs could be important, yet potentially vulnerable to the loss of animal species. Analysis of the surface microbiome from 74 taxa, including teleost fishes, hard and soft corals, crustaceans, echinoderms, bivalves and sponges, revealed that more than 90% of their prokaryotic phylogenetic richness was specific and not recovered in surrounding plankton. Estimate of the total richness associated with coral reef animal surface microbiomes reached up to 2.5% of current estimates of Earth prokaryotic diversity. Therefore, coral reef animal surfaces should be recognized as a hotspot of marine microbial diversity. Loss of the most vulnerable reef animals expected under present-day scenarios of reef degradation would induce an erosion of 28% of the prokaryotic richness, with unknown consequences on coral reef ecosystem functioning.
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Dupont, S., et al. "Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses." Animal Microbiome. 2.1 (2020): 12.
Résumé: The impact of the microbiota on host fitness has so far mainly been demonstrated for the bacterial microbiome. We know much less about host-associated protist and viral communities, largely due to technical issues. However, all microorganisms within a microbiome potentially interact with each other as well as with the host and the environment, therefore likely affecting the host health.
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Pereira, O., et al. "Seasonality of archaeal proteorhodopsin and associated Marine Group IIb ecotypes (Ca. Poseidoniales) in the North Western Mediterranean Sea." Isme J. (2020).
Résumé: The Archaea Marine Group II (MGII) is widespread in the world's ocean where it plays an important role in the carbon cycle. Despite recent discoveries on the group's metabolisms, the ecology of this newly proposed order (Candidatus Poseidoniales) remains poorly understood. Here we used a combination of time-series metagenome-assembled genomes (MAGs) and high-frequency 16S rRNA data from the NW Mediterranean Sea to test if the taxonomic diversity within the MGIIb family (Candidatus Thalassarchaeaceae) reflects the presence of different ecotypes. The MAGs' seasonality revealed a MGIIb family composed of different subclades that have distinct lifestyles and physiologies. The vitamin metabolisms were notably different between ecotypes with, in some, a possible link to sunlight's energy. Diverse archaeal proteorhodopsin variants, with unusual signature in key amino acid residues, had distinct seasonal patterns corresponding to changing day length. In addition, we show that in summer, archaea, as opposed to bacteria, disappeared completely from surface waters. Our results shed light on the diversity and the distribution of the euryarchaeotal proteorhodopsin, and highlight that MGIIb is a diverse ecological group. The work shows that time-series based studies of the taxonomy, seasonality, and metabolisms of marine prokaryotes is critical to uncover their diverse role in the ocean.
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2019 |
Pereira, O., et al. "Genomic ecology of Marine Group II, the most common marine planktonic Archaea across the surface ocean." MicrobiologyOpen. 8.9 (2019): e852.
Résumé: Planktonic Archaea have been detected in all the world's oceans and are found from surface waters to the deep sea. The two most common Archaea phyla are Thaumarchaeota and Euryarchaeota. Euryarchaeota are generally more common in surface waters, but very little is known about their ecology and their potential metabolisms. In this study, we explore the genomic ecology of the Marine Group II (MGII), the main marine planktonic Euryarchaeota, and test if it is composed of different ecologically relevant units. We re-analyzed Tara Oceans metagenomes from the photic layer and the deep ocean by annotating sequences against a custom MGII database and by mapping gene co-occurrences. Our data provide a global view of the distribution of Euryarchaeota, and more specifically of MGII subgroups, and reveal their association to a number of gene-coding sequences. In particular, we show that MGII proteorhodopsins were detected in both the surface and the deep chlorophyll maximum layer and that different clusters of these light harvesting proteins were present. Our approach helped describing the set of genes found together with specific MGII subgroups. We could thus define genomic environments that could theoretically describe ecologically meaningful units and the ecological niche that they occupy.
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Ranchou-Peyruse, M., et al. "Geological gas-storage shapes deep life." Environ. Microbiol. (2019).
Résumé: Around the world, several dozen deep sedimentary aquifers are being used for storage of natural gas. Ad hoc studies of the microbial ecology of some of them have suggested that sulfate reducing and methanogenic microorganisms play a key role in how these aquifers' communities function. Here, we investigate the influence of gas storage on these two metabolic groups by using high-throughput sequencing and show the importance of sulfate-reducing Desulfotomaculum and a new monophyletic methanogenic group. Aquifer microbial diversity was significantly related to the geological level. The distance to the stored natural gas affects the ratio of sulfate-reducing Firmicutes to deltaproteobacteria. In only one aquifer, the methanogenic archaea dominate the sulfate-reducers. This aquifer was used to store town gas (containing at least 50% H-2) around 50 years ago. The observed decrease of sulfates in this aquifer could be related to stimulation of subsurface sulfate-reducers. These results suggest that the composition of the microbial communities is impacted by decades old transient gas storage activity. The tremendous stability of these gas-impacted deep subsurface microbial ecosystems suggests that in situ biotic methanation projects in geological reservoirs may be sustainable over time.
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Robino, E., et al. "Resistance of the oyster pathogen Vibrio tasmaniensis LGP32 against grazing by Vannella sp. marine amoeba involves Vsm and CopA virulence factors." Environ. Microbiol. (2019).
Résumé: Vibrios are ubiquitous in marine environments and opportunistically colonize a broad range of hosts. Strains of Vibrio tasmaniensis present in oyster farms can thrive in oysters during juvenile mortality events and behave as facultative intracellular pathogen of oyster haemocytes. Herein, we wondered whether V. tasmaniensis LGP32 resistance to phagocytosis is specific to oyster immune cells or contributes to resistance to other phagocytes, like marine amoebae. To address this question, we developed an integrative study, from the first description of amoeba diversity in oyster farms to the characterization of LGP32 interactions with amoebae. An isolate of the Vannella genus, Vannella sp. AP1411, which was collected from oyster farms, is ubiquitous, and belongs to one clade of Vannella that could be found associated with Vibrionaceae. LGP32 was shown to be resistant to grazing by Vannella sp. AP1411 and this phenotype depends on some previously identified virulence factors: secreted metalloprotease Vsm and copper efflux p-ATPase CopA, which act at different steps during amoeba-vibrio interactions, whereas some other virulence factors were not involved. Altogether, our work indicates that some virulence factors can be involved in multi-host interactions of V. tasmaniensis ranging from protozoans to metazoans, potentially favouring their opportunistic behaviour.
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2018 |
Bettarel, Y., et al. "Corallivory and the microbial debacle in two branching scleractinians." Isme J.. 12.4 (2018): 1109–1126.
Résumé: The grazing activity by specific marine organisms represents a growing threat to the survival of many scleractinian species. For example, the recent proliferation of the corallivorous gastropod Drupella now constitutes a critical case in all South-East Asian waters. If the damaging effects caused by this marine snail on coral polyps are relatively well known, the indirect incidence of predation on coral microbial associates is still obscure and might also potentially impair coral health. In this study, we compared the main ecological traits of coral-associated bacterial and viral communities living in the mucus layer of Acropora formosa and Acropora millepora, of healthy and predated individuals (i.e., colonized by Drupella rugosa), in the Bay of Van Phong (Vietnam). Our results show a substantial impact of the gastropod on a variety of microbiological markers. Colonized corals harbored much more abundant and active epibiotic bacteria whose community composition shifted toward more pathogenic taxa (belonging to the Vibrionales, Clostridiales, Campylobacterales, and Alteromonadales orders), together with their specific phages. Viral epibionts were also greatly influenced by Drupella corallivory with spectacular modifications in their concentrations, life strategies, genotype richness, and diversity. Novel and abundant circular Rep-encoding ssDNA viruses (CRESS-DNA viruses) were detected and characterized in grazed corals and we propose that their occurrence may serve as indicator of the coral health status. Finally, our results reveal that corallivory can cause severe dysbiosis by altering virus-bacteria interactions in the mucus layer, and ultimately favoring the development of local opportunistic infections.
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Chiarello, M., et al. "Skin microbiome of coral reef fish is highly variable and driven by host phylogeny and diet." Microbiome. 6 (2018): 147.
Résumé: Background: The surface of marine animals is covered by abundant and diversified microbial communities, which have major roles for the health of their host While such microbiomes have been deeply examined in marine invertebrates such as corals and sponges, the microbiomes living on marine vertebrates have received less attention. Specifically, the diversity of these microbiomes, their variability among species, and their drivers are still mostly unknown, especially among the fish species living on coral reefs that contribute to key ecosystem services while they are increasingly affected by human activities. Here, we investigated these knowledge gaps analyzing the skin microbiome of 138 fish individuals belonging to 44 coral reef fish species living in the same area. Results: Prokaryotic communities living on the skin of coral reef fishes are highly diverse, with on average more than 600 OTUs per fish, and differ from planktonic microbes. Skin microbiomes varied between fish individual and species, and interspecific differences were slightly coupled to the phylogenetic affiliation of the host and its ecological traits. Conclusions: These results highlight that coral reef biodiversity is greater than previously appreciated, since the high diversity of macro-organisms supports a highly diversified microbial community. This suggest that beyond the loss of coral reefs-associated macroscopic species, anthropic activities on coral reefs could also lead to a loss of still unexplored host-associated microbial diversity, which urgently needs to be assessed.
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Compte-Port, S., et al. "Metal contaminations impact archaeal community composition, abundance and function in remote alpine lakes." Environ. Microbiol.. 20.7 (2018): 2422–2437.
Résumé: 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 (10(5) to 10(9) 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.
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Galand, P. E., et al. "A strong link between marine microbial community composition and function challenges the idea of functional redundancy." Isme J.. 12.10 (2018): 2470–2478.
Résumé: Marine microbes have tremendous diversity, but a fundamental question remains unanswered: why are there so many microbial species in the sea? The idea of functional redundancy for microbial communities has long been assumed, so that the high level of richness is often explained by the presence of different taxa that are able to conduct the exact same set of metabolic processes and that can readily replace each other. Here, we refute the hypothesis of functional redundancy for marine microbial communities by showing that a shift in the community composition altered the overall functional attributes of communities across different temporal and spatial scales. Our metagenomic monitoring of a coastal northwestern Mediterranean site also revealed that diverse microbial communities harbor a high diversity of potential proteins. Working with all information given by the metagenomes (all reads) rather than relying only on known genes (annotated orthologous genes) was essential for revealing the similarity between taxonomic and functional community compositions. Our finding does not exclude the possibility for a partial redundancy where organisms that share some specific function can coexist when they differ in other ecological requirements. It demonstrates, however, that marine microbial diversity reflects a tremendous diversity of microbial metabolism and highlights the genetic potential yet to be discovered in an ocean of microbes.
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Sebastián, M., et al. "Deep ocean prokaryotic communities are remarkably malleable when facing long-term starvation." Environmental Microbiology. 20.2 (2018): 713–723.
Résumé: The bathypelagic ocean is one of the largest ecosystems on Earth and sustains half of the ocean's microbial activity. This microbial activity strongly relies on surface-derived particles, but there is growing evidence that the carbon released through solubilization of these particles may not be sufficient to meet the energy demands of deep ocean prokaryotes. To explore how bathypelagic prokaryotes respond to the absence of external inputs of carbon, we followed the long-term (1 year) dynamics of an enclosed community. Despite the lack of external energy supply, we observed a continuous succession of active prokaryotic phylotypes, which was driven by recruitment of taxa from the seed bank (i.e., initially rare operational taxonomic units [OTUs]). A single OTU belonging to Marine Group I of Thaumarchaeota, which was originally rare, dominated the microbial community for similar to 4 months and played a fundamental role in this succession likely by introducing new organic carbon through chemolithoautotrophy. This carbon presumably produced a priming effect, because after the decline of Thaumarchaeota, the diversity and metabolic potential of the community increased back to the levels present at the start of the experiment. Our study demonstrates the profound versatility of deep microbial communities when facing organic carbon deprivation.
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2017 |
Chiarello, M., et al. "Captive bottlenose dolphins and killer whales harbor a species-specific skin microbiota that varies among individuals." Scientific Reports. 7.1 (2017): 15269.
Résumé: Marine animals surfaces host diverse microbial communities, which play major roles for host’s health. Most inventories of marine animal surface microbiota have focused on corals and fishes, while cetaceans remain overlooked. The few studies focused on wild cetaceans, making difficult to distinguish intrinsic inter- and/or intraspecific variability in skin microbiota from environmental effects. We used high-throughput sequencing to assess the skin microbiota from 4 body zones of 8 bottlenose dolphins (Tursiops truncatus) and killer whales (Orcinus orca), housed in captivity (Marineland park, France). Overall, cetacean skin microbiota is more diverse than planktonic communities and is dominated by different phylogenetic lineages and functions. In addition, the two cetacean species host different skin microbiotas. Within each species, variability was higher between individuals than between body parts, suggesting a high individuality of cetacean skin microbiota. Overall, the skin microbiota of the assessed cetaceans related more to the humpback whale and fishes’ than to microbiotas of terrestrial mammals.
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2016 |
Fillol, M., et al. "Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage." Isme J. 10.3 (2016): 665–677.
Résumé: Members of the archaeal Miscellaneous Crenarchaeotic Group (MCG) are among the most successful microorganisms on the planet. During its evolutionary diversification, this very diverse group has managed to cross the saline–freshwater boundary, one of the most important evolutionary barriers structuring microbial communities. However, the current understanding on the ecological significance of MCG in freshwater habitats is scarce and the evolutionary relationships between freshwater and saline MCG remains poorly known. Here, we carried out molecular phylogenies using publicly available 16S rRNA gene sequences from various geographic locations to investigate the distribution of MCG in freshwater and saline sediments and to evaluate the implications of saline–freshwater transitions during the diversification events. Our approach provided a robust ecological framework in which MCG archaea appeared as a core generalist group in the sediment realm. However, the analysis of the complex intragroup phylogeny of the 21 subgroups currently forming the MCG lineage revealed that distinct evolutionary MCG subgroups have arisen in marine and freshwater sediments suggesting the occurrence of adaptive evolution specific to each habitat. The ancestral state reconstruction analysis indicated that this segregation was mainly due to the occurrence of a few saline–freshwater transition events during the MCG diversification. In addition, a network analysis showed that both saline and freshwater MCG recurrently co-occur with archaea of the class Thermoplasmata in sediment ecosystems, suggesting a potentially relevant trophic connection between the two clades.
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Jeanbille, M., et al. "Response of Core Microbial Consortia to Chronic Hydrocarbon Contaminations in Coastal Sediment Habitats." Front. Microbiol. (2016): 1637.
Résumé: Traditionally, microbial surveys investigating the effect of chronic anthropogenic pressure such as polyaromatic hydrocarbons (PAHs) contaminations consider just the alpha and beta diversity and ignore the interactions among the different taxa forming the microbial community. Here, we investigated the ecological relationships between the three domains of life (i.e., Bacteria, Archaea, and Eukarya) using 454 pyrosequencing on the 16S rRNA and 18S rRNA genes from chronically impacted and pristine sediments, along the coasts of the Mediterranean Sea (Gulf of Lion, Vermillion coast, Corsica, Bizerte lagoon and Lebanon) and the French Atlantic Ocean (Bay of Biscay and English Channel). Our approach provided a robust ecological framework for the partition of the taxa abundance distribution into 859 core Operational taxonomic units (OTUs) and 6629 satellite OTUs. OTUs forming the core microbial community showed the highest sensitivity to changes in environmental and contaminant variations, with salinity, latitude, temperature, particle size distribution, total organic carbon (TOC) and PAH concentrations as main drivers of community assembly. The core communities were dominated by Gammaproteobacteria and Deltaproteobacteria for Bacteria, by Thaumarchaeota, Bathyarchaeota and Thermoplasmata for Archaea and Metazoa and Dinoflagellata for Eukarya. In order to find associations among microorganisms, we generated a co-occurrence network in which PAHs were found to impact significantly the potential predator – prey relationship in one microbial consortium composed of ciliates and Actinobacteria. Comparison of network topological properties between contaminated and non-contaminated samples showed substantial differences in the network structure and indicated a higher vulnerability to environmental perturbations in the contaminated sediments.
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Jeanbille, M., et al. "Chronic Polyaromatic Hydrocarbon (PAH) Contamination Is a Marginal Driver for Community Diversity and Prokaryotic Predicted Functioning in Coastal Sediments." Front. Microbiol.. 7 (2016): Unsp-1303.
Résumé: Benthic microorganisms are key players in the recycling of organic matter and recalcitrant compounds such as polyaromatic hydrocarbons (PAHs) in coastal sediments. Despite their ecological importance, the response of microbial communities to chronic PAH pollution, one of the major threats to coastal ecosystems, has received very little attention. In one of the largest surveys performed so far on coastal sediments, the diversity and composition of microbial communities inhabiting both chronically contaminated and non-contaminated coastal sediments were investigated using high throughput sequencing on the 18S and 16S rRNA genes. Prokaryotic alpha-diversity showed significant association with salinity, temperature, and organic carbon content. The effect of particle size distribution was strong on eukaryotic diversity. Similarly to alpha-diversity, beta diversity patterns were strongly influenced by the environmental filter, while PAHs had no influence on the prokaryotic community structure and a weak impact on the eukaryotic community structure at the continental scale. However, at the regional scale, PAHs became the main driver shaping the structure of bacterial and eukaryotic communities. These patterns were not found for PICRUSt predicted prokaryotic functions, thus indicating some degree of functional redundancy. Eukaryotes presented a greater potential for their use as PAH contamination biomarkers, owing to their stronger response at both regional and continental scales.
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Roux, S., et al. "Analysis of metagenomic data reveals common features of halophilic viral communities across continents." Environ Microbiol. 18.3 (2016): 889–903.
Résumé: Microbial communities from hypersaline ponds, dominated by halophilic archaea, are considered specific of such extreme conditions. The associated viral communities have accordingly been shown to display specific features, such as similar morphologies among different sites. However, little is known about the genetic diversity of these halophilic viral communities across the Earth. Here, we studied viral communities in hypersaline ponds sampled on the coast of Senegal (8–36% of salinity) using metagenomics approach, and compared them with hypersaline viromes from Australia and Spain. The specificity of hyperhalophilic viruses could first be demonstrated at a community scale, salinity being a strong discriminating factor between communities. For the major viral group detected in all samples (Caudovirales), only a limited number of halophilic Caudovirales clades were highlighted. These clades gather viruses from different continents and display consistent genetic composition, indicating that they represent related lineages with a worldwide distribution. Non-tailed hyperhalophilic viruses display a greater rate of gene transfer and recombination, with uncharacterized genes conserved across different kind of viruses and plasmids. Thus, hypersaline viral communities around the world appear to form a genetically consistent community that are likely to harbour new genes coding for enzymes specifically adapted to these environments.
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2015 |
Faure, D., et al. "Environmental microbiology as a mosaic of explored ecosystems and issues." Environmental Science and Pollution Research. 22.18 (2015): 13577–13598.
Résumé: Microbes are phylogenetically (Archaea, Bacteria, Eukarya, and viruses) and functionally diverse. They colonize highly varied environments and rapidly respond to and evolve as a response to local and global environmental changes, including those induced by pollutants resulting from human activities. This review exemplifies the Microbial Ecology EC2CO consortium's efforts to explore the biology, ecology, diversity, and roles of microbes in aquatic and continental ecosystems.
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Sarmento, H., et al. "Microbial food web components, bulk metabolism, and single-cell physiology of piconeuston in surface microlayers of high-altitude lakes." Front Microbiol. 6 (2015).
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2014 |
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Merbt, S. N., et al. "Wastewater Treatment Plant Effluents Change Abundance and Composition of Ammonia-Oxidizing Microorganisms in Mediterranean Urban Stream Biofilms." Microb Ecol (2014).
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Restrepo-Ortiz, C. X., J. C. Auguet, and E. O. Casamayor. "Targeting spatiotemporal dynamics of planktonic SAGMGC-1 and segregation of ammonia-oxidizing thaumarchaeota ecotypes by newly designed primers and quantitative polymerase chain reaction." Environmental Microbiology. 16.3 (2014): 689–700.
Résumé: The annual dynamics of three different ammonia-oxidizing archaea (AOA) ecotypes (amoA gene) and of the SAGMGC-1 (Nitrosotalea-like aquatic Thaumarchaeota) group (16S rRNA gene) were studied by newly designed specific primers and quantitative polymerase chain reaction analysis in a deep oligotrophic high mountain lake (Lake Redon, Limnological Observatory of the Pyrenees, Spain). We observed segregated distributions of the main AOA populations, peaking separately in time and space, and under different ammonia concentrations and irradiance conditions. Strong positive correlation in gene abundances was found along the annual survey between 16S rRNA SAGMAGC-1 and one of the amoA ecotypes suggesting the potential for ammonia oxidation in the freshwater SAGMAGC-1 clade. We also observed dominance of Nitrosotalea-like ecotypes over Nitrosopumilus-like (Marine Group 1.1a) and not the same annual dynamics for the two thaumarchaeotal clades. The fine scale segregation in space and time of the different AOA ecotypes indicated the presence of phylogenetically close but ecologically segregated AOA species specifically adapted to specific environmental conditions. It remains to be elucidated what would be such environmental drivers.
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2013 |
Auguet, J. C., and E. O. Casamayor. "Partitioning of Thaumarchaeota populations along environmental gradients in high mountain lakes." FEMS Microbiology Ecology. 84.1 (2013): 154–164.
Résumé: We investigated the spatial distribution and diversity of ammonia-oxidizing Archaea (AOA) across gradients of pH, trophic status and altitude in a set of high mountain lakes (Limnological Observatory of the Pyrenees, north-east Spain). Both phylogeny- and taxonomy-based approaches revealed well-defined AOA community patterns with pH as the main potential driving environmental factor. The I.1a and SAGMGC-1 Thaumarchaeota clusters, and their potentially associated amoA gene variants (clusters Fresh 5 and Soil/Fresh 1, respectively) showed highest relative abundances in the most oligotrophic lakes. Euryarchaeota (i.e. HV-Fresh cluster, Methanomicrobiales and Thermoplasmatales) dominated in lakes with higher trophic status. Phylogenetic diversity (PD) in Pyrenean lakes was 1.5- to 2.3-fold higher than the PD from an equivalent number of globally distributed marine and soil sites. We observed segregated distributions for SAGMGC-1, preferentially distributed in the lakes with the lowest pH (< 5) and the highest nitrite concentration (> 0.12 μm), and I.1a in lakes with lower nitrite and dissolved organic carbon concentrations below 0.5 mg L-1. Overall, these results showed strong selection by local environmental conditions, unveiled new ecological niches for freshwater SAGMGC-1 in low pH oligotrophic lakes, and suggested specific and successful adaptations of planktonic archaea to the high mountain lakes landscape. © 2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.
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Cao, H., J. - C. Auguet, and J. - D. Gu. "Global ecological pattern of ammonia-oxidizing archaea." PLoS ONE. 8.2 (2013): e52853.
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Vila-Costa, M., et al. "Bacterial and archaeal community structure in the surface microlayer of high mountain lakes examined under two atmospheric aerosol loading scenarios." FEMS Microbiology Ecology (2013).
Résumé: Bacteria and Archaea of the air-water surface microlayer (neuston) and plankton from three high mountain lakes (Limnological Observatory of the Pyrenees, Spain) were analyzed by 16S rRNA gene 454 pyrosequencing (V6 region) in two dates with different atmospheric aerosol loading conditions: (i) under a Saharan dust plume driven by southern winds, and (ii) under northern winds with oceanic influence. In general, bacterial communities were richer than archaea, with estimated total richness of 2,500 OTUs for Bacteria and 900 OTUs for Archaea equivalent to a sequencing effort of 250,000 and 20,000 sequences, respectively. The dominant bacterial OTU was affiliated to Actinobacteria. Archaea were one to two orders-of-magnitude less abundant than bacteria but were more evenly distributed. Apparently, Bacteroidetes and Thaumarchaeota sequences were preferentially found at the neuston, but no consistent pattern in either total microbial abundance or richness was found in any sample. However, we observed more marked changes in microbial relative abundances between neuston and plankton in the dust-influenced scenario. Higher community dissimilarities between neuston and plankton were also found during the Saharan dust episode, and such differences were higher for Bacteria than for Archaea. Nonetheless, relatively few (<0.05%) of the neuston sequences matched previously identified airborne microbes, and none became important in the dates analyzed. © 2013 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved
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2012 |
Auguet, J. C., et al. "Vertical segregation and phylogenetic characterization of ammonia-oxidizing Archaea in a deep oligotrophic lake." Isme J. 6 (2012): 1786–1797.
Résumé: Freshwater habitats have been identified as one of the largest reservoirs of archaeal genetic diversity, with specific lineages of ammonia-oxidizing archaea (AOA) populations different from soils and seas. The ecology and biology of lacustrine AOA is, however, poorly known. In the present study, vertical changes in archaeal abundance by CARD-FISH, quantitative PCR (qPCR) analyses and identity by clone libraries were correlated with environmental parameters in the deep glacial high-altitude Lake Redon. The lake is located in the central Spanish Pyrenees where atmospheric depositions are the main source of reactive nitrogen. Strong correlations were found between abundance of thaumarchaeotal 16S rRNA gene, archaeal amoA gene and nitrite concentrations, indicating an ammonium oxidation potential by these microorganisms. The bacterial amoA gene was not detected. Three depths with potential ammonia-oxidation activity were unveiled along the vertical gradient, (i) on the top of the lake in winter-spring (that is, the 0 (o)C slush layers above the ice-covered sheet), (ii) at the thermocline and (iii) the bottom waters in summer-autumn. Overall, up to 90% of the 16S rRNA gene sequences matched Thaumarchaeota, mostly from both the Marine Group (MG) 1.1a (Nitrosoarchaeum-like) and the sister clade SAGMGC-1 (Nitrosotalea-like). Clone-libraries analysis showed the two clades changed their relative abundances with water depth being higher in surface and lower in depth for SAGMGC-1 than for MG 1.1a, reflecting a vertical phylogenetic segregation. Overall, the relative abundance and recurrent appearance of SAGMGC-1 suggests a significant environmental role of this clade in alpine lakes. These results expand the set of ecological and thermal conditions where Thaumarchaeota are distributed, unveiling vertical positioning in the water column as a key factor to understand the ecology of different thaumarchaeotal clades in lacustrine environments.
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Llorens-Marès, T., J. C. Auguet, and E. O. Casamayor. "Winter to Spring changes in the slush bacterial community composition of a high mountain lake (Lake Redon, Pyrenees)." Environ. Microbiol. Rep.. 4.1 (2012): 50–56.
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2011 |
Auguet, J. C., et al. "Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophic alpine lakes." Appl Environ Microbiol. 77.6 (2011): 1937–1945.
Résumé: The annual changes in the composition and abundance of ammonia-oxidizing archaea (AOA) were analyzed monthly in surface waters of three high mountain lakes within the Limnological Observatory of the Pyrenees (LOOP; northeast Spain) using both 16S rRNA and functional (ammonia monooxygenase gene, amoA) gene sequencing as well as quantitative PCR amplification. The set of biological data was related to changes in nitrogen species and to other relevant environmental variables. The whole archaeal assemblage was dominated by phylotypes closely related to the crenarchaeal 1.1a group (58% +/- 18% of total 16S rRNA gene sequences), and consistent structural changes were detected during the study. Water temperature was the environmental variable that better explained spring, summer, and winter (ice-covered lakes) archaeal assemblage structure. The amoA gene was detected year round, and seasonal changes in amoA gene composition were well correlated with changes in the archaeal 16S rRNA gene pool. In addition, copy numbers of both the specific 1.1a group 16 rRNA and archaeal amoA genes were well correlated, suggesting that most freshwater 1.1a Crenarchaeota had the potential to carry out ammonia oxidation. Seasonal changes in the diversity and abundance of AOA (i.e., amoA) were better explained by temporal changes in ammonium, the substrate for nitrification, and mostly nitrite, the product of ammonia oxidation. Lacustrine amoA gene sequences grouped in coherent freshwater phylogenetic clusters, suggesting that freshwater habitats harbor typical amoA-containing ecotypes, which is different from soils and seas. We observed within the freshwater amoA gene sequence pool a high genetic divergence (translating to up to 32% amino acid divergence) between the spring and the remaining AOA assemblages. This suggests that different AOA ecotypes are adapted to different temporal ecological niches in these lakes.
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Barberan, A., et al. "Phylogenetic ecology of widespread uncultured clades of the Kingdom Euryarchaeota." Mol Ecol. 20.9 (2011): 1988–1996.
Résumé: Despite its widespread distribution and high levels of phylogenetic diversity, microbes are poorly understood creatures. We applied a phylogenetic ecology approach in the Kingdom Euryarchaeota (Archaea) to gain insight into the environmental distribution and evolutionary history of one of the most ubiquitous and largely unknown microbial groups. We compiled 16S rRNA gene sequences from our own sequence libraries and public genetic databases for two of the most widespread mesophilic Euryarchaeota clades, Lake Dagow Sediment (LDS) and Rice Cluster-V (RC-V). The inferred population history indicated that both groups have undergone specific nonrandom evolution within environments, with several noteworthy habitat transition events. Remarkably, the LDS and RC-V groups had enormous levels of genetic diversity when compared with other microbial groups, and proliferation of sequences within each single clade was accompanied by significant ecological differentiation. Additionally, the freshwater Euryarchaeota counterparts unexpectedly showed high phylogenetic diversity, possibly promoted by their environmental adaptability and the heterogeneous nature of freshwater ecosystems. The temporal phylogenetic diversification pattern of these freshwater Euryarchaeota was concentrated both in early times and recently, similarly to other much less diverse but deeply sampled archaeal groups, further stressing that their genetic diversity is a function of environment plasticity. For the vast majority of living beings on Earth (i.e. the uncultured microorganisms), how they differ in the genetic or physiological traits used to exploit the environmental resources is largely unknown. Inferring population history from 16S rRNA gene-based molecular phylogenies under an ecological perspective may shed light on the intriguing relationships between lineage, environment, evolution and diversity in the microbial world.
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Merbt, S. N., et al. "Biofilm recovery in a wastewater treatment plant-influenced stream and spatial segregation of ammonia-oxidizing microbial populations." Limnology and Oceanography. 56.3 (2011): 1054–1064.
Résumé: We monitored the effects of wastewater treatment plant (WWTP) inputs on the recovery of stream biofilms after a large flood event that eroded most of the former biofilm communities. We monitored biomass recovery, chlorophyll a, nitrogen content, and stable isotope natural abundance ((15)N) over 8 weeks in light-and dark-exposed biofilms upstream and downstream from WWTP inputs, respectively, as well as the abundance of ammonia oxidizers by quantitative polymerase chain reaction. Biomass and chlorophyll a recovered quickly (< 2 weeks), and were significantly higher for light-than for dark-exposed biofilms. There was no consistent effect of WWTP inputs on these parameters, except for the biomass on dark-exposed biofilm that was higher at the WWTP-influenced sites. The influence of the WWTP inputs on stream-water ammonium concentration and its isotopic (15)N signature increased as the flood receded. Biofilm (15)N downstream of WWTP increased over time, tracking the increase in (15)N-ammonium from the WWTP waters. Bacterial and archaeal ammonia oxidizers were present within the biofilm assemblages from early stages of postflood recovery. However, spatial distribution of these two clades was clearly segregated among sites and between light-and dark-exposed biofilms, probably related to ammonium availability and the development of photoautotrophic organisms.
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2010 |
Auguet, J. C., A. Barberan, and E. O. Casamayor. "Global ecological patterns in uncultured Archaea." Isme J. 4.2 (2010): 182–190.
Résumé: We have applied a global analytical approach to uncultured Archaea that for the first time reveals well-defined community patterns along broad environmental gradients and habitat types. Phylogenetic patterns and the environmental factors governing the creation and maintenance of these patterns were analyzed for c. 2000 archaeal 16S rRNA gene sequences from 67 globally distributed studies. The sequences were dereplicated at 97% identity, grouped into seven habitat types, and analyzed with both Unifrac (to explore shared phylogenetic history) and multivariate regression tree (that considers the relative abundance of the lineages or taxa) approaches. Both phylogenetic and taxon-based approaches showed salinity and not temperature as one of the principal driving forces at the global scale. Hydrothermal vents and planktonic freshwater habitats emerged as the largest reservoirs of archaeal diversity and consequently are promising environments for the discovery of new archaeal lineages. Conversely, soils were more phylogenetically clustered and archaeal diversity was the result of a high number of closely related phylotypes rather than different lineages. Applying the ecological concept of 'indicator species', we detected up to 13 indicator archaeal lineages for the seven habitats prospected. Some of these lineages (that is, hypersaline MSBL1, marine sediment FCG1 and freshwater plSA1), for which ecological importance has remained unseen to date, deserve further attention as they represent potential key archaeal groups in terms of distribution and ecological processes. Hydrothermal vents held the highest number of indicator lineages, suggesting it would be the earliest habitat colonized by Archaea. Overall, our approach provided ecological support for the often arbitrary nomenclature within uncultured Archaea, as well as phylogeographical clues on key ecological and evolutionary aspects of archaeal biology.
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Lliros, M., et al. "Vertical distribution of ammonia-oxidizing crenarchaeota and methanogens in the epipelagic waters of Lake Kivu (Rwanda-Democratic Republic of the Congo)." Appl Environ Microbiol. 76.20 (2010): 6853–6863.
Résumé: Four stratified basins in Lake Kivu (Rwanda-Democratic Republic of the Congo) were sampled in March 2007 to investigate the abundance, distribution, and potential biogeochemical role of planktonic archaea. We used fluorescence in situ hybridization with catalyzed-reported deposition microscopic counts (CARD-FISH), denaturing gradient gel electrophoresis (DGGE) fingerprinting, and quantitative PCR (qPCR) of signature genes for ammonia-oxidizing archaea (16S rRNA for marine Crenarchaeota group 1.1a [MCG1] and ammonia monooxygenase subunit A [amoA]). Abundance of archaea ranged from 1 to 4.5% of total DAPI (4',6-diamidino-2-phenylindole) counts with maximal concentrations at the oxic-anoxic transition zone ( approximately 50-m depth). Phylogenetic analysis of the archaeal planktonic community revealed a higher level of richness of crenarchaeal 16S rRNA gene sequences (21 of the 28 operational taxonomic units [OTUs] identified [75%]) over euryarchaeotal ones (7 OTUs). Sequences affiliated with the kingdom Euryarchaeota were mainly recovered from the anoxic water compartment and mostly grouped into methanogenic lineages (Methanosarcinales and Methanocellales). In turn, crenarchaeal phylotypes were recovered throughout the sampled epipelagic waters (0- to 100-m depth), with clear phylogenetic segregation along the transition from oxic to anoxic water masses. Thus, whereas in the anoxic hypolimnion crenarchaeotal OTUs were mainly assigned to the miscellaneous crenarchaeotic group, the OTUs from the oxic-anoxic transition and above belonged to Crenarchaeota groups 1.1a and 1.1b, two lineages containing most of the ammonia-oxidizing representatives known so far. The concomitant vertical distribution of both nitrite and nitrate maxima and the copy numbers of both MCG1 16S rRNA and amoA genes suggest the potential implication of Crenarchaeota in nitrification processes occurring in the epilimnetic waters of the lake.
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2009 |
Auguet, J. C., et al. "Potential effect of freshwater virus on the structure and activity of bacterial communities in the Marennes-Oleron Bay (France)." Microb Ecol. 57.2 (2009): 295–306.
Résumé: Batch culture experiments using viral enrichment were conducted to test the response of a coastal bacterial community to autochthonous (i.e., co-existing) or allochthonous riverine viruses. The effects of viral infections on bacterial dynamics and activity were assessed by epifluorescence microscopy and thymidine incorporation, respectively, whereas the effect of viral infection on bacterial community composition was examined by polymerase chain reaction-single strand conformation polymorphism 16S ribosomal RNA fingerprinting. The percentages of high nucleic acid-containing cells, evaluated by flow cytometry, were significantly correlated (r2=0.91, n=12, p<0.0001) to bacterial production, making this value a good predictor of active cell dynamics along the study. While confinement and temperature were the two principal experimental factors affecting bacterial community composition and dynamics, respectively, additions of freshwater viruses had significant effects on coastal bacterial communities. Thus, foreign viruses significantly reduced net bacterial population increase as compared to the enrichment treated with inactivated virus. Moreover, freshwater viruses recurrently and specifically affected bacterial community composition, as compared to addition of autochthonous viruses. In most cases, the combined treatment viruses and freshwater dissolved organic matter helped to maintain or even enhance species richness in coastal bacterial communities in agreement to the 'killing the winner' hypothesis. Thus, riverine virus input could potentially influence bacterial community composition of the coastal bay albeit with modest modification of bulk bacterial growth.
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2008 |
Auguet, J. C., and E. O. Casamayor. "A hotspot for cold crenarchaeota in the neuston of high mountain lakes." Environ Microbiol. 10.4 (2008): 1080–1086.
Résumé: We have surveyed the first 1 m of 10 oligotrophic high mountain lakes in the Central Pyrenees (Spain) for both abundance and predominant phylotypes richness of the archaeaplankton assemblage, using CARD-FISH and 16S rRNA gene sequencing respectively. Archaea inhabiting the air-water surface microlayer (neuston) ranged between 3% and 37% of total 4,6-diamidino-2-phenylindole (DAPI) counts and were mainly Crenarchaeota of a new freshwater cluster distantly related to the Marine Group 1.1a. Conversely, most of the Archaea from the underlying waters (the remaining first 1 m integrated) were mainly Euryarchaeota of three distantly related branches ranging between 0.4% and 27% of total DAPI counts. Therefore, a consistent qualitative and quantitative spatial segregation was observed for the two main archaeal phyla between neuston and underlying waters at a regional scale. We also observed a consistent pattern along the lakes surveyed between lake area, lake depth and water residence time, and the archaeal enrichment in the neuston: the larger the lake the higher the proportion of archaea in the neuston as compared with abundances from the underlying waters (n = 10 lakes; R(2) > 0.80; P < 0.001, in all three cases). This is the first report identifying a widespread non-thermophilic habitat where freshwater planktonic Crenarchaeota can be found naturally enriched. High mountain lakes offer great research opportunities to explore the ecology of one of the most enigmatic and far from being understood group of prokaryotes.
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Auguet, J. C., et al. "Fingerprinting the genetic diversity of the biotin carboxylase gene (accC) in aquatic ecosystems as a potential marker for studies of carbon dioxide assimilation in the dark." Environ Microbiol. 10.10 (2008): 2527–2536.
Résumé: We designed and tested a set of specific primers for specific PCR amplification of the biotin carboxylase subunit gene (accC) of the Acetyl CoA carboxylase (ACCase) enzyme. The primer set yielded a PCR product of c. 460 bp that was suitable for denaturing gradient gel electrophoresis (DGGE) fingerprinting followed by direct sequencing of excised DGGE bands and sequence analysis. Optimization of PCR conditions for selective amplification was carried out with pure cultures of different bacteria and archaea, and laboratory enrichments. Next, fingerprinting comparisons were done in several aerobic and anaerobic freshwater planktonic samples. The DGGE fingerprints showed between 2 and 19 bands in the different samples, and the primer set provided specific amplification in both pure cultures and natural samples. Most of the samples had sequences grouped with bacterial accC, hypothetically related to the anaplerotic fixation of inorganic carbon. Some other samples, however, yielded accC gene sequences that clustered with Crenarchaeota and were related to the 3-hydroxypropionate/4-hydroxybutyrate cycle of autotrophic crenarchaeota. Such samples came from oligotrophic high mountain lakes and the hypolimnia of a sulfide-rich lake, where crenarchaeotal populations had been previously reported by 16S rRNA surveys. This study provided a fast tool to look for presence of accC genes in natural environments as potential marker for studies of carbon dioxide assimilation in the dark. After further refinement for better specificity against archaea, the new and novel primers could be very helpful to establish a target for crenarchaeota with implications for our understanding of archaeal carbon biogeochemistry.
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2006 |
Auguet, J. C., H. Montanie, and P. Lebaron. "Structure of virioplankton in the Charente Estuary (France): transmission electron microscopy versus pulsed field gel electrophoresis." Microb Ecol. 51.2 (2006): 197–208.
Résumé: Changes in the composition of viral communities were investigated along a salinity gradient and at different times by means of transmission electron microscopy (TEM) and pulsed field gel electrophoresis (PFGE). Samples were collected in fresh (Charente River), estuarine (Charente Estuary), and coastal (Pertuis d'Antioche, French Atlantic coast) waters. Both methods revealed similar patterns in viral community structure with a dominance of small viral particles (capsid and genome size). Viruses with a head size below 65 nm made up 71 +/- 5% of total virus-like particles, and virus-like genomes (VLG) below 100 kb accounted for 89 +/- 9% of total VLG. Despite this apparent stability of virioplankton composition over spatial scale (salinity gradient), the occurrence of large viruses (capsid and genome size) in estuarine and seawater samples indicated the presence of viral populations specific to a geographical location. Temporal changes in the structure (capsid and genome size) of viral communities were more pronounced than those reported at the spatial scale. From January to May 2003, seasonal changes in viral abundance and bacterial production occurred concomitantly with an increase in viral genomic diversity (richness), suggesting that virioplankton composition was strongly linked to changes in microbial activity and/or in the structure of the host communities. Although PFGE and TEM yielded complementary results in the description of virioplankton structures, it seems that the use of PFGE alone should be enough for the monitoring of community changes.
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Degre, D., et al. "Comparative analysis of the food webs of two intertidal mudflats during two seasons using inverse modelling: Aiguillon Cove and Brouage Mudflat, France." Estuarine Coastal and Shelf Science. 69.1-2 (2006): 107–124.
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2005 |
Auguet, J. C., et al. "Dynamic of virioplankton abundance and its environmental control in the Charente estuary (France)." Microb Ecol. 50.3 (2005): 337–349.
Résumé: The Charente River provides nutrient- and virus-rich freshwater input to the Marennes Oleron Basin, the largest oyster-producing region in Europe. To evaluate virioplankton distribution in the Charente Estuary and identify which environmental variables control dynamic of virioplankton abundance, five stations defined by a salinity gradient (0-0.5, 0.6-5, 13-17, 20-24, and higher than 30 PSU) were surveyed over a year. Viral abundance was related to bacterioplankton abundance and activities, photosynthetic pigments, nutrient concentration, and physical parameters (temperature and salinity). On a spatial scale, virus displayed a decreasing pattern seaward with abundance ranging over the sampling period from 1.4x10(7) to 20.8x10(7) viruses mL-1 making virioplankton the most abundant component of planktonic microorganisms in the Charente Estuary. A good correlation was found between viral and bacterial abundance (rs=0.85). Furthermore, bacterial abundance was the most important predictor of viral abundance explaining alone between 66% (winter) and 76% (summer) of viral variability. However, no relation existed between viral abundance and chlorophyll a. Temporal variations in viral distributions were mainly controlled by temperature through the control of bacterial dynamics. Spatial variations of viral abundance were influenced by hydrodynamic conditions especially during the winter season where virioplankton distribution was entirely driven by mixing processes.
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Jean-Christophe Auguet
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