Showing papers by "Christa Schleper published in 2018"

Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes.

Abstract: Ammonia-oxidising archaea (AOA) are ubiquitous and abundant in nature and play a major role in nitrogen cycling. AOA have been studied intensively based on the amoA gene (encoding ammonia monooxygenase subunit A), making it the most sequenced functional marker gene. Here, based on extensive phylogenetic and meta-data analyses of 33,378 curated archaeal amoA sequences, we define a highly resolved taxonomy and uncover global environmental patterns that challenge many earlier generalisations. Particularly, we show: (i) the global frequency of AOA is extremely uneven, with few clades dominating AOA diversity in most ecosystems; (ii) characterised AOA do not represent most predominant clades in nature, including soils and oceans; (iii) the functional role of the most prevalent environmental AOA clade remains unclear; and (iv) AOA harbour molecular signatures that possibly reflect phenotypic traits. Our work synthesises information from a decade of research and provides the first integrative framework to study AOA in a global context.

Biological methane production under putative Enceladus-like conditions.

Abstract: The detection of silica-rich dust particles, as an indication for ongoing hydrothermal activity, and the presence of water and organic molecules in the plume of Enceladus, have made Saturn’s icy moon a hot spot in the search for potential extraterrestrial life. Methanogenic archaea are among the organisms that could potentially thrive under the predicted conditions on Enceladus, considering that both molecular hydrogen (H2) and methane (CH4) have been detected in the plume. Here we show that a methanogenic archaeon, Methanothermococcus okinawensis, can produce CH4 under physicochemical conditions extrapolated for Enceladus. Up to 72% carbon dioxide to CH4 conversion is reached at 50 bar in the presence of potential inhibitors. Furthermore, kinetic and thermodynamic computations of low-temperature serpentinization indicate that there may be sufficient H2 gas production to serve as a substrate for CH4 production on Enceladus. We conclude that some of the CH4 detected in the plume of Enceladus might, in principle, be produced by methanogens. Many methanogenic archaea use H2 and CO2 to produce methane. Here, Taubner et al. show that Methanothermococcus okinawensis produces methane under conditions extrapolated for Saturn’s icy moon, Enceladus, and estimate that serpentinization may produce sufficient H2 for biological methane production.

A plant-microbe interaction framework explaining nutrient effects on primary production.

Abstract: In most terrestrial ecosystems, plant growth is limited by nitrogen and phosphorus. Adding either nutrient to soil usually affects primary production, but their effects can be positive or negative. Here we provide a general stoichiometric framework for interpreting these contrasting effects. First, we identify nitrogen and phosphorus limitations on plants and soil microorganisms using their respective nitrogen to phosphorus critical ratios. Second, we use these ratios to show how soil microorganisms mediate the response of primary production to limiting and non-limiting nutrient addition along a wide gradient of soil nutrient availability. Using a meta-analysis of 51 factorial nitrogen-phosphorus fertilization experiments conducted across multiple ecosystems, we demonstrate that the response of primary production to nitrogen and phosphorus additions is accurately predicted by our stoichiometric framework. The only pattern that could not be predicted by our original framework suggests that nitrogen has not only a structural function in growing organisms, but also a key role in promoting plant and microbial nutrient acquisition. We conclude that this stoichiometric framework offers the most parsimonious way to interpret contrasting and, until now, unresolved responses of primary production to nutrient addition in terrestrial ecosystems.

Candidatus Nitrosocaldus cavascurensis, an Ammonia Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile Genome.

Abstract: Ammonia oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread in moderate environments but their occurrence and activity has also been demonstrated in hot springs. Here we present the first enrichment of a thermophilic representative with a sequenced genome, which facilitates the search for adaptive strategies and for traits that shape the evolution of Thaumarchaeota. Candidatus Nitrosocaldus cavascurensis has been enriched from a hot spring in Ischia, Italy. It grows optimally at 68°C under chemolithoautotrophic conditions on ammonia or urea converting ammonia stoichiometrically into nitrite with a generation time of approximately 23 h. Phylogenetic analyses based on ribosomal proteins place the organism as a sister group to all known mesophilic AOA. The 1.58 Mb genome of Ca. N. cavascurensis harbors an amoAXCB gene cluster encoding ammonia monooxygenase and genes for a 3-hydroxypropionate/4-hydroxybutyrate pathway for autotrophic carbon fixation, but also genes that indicate potential alternative energy metabolisms. Although a bona fide gene for nitrite reductase is missing, the organism is sensitive to NO-scavenging, underlining the potential importance of this compound for AOA metabolism. Ca. N. cavascurensis is distinct from all other AOA in its gene repertoire for replication, cell division and repair. Its genome has an impressive array of mobile genetic elements and other recently acquired gene sets, including conjugative systems, a provirus, transposons and cell appendages. Some of these elements indicate recent exchange with the environment, whereas others seem to have been domesticated and might convey crucial metabolic traits.

Holistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation.

Abstract: Ruminant livestock is a major source of the potent greenhouse gas methane. The complex rumen microbiome, consisting of bacteria, archaea, and microbial eukaryotes, facilitates anaerobic plant biomass degradation in the cow rumen, leading to methane emissions. Using an integrated approach combining multidomain quantitative metatranscriptomics with gas and volatile fatty acid (VFA) profiling, we aimed at obtaining the most comprehensive picture of the active rumen microbiome during feed degradation to date. Bacterial, archaeal, and eukaryotic biomass, but also methane emissions and VFA concentrations, increased drastically within an hour after feed intake. mRNA profiling revealed a dynamic response of carbohydrate-active enzyme transcripts, transcripts involved in VFA production and methanogenesis. While the relative abundances of functional transcripts did not mirror observed processes, such as methane emissions, transformation to mRNA abundance per gram of rumen fluid echoed ruminant processes. The microbiome composition was highly individual, with, e.g., ciliate, Neocallimastigaceae, Prevotellaceae, Succinivibrionaceae, and Fibrobacteraceae abundances differing between cows. Microbiome individuality was accompanied by inter- and intradomain multifunctional redundancy among microbiome members during feed degradation. This likely enabled the robust performance of the anaerobic degradation process in each rumen. Neocallimastigaceae and ciliates contributed an unexpectedly large share of transcripts for cellulose- and hemicellulose-degrading enzymes, respectively. Methyl-reducing but not CO2-reducing methanogens were positively correlated with methane emissions. While Methanomassiliicoccales switched from methanol to methylamines as electron acceptors, Methanosphaera became the dominating methanol-reducing methanogen. This study for the first time linked rumen meta-omics with processes and enabled holistic insights into the contribution of all microbiome members to feed degradation. IMPORTANCE Ruminant animals, such as cows, live in a tight symbiotic association with microorganisms, allowing them to feed on otherwise indigestible plant biomass as food sources. Methane is produced as an end product of the anaerobic feed degradation in ruminants and is emitted to the atmosphere, making ruminant animals among the major anthropogenic sources of the potent greenhouse gas methane. Using newly developed quantitative metatranscriptomics for holistic microbiome analysis, we here identified bacterial, archaeal, and eukaryotic key players and the short-term dynamics of the rumen microbiome during anaerobic plant biomass degradation and subsequent methane emissions. These novel insights might pave the way for novel ecologically and economically sustainable methane mitigation strategies, much needed in times of global climate change.

Significance of dark CO2 fixation in arctic soils

Abstract: The occurrence of dark fixation of CO2 by heterotrophic microorganisms in soil is generally accepted, but its importance for microbial metabolism and soil organic carbon (C) sequestration is unknown, especially under C-limiting conditions. To fill this knowledge gap, we measured dark 13CO2 incorporation into soil organic matter and conducted a 13C-labelling experiment to follow the 13C incorporation into phospholipid fatty acids as microbial biomass markers across soil profiles of four tundra ecosystems in the northern circumpolar region, where net primary productivity and thus soil C inputs are low. We further determined the abundance of various carboxylase genes and identified their microbial origin with metagenomics. The microbial capacity for heterotrophic CO2 fixation was determined by measuring the abundance of carboxylase genes and the incorporation of 13C into soil C following the augmentation of bioavailable C sources. We demonstrate that dark CO2 fixation occurred ubiquitously in arctic tundra soils, with increasing importance in deeper soil horizons, presumably due to increasing C limitation with soil depth. Dark CO2 fixation accounted on average for 0.4, 1.0, 1.1, and 16% of net respiration in the organic, cryoturbated organic, mineral and permafrost horizons, respectively. Genes encoding anaplerotic enzymes of heterotrophic microorganisms comprised the majority of identified carboxylase genes. The genetic potential for dark CO2 fixation was spread over a broad taxonomic range. The results suggest important regulatory function of CO2 fixation in C limited conditions. The measurements were corroborated by modeling the long-term impact of dark CO2 fixation on soil organic matter. Our results suggest that increasing relative CO2 fixation rates in deeper soil horizons play an important role for soil internal C cycling and can, at least in part, explain the isotopic enrichment with soil depth.

Microbial diversity of a closed salt lagoon in the Puertecitos area, Upper Gulf of California

Abstract: espanolVeinte kilometros hacia el sur de Puertecitos, en la peninsula de Baja California, Mexico, se localiza una laguna con un area super-ficial de ~265,000 m2 que esta cubierta por una costra salina y aislada de la parte alta del golfo de California por una berma de 50 m de ancho. Laberma se eleva 2 m sobre el nivel medio del mar y se extiende por 530 m a lo largo del frente marino de la laguna evitando el reabastecimiento normal con agua de mar excepto, posiblemente, por filtracion. En otro lado de la laguna, un volcan extinto del Plioceno, el volcan Prieto, marca un limite igualmente abrupto delineado por los flujos de basalto. La geografia fisica bien delimitada de la laguna representa un entorno de alta salinidad en condiciones de extrema aridez, inundada solo durante eventos poco frecuentes asociados con tormentas subtropicales. La laguna Volcan Prieto (asi llamada aqui) se formo a traves de distintas etapas en el desarrollo de la geomorfologia descrita en este estudio. Se recupero un conjunto duplicado de nucleos de la laguna (17 cm de longitud) y se tomaron muestras para determinar asociaciones biologicas que registran la colonizacion de alta diversidad y la estratificacion de tapetes microbianos dominados por bacterias. Con base en la secuenciacion de genes de ARN ribosomico de subunidades pequenas de diferentes horizontes, se identificaron al menos 25 filos bacterianos nombrados principales y 8 filos de arqueas nombrados principales, asi como varios taxones candidatos sin nombre de grupos diversos. Los analisis de biomarcadores lipidicos de los mismos horizontes revelaron que las cianobacterias contribuyeron significativamente a la produccion de biomasa unicamente a una profundidad somera, mientras que los lipidos de las bacterias fototrofas anoxigenicas persistieron a una profundidad de 15 cm, aunque con contenidos decrecientes. Los patrones de lipidos tambien mostraron que las bacterias reductoras de sulfato se volvieron mas abundantes con la profundidad, mientras que los contenidos de los lipidos de las arqueas aumentaron entre 1 y 5 cm de profundidad y permanecieron relativamente constantes a mayor profundidad. Las lagunas cerradas en el golfo de California estan ampliamente distribuidas a lo largo de la peninsula de Baja California, pero los estudios taxonomicos detallados sobre las diversas comunidades microbianas que colonizaron estos habitats extremos apenas han comenzado a dilucidar los complejos patrones de colonizacion. EnglishLocated 20 km south of Puertecitos on the Baja California Peninsula, Mexico, is a salt-crusted lagoon with a surface area of approximately 265,000 m2 that is isolated from the adjacent Upper Gulf of California by a 50-m wide berm. The berm rises 2 m above mean sea level extending for 530 m across the lagoon’s seaward front to bar replenishment by normal seawater except possibly by seepage. On another side of the lagoon an extinct Pliocene volcano, Volcan Prieto, marks an equally abrupt boundary delineated by basalt flows. The lagoon’s well-constrained physical geography represents a high-salinity environment under conditions of extreme aridity, flooded only during rare events associated with subtropical storms. The Volcan Prieto Lagoon (so named herein) formed through distinct stages in developmental geo-morphology outlined in this study. A duplicate set of sediment cores (17 cm in length) were retrieved from the lagoon and sampled for biological associations that record high-diversity colonization and stratification of microbial mats dominated by bacteria. Small subunit ribosomal RNA gene sequencing of different horizons revealed at least 25 major named bacterial phyla and 8 major named archaeal phyla as well as several unnamed candidate taxa from miscellaneous groups. Lipid biomarker analyses of the same horizons revealed that cyanobacteria contributed significantly to biomass production only at shallow depth, whereas the lipids of anoxygenic phototrophic bacteria persisted to a depth of 15 cm, although with decreasing contents. The lipid patterns also showed that sulfate-reducing bacteria became more abundant with depth, whereas the contents of archaeal lipids increased from 1 to 5 cm depth but remained relatively constant below. Closed lagoons on the Gulf of California are widely distributed over the length of the Baja California Peninsula, but detailed taxonomic studies regarding the diverse microbial communities that colonized these extreme habitats have only begun to shed light on complex colonization patterns.

Inter- and intra-domain functional redundancy in the rumen microbiome during plant biomass degradation

Abstract: Background: Ruminant livestock is a major source of the potent greenhouse gas methane (CH4), produced by the complex rumen microbiome. Using an integrated approach, combining quantitative metatranscriptomics with gas- and volatile fatty acid (VFA) profiling, we gained fundamental insights into temporal dynamics of the cow rumen microbiome during feed degradation. Results: The microbiome composition was highly individual and remarkably stable within each cow, despite similar gas emission and VFA profiles between cows. Gene expression profiles revealed a fast microbial growth response to feeding, reflected by drastic increases in microbial biomass, CH4 emissions and VFA concentrations. Microbiome individuality was accompanied by high inter- and intra-domain functional redundancy among pro- and eukaryotic microbiome members in the key steps of anaerobic feed degradation. Methyl-reducing but not CO2-reducing methanogens were correlated with increased CH4 emissions during plant biomass degradation. Conclusions: The major response of the rumen microbiome to feed intake was a general growth of the whole community. The high functional redundancy of the cow-individual microbiomes was possibly linked to the robust performance of the anaerobic degradation process. Furthermore, the strong response of methylotrophic methanogens is suggesting that they might play a more important role in ruminant CH4 emissions than previously assumed, making them potential targets for CH4 mitigation strategies.

Simulating putative Enceladus-like conditions: The possibility of biological methane production on Saturn's icy moon

Abstract: In this study (Taubner et al.2018), three different methanogenic archaea (Methanothermococcus okinawensis, Methanothermobacter marburgensis, and Methanococcus villosus) were tested for metabolic activities and growth under putative Enceladus-like conditions, including high pressure experiments and tests on the tolerance towards potential gaseous and liquid inhibitors detected in Enceladus’ plume. In particular, M. okinawensis, an isolate from a deep marine trench (Takai et al.2002), showed tolerance towards all of the added inhibitors and maintained methanogenesis even in the range of 10 to 50 bar. Further, we were able to show that H2 production based on serpentinization may be sufficient to fuel such methanogenic life on Enceladus. The experiments revealed that methanogenesis could, in principle, be feasible under Enceladus-like conditions.