Diversity of archaea and niche preferences among putative ammonia-oxidizing Nitrososphaeria dominating across European arable soils

Archaeal communities in arable soils are dominated by Nitrososphaeria, a class within Thaumarchaeota comprising all known ammonia-oxidizing archaea (AOA). AOA are key players in the nitrogen cycle and defining their niche specialization can help predicting effects of environmental change on these communities. However, hierarchical effects of environmental filters on AOA and the delineation of niche preferences of nitrososphaerial lineages remain poorly understood. We used phylogenetic information at fine scale and machine learning approaches to identify climatic, edaphic and geomorphological drivers of Nitrososphaeria and other archaea along a 3000 km European gradient. Only limited insights into the ecology of the low-abundant archaeal classes could be inferred, but our analyses underlined the multifactorial nature of niche differentiation within Nitrososphaeria. Mean annual temperature, C:N ratio and pH were the best predictors of their diversity, evenness and distribution. Thresholds in the predictions could be defined for C:N ratio and cation exchange capacity. Furthermore, multiple, independent and recent specializations to soil pH were detected in the Nitrososphaeria phylogeny. The coexistence of widespread ecophysiological differences between closely related soil Nitrososphaeria highlights that their ecology is best studied at fine phylogenetic scale

Metagenome-based diversity analyses suggest a significant contribution of non-cyanobacterial lineages to carbonate precipitation in modern microbialites

Frontiers in Microbiology 6 (2015): 797 This Document is Protected by copyright and was first published by Frontiers. All rights reserved. It is reproduced with permissionCyanobacteria are thought to play a key role in carbonate formation due to their metabolic activity, but other organisms carrying out oxygenic photosynthesis (photosynthetic eukaryotes) or other metabolisms (e.g., anoxygenic photosynthesis, sulfate reduction), may also contribute to carbonate formation. To obtain more quantitative information than that provided by more classical PCR-dependent methods, we studied the microbial diversity of microbialites from the Alchichica crater lake (Mexico) by mining for 16S/18S rRNA genes in metagenomes obtained by direct sequencing of environmental DNA. We studied samples collected at the Western (AL-W) and Northern (AL-N) shores of the lake and, at the latter site, along a depth gradient (1, 5, 10, and 15 m depth). The associated microbial communities were mainly composed of bacteria, most of which seemed heterotrophic, whereas archaea were negligible. Eukaryotes composed a relatively minor fraction dominated by photosynthetic lineages, diatoms in AL-W, influenced by Si-rich seepage waters, and green algae in AL-N samples. Members of the Gammaproteobacteria and Alphaproteobacteria classes of Proteobacteria, Cyanobacteria, and Bacteroidetes were the most abundant bacterial taxa, followed by Planctomycetes, Deltaproteobacteria (Proteobacteria), Verrucomicrobia, Actinobacteria, Firmicutes, and Chloroflexi. Community composition varied among sites and with depth. Although cyanobacteria were the most important bacterial group contributing to the carbonate precipitation potential, photosynthetic eukaryotes, anoxygenic photosynthesizers and sulfate reducers were also very abundant. Cyanobacteria affiliated to Pleurocapsales largely increased with depth. Scanning electron microscopy (SEM) observations showed considerable areas of aragonite-encrusted Pleurocapsa-like cyanobacteria at microscale. Multivariate statistical analyses showed a strong positive correlation of Pleurocapsales and Chroococcales with aragonite formation at macroscale, and suggest a potential causal link. Despite the previous identification of intracellularly calcifying cyanobacteria in Alchichica microbialites, most carbonate precipitation seems extracellular in this systemWe are grateful to Eleonor Cortés for help and good company during the field trip and to Eberto Novelo for helpful discussions at the UNAM lab. This research was funded by the European Research Council Grants ProtistWorld (PI PL-G., Grant Agreement no. 322669) and CALCYAN (PI KB, Grant Agreement no. 307110) under the European Union’s Seventh Framework Program and the RTP Génomique environnementale of the CNRS (project MetaStrom, PI DM

Diversity of archaea and niche preferences among putative ammonia-oxidizing Nitrososphaeria dominating across European arable soils

Archaeal communities in arable soils are dominated by Nitrososphaeria, a class within Thaumarchaeota comprising all known ammonia-oxidizing archaea (AOA). AOA are key players in the nitrogen cycle and defining their niche specialization can help predicting effects of environmental change on these communities. However, hierarchical effects of environmental filters on AOA and the delineation of niche preferences of nitrososphaerial lineages remain poorly understood. We used phylogenetic information at fine scale and machine learning approaches to identify climatic, edaphic and geomorphological drivers of Nitrososphaeria and other archaea along a 3000 km European gradient. Only limited insights into the ecology of the low-abundant archaeal classes could be inferred, but our analyses underlined the multifactorial nature of niche differentiation within Nitrososphaeria. Mean annual temperature, C:N ratio and pH were the best predictors of their diversity, evenness and distribution. Thresholds in the predictions could be defined for C:N ratio and cation exchange capacity. Furthermore, multiple, independent and recent specializations to soil pH were detected in the Nitrososphaeria phylogeny. The coexistence of widespread ecophysiological differences between closely related soil Nitrososphaeria highlights that their ecology is best studied at fine phylogenetic scale.The Digging Deeper project was funded through the 2015–2016 BiodivERsA call, with national funding from the Swiss National Science Foundation (grant 31BD30-172466), the Deutsche Forschungsgemeinschaft (grant 317895346), the Swedish Research Council Formas (grant 2016-0194), the Spanish Ministerio de Economía y Competitividad (grant PCIN-2016-028) and the Agence Nationale de la Recherche (grant ANR-16-EBI3-0004-01). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Sequencing was performed by the SNP&SEQ Technology Platform in Uppsala. The facility is part of the National Genomics Infrastructure (NGI) Sweden and Science for Life Laboratory. The SNP&SEQ Platform is also supported by the Swedish Research Council and the Knut and Alice Wallenberg Foundation

The impact of agricultural management on soil aggregation and carbon storage is regulated by climatic thresholds across a 3000 km European gradient

Organic carbon and aggregate stability are key features of soil quality and are important to consider when evaluating the potential of agricultural soils as carbon sinks. However, we lack a comprehensive understanding of how soil organic carbon (SOC) and aggregate stability respond to agricultural management across wide environmental gradients. Here, we assessed the impact of climatic factors, soil properties and agricultural management (including land use, crop cover, crop diversity, organic fertilization, and management intensity) on SOC and the mean weight diameter of soil aggregates, commonly used as an indicator for soil aggregate stability, across a 3000 km European gradient. Soil aggregate stability (-56%) and SOC stocks (-35%) in the topsoil (20 cm) were lower in croplands compared with neighboring grassland sites (uncropped sites with perennial vegetation and little or no external inputs). Land use and aridity were strong drivers of soil aggregation explaining 33% and 20% of the variation, respectively. SOC stocks were best explained by calcium content (20% of explained variation) followed by aridity (15%) and mean annual temperature (10%). We also found a threshold-like pattern for SOC stocks and aggregate stability in response to aridity, with lower values at sites with higher aridity. The impact of crop management on aggregate stability and SOC stocks appeared to be regulated by these thresholds, with more pronounced positive effects of crop diversity and more severe negative effects of crop management intensity in nondryland compared with dryland regions. We link the higher sensitivity of SOC stocks and aggregate stability in nondryland regions to a higher climatic potential for aggregate-mediated SOC stabilization. The presented findings are relevant for improving predictions of management effects on soil structure and C storage and highlight the need for site-specific agri-environmental policies to improve soil quality and C sequestration

Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts

Phosphorus (P) acquisition is key for plant growth. Arbuscular mycorrhizal fungi (AMF) help plants acquire P from soil. Understanding which factors drive AMF-supported nutrient uptake is essential to develop more sustainable agroecosystems. Here we collected soils from 150 cereal fields and 60 non-cropped grassland sites across a 3,000 km trans-European gradient. In a greenhouse experiment, we tested the ability of AMF in these soils to forage for the radioisotope 33P from a hyphal compartment. AMF communities in grassland soils were much more efficient in acquiring 33P and transferred 64% more 33P to plants compared with AMF in cropland soils. Fungicide application best explained hyphal 33P transfer in cropland soils. The use of fungicides and subsequent decline in AMF richness in croplands reduced 33P uptake by 43%. Our results suggest that land-use intensity and fungicide use are major deterrents to the functioning and natural nutrient uptake capacity of AMF in agroecosystems.The Digging Deeper project was funded through the 2015-2016 BiodivERsA COFUND call for research proposals, with the national funders Swiss National Science Foundation (grant 31BD30-172466), Deutsche Forschungsgemeinschaft (317895346), Swedish Research Council Formas (contract 2016-0194), Ministerio de Economía y Competitividad (Digging_Deeper, Ref. PCIN-2016-028) and Agence Nationale de la Recherche (ANR, France; grant ANR-16-EBI3-0004-01)

Caractérisation phylogénétique et fonctionnelle de microbialites et de tapis microbiens

Microbial mats are phylogenetically and functionally diverse benthic microbial communities, which can be sometimes calcified (i.e. microbialites). Fossil microbial mats constitute the oldest traces of life on Earth and their modern representatives are thus used as analogues of those primordial ecosystems to gain insights into their functioning. I have studied the microbial communities (archaea, bacteria and eukaryotes) of several microbialites (lake Alchichica, Mexico) and microbial mats (in a small pond in the salar de Llamara, Chile). The main objectives of my PhD were to finely characterize their phylogenetic structure and to improve our understanding of the functioning of these complex ecosystems. To do so, I have applied a multi-disciplinary approach combining molecular approaches (metabarcoding, metagenomics) to environmental data (physico-chemical parameters of the water column or mineral composition of the microbialites).The results presented in this thesis allowed refining our model of microbialite formation in Lake Alchichica. We showed that, in addition to cyanobacterial photosynthesis, both eukaryotic and, particularly, anoxygenic photosyntheses were potentially important to promote carbonate precipitation. Llamara mat communities were characterised by the presence of numerous novel archaeal and bacterial lineages, some of which were identified for the first time in this work. Our analyses have also highlighted the diversity of organisms involved in both sulphur and nitrogen cycles in these mats and identified potential biotic interactions between poorly known prokaryotic lineages. Finally, we showed that the composition of the microbial communities associated to these microbialites and microbial mats was strongly influenced by environmental parameters. Overall, these results represent a substantial contribution to our understanding of the ecology of these systems as well as of the factors that influence their phylogenetic and functional structures.Les tapis microbiens sont des communautés benthiques, calcifiées (i.e. microbialites) ou non, diverses à la fois phylogénétiquement et métaboliquement. Les tapis microbiens fossiles constituent les plus anciennes traces de vie sur Terre et leurs représentants modernes peuvent donc être utilisés pour comprendre le fonctionnement de ces écosystèmes anciens. J'ai étudié les communautés microbiennes (archées, bactéries et eucaryotes) de plusieurs microbialites (lac Alchichica, Mexique) et tapis microbiens (dans une mare du salar de Llamara, Chili) afin de caractériser finement leur structure phylogénétique et d'améliorer notre compréhension de leur fonctionnement. J'ai pour cela utilisé une approche combinant des outils moléculaires (métabarcoding, métagénomique) à des données environnementales (paramètres physico-chimiques de la colonne d'eau ou composition minérale des microbialites). Mon travail de thèse a permis d'affiner le modèle de formation des microbialites d'Alchichica, en montrant notamment que, en plus de la photosynthèse oxygénique cyanobactérienne, le potentiel à précipiter des carbonates de la photosynthèse eucaryote et, surtout, de la photosynthèse anoxygénique est important. Les communautés des tapis de Llamara étaient quant à elles caractérisées par la présence de nombreuses lignées d'archées et de bactéries très divergentes, dont certaines ont été identifiées pour la première fois dans ce travail. Nos analyses ont aussi souligné la diversité des organismes impliqués dans les cycles du soufre et de l'azote au sein de ces systèmes et permis d'identifier de potentielles interactions biotiques entre des lignées procaryotes dont l'écologie est peu connue. Enfin, nous avons mis en évidence que les paramètres environnementaux influencent fortement la composition des communautés associées à ces microbialites et à ces tapis microbiens. L'ensemble de ces résultats permet de mieux comprendre le fonctionnement de ces systèmes ainsi que les facteurs qui influencent leur structure phylogénétique et fonctionnelle

Phylogenetic and functional characterization of microbialites and microbial mats

Les tapis microbiens sont des communautés benthiques, calcifiées (i.e. microbialites) ou non, diverses à la fois phylogénétiquement et métaboliquement. Les tapis microbiens fossiles constituent les plus anciennes traces de vie sur Terre et leurs représentants modernes peuvent donc être utilisés pour comprendre le fonctionnement de ces écosystèmes anciens. J'ai étudié les communautés microbiennes (archées, bactéries et eucaryotes) de plusieurs microbialites (lac Alchichica, Mexique) et tapis microbiens (dans une mare du salar de Llamara, Chili) afin de caractériser finement leur structure phylogénétique et d'améliorer notre compréhension de leur fonctionnement. J'ai pour cela utilisé une approche combinant des outils moléculaires (métabarcoding, métagénomique) à des données environnementales (paramètres physico-chimiques de la colonne d'eau ou composition minérale des microbialites). Mon travail de thèse a permis d'affiner le modèle de formation des microbialites d'Alchichica, en montrant notamment que, en plus de la photosynthèse oxygénique cyanobactérienne, le potentiel à précipiter des carbonates de la photosynthèse eucaryote et, surtout, de la photosynthèse anoxygénique est important. Les communautés des tapis de Llamara étaient quant à elles caractérisées par la présence de nombreuses lignées d'archées et de bactéries très divergentes, dont certaines ont été identifiées pour la première fois dans ce travail. Nos analyses ont aussi souligné la diversité des organismes impliqués dans les cycles du soufre et de l'azote au sein de ces systèmes et permis d'identifier de potentielles interactions biotiques entre des lignées procaryotes dont l'écologie est peu connue. Enfin, nous avons mis en évidence que les paramètres environnementaux influencent fortement la composition des communautés associées à ces microbialites et à ces tapis microbiens. L'ensemble de ces résultats permet de mieux comprendre le fonctionnement de ces systèmes ainsi que les facteurs qui influencent leur structure phylogénétique et fonctionnelle.Microbial mats are phylogenetically and functionally diverse benthic microbial communities, which can be sometimes calcified (i.e. microbialites). Fossil microbial mats constitute the oldest traces of life on Earth and their modern representatives are thus used as analogues of those primordial ecosystems to gain insights into their functioning. I have studied the microbial communities (archaea, bacteria and eukaryotes) of several microbialites (lake Alchichica, Mexico) and microbial mats (in a small pond in the salar de Llamara, Chile). The main objectives of my PhD were to finely characterize their phylogenetic structure and to improve our understanding of the functioning of these complex ecosystems. To do so, I have applied a multi-disciplinary approach combining molecular approaches (metabarcoding, metagenomics) to environmental data (physico-chemical parameters of the water column or mineral composition of the microbialites).The results presented in this thesis allowed refining our model of microbialite formation in Lake Alchichica. We showed that, in addition to cyanobacterial photosynthesis, both eukaryotic and, particularly, anoxygenic photosyntheses were potentially important to promote carbonate precipitation. Llamara mat communities were characterised by the presence of numerous novel archaeal and bacterial lineages, some of which were identified for the first time in this work. Our analyses have also highlighted the diversity of organisms involved in both sulphur and nitrogen cycles in these mats and identified potential biotic interactions between poorly known prokaryotic lineages. Finally, we showed that the composition of the microbial communities associated to these microbialites and microbial mats was strongly influenced by environmental parameters. Overall, these results represent a substantial contribution to our understanding of the ecology of these systems as well as of the factors that influence their phylogenetic and functional structures

Loss in soil microbial diversity constrains microbiome selection and alters the abundance of N-cycling guilds in barley rhizosphere

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Genomes of Abundant and Widespread Viruses from the Deep Ocean

The deep sea is a massive, largely oligotrophic ecosystem, stretched over nearly 65% of the planet’s surface. Deep-sea planktonic communities are almost completely dependent upon organic carbon sinking from the productive surface, forming a vital component of global biogeochemical cycles. However, despite their importance, viruses from the deep ocean remain largely unknown. Here, we describe the first complete genomes of deep-sea viruses assembled from metagenomic fosmid libraries. “Candidatus Pelagibacter” (SAR11) phage HTVC010P and Puniceispirillum phage HMO-2011 are considered the most abundant cultured marine viruses known to date. Remarkably, some of the viruses described here recruited as many reads from deep waters as these viruses do in the photic zone, and, considering the gigantic scale of the bathypelagic habitat, these genomes provide information about what could be some of the most abundant viruses in the world at large. Their role in the viral shunt in the global ocean could be very significant. Despite the challenges encountered in inferring the identity of their hosts, we identified one virus predicted to infect members of the globally distributed SAR11 cluster. We also identified a number of putative proviruses from diverse taxa, including deltaproteobacteria, bacteroidetes, SAR11, and gammaproteobacteria. Moreover, our findings also indicate that lysogeny is the preferred mode of existence for deep-sea viruses inhabiting an energy-limited environment, in sharp contrast to the predominantly lytic lifestyle of their photic-zone counterparts. Some of the viruses show a widespread distribution, supporting the tenet “everything is everywhere” for the deep-ocean viromeWork in FR-V laboratory was supported by projects MEDIMAX BFPU2013-48007-P from the Spanish Ministerio de Economía y Competitividad,MaCuMBA Project 311975 of the European Commission FP7PROMETEO II/2014/012 project AQUAMET from the Generalitat ValencianaCMM was partially supported by an EMBO short-term fellowshipRG was partially supported by the Grant Agency of the Czech Science Foundation under the research grant 13-00243SWork in PLG’s lab was funded by the French National Agency for Research (ANR-08-GENM-024-002)The European Research Council (ERC) under the European Commission 7th Framework Program (ERC Grant Agreement 322669)

Functional shifts in microbial mats recapitulate early Earth metabolic transitions

International audiencePhototrophic microbial mats dominated terrestrial ecosystems for billions of years, largely causing, through cyanobacterial oxygenic photosynthesis, but also undergoing, the great oxidation event (GOE) at ca. 2.5 Ga. Taking a space-for-time approach based on the universality of core metabolic pathways expressed at ecosystem level, we studied gene content and co-occurrence networks in high-diversity metagenomes from spatially close microbial mats along a steep redox gradient. The observed functional shifts suggest that anoxygenic photosynthesis was present but not predominant under early Precambrian conditions, being accompanied by other autotrophic processes. Our data also suggest that, in contrast to general assumptions, anoxygenic photosynthesis largely expanded in parallel to the subsequent evolution of oxygenic photosynthesis and aerobic respiration. Finally, our observations might represent space-for-time evidence that the Wood-Ljungdahl carbon fixation pathway dominated phototrophic mats in early ecosystems, whereas the Calvin cycle likely evolved from pre-existing variants before becoming the dominant contemporary form of carbon fixation