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Kuesel, K.

Publications and source records attributed to Kuesel, K..

14 recordsLinked to original sources

Phagocytosis without mitochondria is a lineage trait of planctomycetal bacteria of prey

Phagocytosis is considered energetically out of reach for prokaryotes. Mitochondria-first models of eukaryogenesis therefore suggest a non-phagocytic archaeal host. Yet two recently described planctomycetes lack mitochondria and engulf entire bacteria. Whether this mode of predation is an oddity of two isolates or the hallmark of a bacterial lineage remained unresolved. Here, we report eight additional predatory Planctomycetota from three aquatic habitats. The ten cultured strains now span two classes of the phylum Planctomycetota,"Candidatus Uabimicrobiia" and one newly proposed class. Using engineered fluorescent prey, we show that nine strains internalize prey into fully sealed compartments whereas one digests its prey externally, a non-engulfing predator for comparison. The strains additionally divide by two distinct modes, however, not correlating with their feeding behavior. Sequence- and structure-based searches detect no eukaryotic phagocytosis protein conserved across the engulfing strains. The actin homologue previously proposed to mediate uptake occurs only in three engulfing strains. Routine engulfment by aerobic bacteria without mitochondria thus unsettles a premise of mitochondria-first models and reopens the question of which cell plans could have hosted the mitochondrial endosymbiont.

microbiology↗

Fungal community composition links rhizosphere microbiome organization to plant phenotype in response to moderate warming

BackgroundGlobal warming increasingly challenges plant performance and ecosystem function, and plant responses to elevated temperature are shaped not only by intrinsic plasticity, but also by interactions with rhizosphere microbial communities. However, it remains unclear how warming-induced microbiome reorganization relates to plant performance, whether microbiome community composition predicts plant phenotypic responses to elevated temperature better than simple host-microbiome origin matching, and which bacterial or fungal community features contribute most strongly to this prediction. ResultsWe implemented a full factorial design manipulating plant genotype (P), microbial inoculum (M), and temperature (T) using natural Arabidopsis thaliana ecotypes and their corresponding rhizosphere microbiomes from contrasting climatic regions. By integrating high-throughput plant phenotyping, microbial community profiling, microbiome-phenotype coupling analyses, and predictive modeling, we found that elevated temperature induced a coherent thermomorphogenic shift in plant architecture, while plant phenotypic variation remained determined primarily by genotype over the 14-day vegetative growth period covered in this study. Overall, cold-origin genotypes showed larger temperature-induced trait shifts than warm-origin genotypes. Rhizosphere microbial communities were structured predominantly by inoculum origin, but were also affected by warming. Evidence for a increased thermomorphogenic growth when genotypes were combined with inoculum from their home site was limited. Instead, microbiome-phenotype associations were better captured by community composition than by matching status, with fungal community variation showing stronger and more consistent associations with plant phenotype than bacterial variation and providing more robust predictions of plant phenotypes across models. ConclusionsWarming reorganized plant-rhizosphere systems within persistent host- and inoculum-associated baselines. Plant phenotypic variation during vegetative development under elevated temperature was linked more closely to microbiome composition, especially in fungi, than to simple host-microbiome matching of origins. These findings provide a framework for identifying microbiome features associated with plant performance under climate warming.

plant biology↗

Traversing the canopy: phenology-driven changes and within-canopy transport shape the phyllosphere microbiome in a temperate floodplain hardwood forest

O_LIPhyllosphere microbiomes are subject to microbial import from various sources and undergo substantial changes during phenological changes of plants. However, these processes are still poorly understood for forest canopies. We propose that phenology-driven changes in host properties, and rainwater-mediated, within-canopy transport shape the phyllosphere microbiome in temperate forests. Leaves and throughfall samples were collected from oak, ash and linden trees at top, mid, and bottom canopy positions at the Leipzig canopy crane facility (Germany) at time points representing early, mid and late phenological stages. Bacterial community composition was assessed by 16S rRNA gene amplicon sequencing. C_LIO_LIPhenological stages explained 19% of phyllosphere bacterial community variation, followed by tree species identity (12%) and canopy position (2%). Later phenological stages exhibited more homogeneous and functionally redundant phyllosphere communities along with a strong decline of plant pathogens and increasing potential for microbially mediated biocontrol mechanisms. Throughfall transported up to 1011 bacterial cells per litre with maximum bacterial fluxes at the canopy top. C_LIO_LIOur findings demonstrate that in temperate forests, phenology-driven effects on the phyllosphere microbiome are far more important than tree species specific effects. Extent and selectivity of throughfall-mediated mobilization may play a crucial role for the spatial heterogeneity of microbial communities in tree crowns. C_LI

ecology↗

Source-independent enrichment of light lanthanides: microbial mobilization, selective uptake, and intracellular storage

Poorly soluble lanthanide minerals pose challenges for both a sustainable extraction of lanthanides as key resources for decarbonization and lanthanide-dependent microbial metabolism. Microbial use of lanthanides is widespread, yet bacterias preference for light lanthanides requires differentiation mechanisms that enable downstream utilization. Whether lanthanide discrimination occurs during access, mobilization, uptake, or intracellular processing is mostly unknown and likely controlled by habitat and bioavailability. We studied microbial lanthanide mobilization and uptake from different lanthanide minerals, an alloy, and pure lanthanide compounds. Beijerinckiaceae bacterium RH AL1 served as a model organism for an integrated approach combining transcriptomics, analytics, and electron microscopy. This facultative methylotroph depends on light lanthanides for methanol oxidation and forms periplasmic lanthanide deposits. AL1 grew with all tested lanthanide sources and selectively enriched light lanthanides independent of source type, overall lanthanide content, and the proportion of light lanthanides. Transcriptomics revealed that the type of lanthanide source significantly influenced gene expression beyond lanthanide utilization. Lanthanide discrimination in Beijerinckiaceae bacterium RH AL1 is a multilayered process rooted in the complementary action of chelation, uptake mechanisms, and periplasmic storage. Adaptations that increase lanthanide bioavailability transform mineral-bound lanthanides into shared resources within microbial communities, with implications for sustainable lanthanide use.

microbiology↗

The glycine betaine-cobalamin feedback loop drives cross-feeding between marine bacteria and algae

Heterotrophic bacteria supply cobalt-containing cobalamin (Cbl) to marine microalgae, which in return provide organic substrates. Such metabolic cross-feeding can regulate the species composition of prolific marine plankton and biofilms. Algal-produced glycine betaine (GB) can be catabolized by bacteria using a Cbl-dependent demethylase (MtgBCD). Yet, GBs impact on bacterial Cbl production during cross-feeding, and its control by cobalt scarcity remains elusive. Here, we demonstrate that Phaeobacter inhibens bacteria boost their Cbl production 25-fold when grown in monocultures with GB compared to glucose. During co-cultivation, P. inhibens satisfied the Cbl requirements of Gephyrocapsa huxleyi algae. Transcriptomic analysis of mono- and co-cultures revealed co-expression of mtgBCD and gbcAB genes encoding Cbl-dependent and -independent GB demethylases, respectively. Distinct growth defects of deletion mutants indicate that P. inhibens switches from Cbl-dependent to -independent GB demethylation under cobalt limitation, involving a Cbl riboswitch. Our findings suggest a positive feedback loop in which algal GB release stimulates the bacterial supply of Cbl. We predict the breakdown of this interaction under naturally occurring cobalt limitation which potentially contributes to the transient nature of algal blooms. Comparative genomics indicate that this mechanism is widespread in Rhodobacterales and other abundant marine Alphaproteobacteria, underscoring its pivotal role in global ocean productivity.

microbiology↗

An organotrophic Sideroxydans reveals potential iron oxidation marker genes

To understand the ecophysiology and the role of iron-oxidizing bacteria (FeOB) in various ecosystems, we need to identify marker genes of the iron oxidation pathway to track activity in situ. The Gallionellaceae Sideroxydans sp. CL21, an autotrophic iron-oxidizing bacteria isolated from a peatland, is unusual amongst FeOB isolates in its genomic potential to utilize organic compounds as energy sources. Therefore, it offers the unique opportunity to determine genes expressed under litho- versus organotrophic conditions. We demonstrated the growth of Sideroxydans sp. CL21 on organic substrates (lactate and pyruvate) and inorganic substrates (Fe(II), magnetite, thiosulfate, and S(0)). Thus, cells were capable of lithoautotrophic, organotrophic, and potentially organoheterotrophic growth. Surprisingly, when lactate-grown cells were given Fe(II), mid-log phase cells were unable to oxidize iron, while late-log phase cells oxidized iron. To elucidate iron oxidation pathways, we compared gene expression between mid-log (non-iron-oxidizing) and late-log (iron-oxidizing) lactate-grown cells. Genes for iron oxidases (cyc2, mtoA) were highly expressed at both time points, so did not correspond to iron oxidation capability, making them unsuitable marker genes of iron oxidation activity by themselves. However, genes encoding periplasmic and inner membrane cytochromes were significantly upregulated in cells capable of iron oxidation. These genes include mtoD, cymA/imoA, and a cluster of Fe(II)-responsive genes (ircABCD). These findings suggest Gallionellaceae regulate their iron oxidation pathways in multiple stages, with iron oxidase-encoding genes proactively expressed. Other genes encoding electron carriers are upregulated only when iron oxidation is needed, which makes these genes (i.e. ircABCD) good prospective indicators of iron oxidation ability. ImportanceFeOB are widespread in the environment and we suspect that they play key roles in nutrient and other elemental cycles. However, with no isotopic marker, we lack the ability to monitor FeOB activity, prompting us to search for genetic markers. Previous work suggests that expression of iron oxidase genes does not directly correspond to iron oxidation activity in Gallionellaceae and little was known about the other genes in the pathway. Here we study a unique FeOB isolate that possesses organotrophic capabilities and demonstrate its potential for mixotrophic growth on lactate and Fe(II). Its ability to oxidize iron is regulated, allowing us to discover potential iron oxidation pathway genes with expression that corresponds to iron oxidation activity. If these genes can be further validated as iron oxidation marker genes, they will enable us to delineate autotrophic and organoheterotrophic FeOB impacts on carbon cycling in wetlands and other natural and engineered environments.

microbiology↗

Genetic potential for aerobic respiration and denitrification in globally distributed respiratory endosymbionts

The endosymbiont Candidatus Azoamicus ciliaticola generates ATP for its eukaryotic host, an anaerobic ciliate of the Plagiopylea class, fulfilling a function analogous to mitochondria in other eukaryotic cells. The discovery of this respiratory endosymbiosis has major implications for both evolutionary history and ecology of microbial eukaryotes. However, with only a single species described, knowledge of its environmental distribution and diversity is limited. Here we report four new complete, circular metagenome assembled genomes (cMAGs) representing respiratory endosymbionts inhabiting groundwater in California, Ohio, and Germany. These cMAGs form two lineages comprising a monophyletic clade within the uncharacterized gammaproteobacterial order UBA6186, enabling evolutionary analysis of their key protein complexes. Strikingly, all four novel cMAGs encode a cytochrome cbb3 oxidase, which indicates the capacity for both aerobic and anaerobic respiration. Accordingly, we detect these respiratory endosymbionts in diverse habitats worldwide, thus significantly expanding the ecological scope of this respiratory symbiosis.

microbiology↗

Genome streamlining in CPR bacteria transitioning from soil to groundwater

To better understand the influence of habitat on the genetic content of Candidate Phyla Radiation (CPR) bacteria, we studied the effects of transitioning from soil to groundwater on genomic divergences of these organisms. Bacterial metagenome-assembled genomes (318 total, 35 of CPR bacteria) were generated from seepage waters and compared directly to groundwater counterparts. Seepage water CPR bacteria exhibited 1.24-fold greater mean genome size, while their inferred mean replication rate was 21.1% lower than groundwater lineages. While exploring gene loss and adaptive gains in closely related lineages in groundwater, we identified a zinc transporter, a surface protein, and a lipogylcopeptide resistance gene unique to a seepage Parcubacterium. A nitrite reductase gene unique to the groundwater Parcubacterium, likely acquired from pelagic microbes via horizontal gene transfer, was also identified. Groundwater Parcubacteria harbored nearly double the fraction (9.4%) of pseudogenes than their seepage kin (4.9%), suggesting further genome streamlining.

microbiology↗

Differential contribution of nitrifying prokaryotes to nitrification in groundwater

The ecophysiology of complete ammonia-oxidizing bacteria (CMX) of the genus Nitrospira and their widespread occurrence in groundwater suggests that CMX bacteria have a competitive advantage over ammonia-oxidizing bacteria (AOB) and archaea (AOA) in these environments. However, the specific contribution of their activity to nitrification processes has remained unclear. We aimed to disentangle the contribution of CMX, AOA and AOB to nitrification and to identify the environmental drivers of their niche differentiation at different levels of ammonium and oxygen in oligotrophic carbonate rock aquifers. CMX amoA genes accounted on average for 16 to 75% of the total groundwater amoA genes detected. Nitrification rates were positively correlated to CMX clade A associated phylotypes and AOB affiliated with Nitrosomonas ureae. Short-term incubations amended with the nitrification inhibitors allylthiourea and chlorate suggested that AOB contributed a large fraction to overall ammonia oxidation, while metaproteomics analysis confirmed an active role of CMX in both ammonia and nitrite oxidation. Ecophysiological niche differentiation of CMX clades A and B, AOB and AOA was linked to their requirements for ammonium, oxygen tolerance, and metabolic versatility. Our results demonstrate that despite numerical predominance of CMX, the first step of nitrification in oligotrophic groundwater appears to be primarily governed by AOB. Higher growth yields at lower ammonia turnover rates and energy derived from nitrite oxidation most likely enable CMX to maintain consistently high populations.

microbiology↗

A glimpse of the paleome in endolithic microbial communities

The terrestrial subsurface houses a significant proportion of the Earths microbial biomass. Our understanding about terrestrial subsurface microbiomes is almost exclusively derived from groundwater and porous sediments. To obtain more insights about endolithic microbiomes and their metabolic status, we investigated rock samples from the vadose zone, fractured aquifers, and deep aquitards. Using methods from paleogenomics, we recovered sufficient DNA for metagenomics from rock specimens independent of porosity, lithology, and depth. We estimated between 2.81 and 4.25 x 105 cells x g-1 rock. DNA damage patterns revealed paleome signatures (genetic records of past microbial communities) for three rock specimens from the vadose zone. The taxonomy and functional potential of paleome communities revealed increased abundances of chemolithoautotrophs, and a broader metabolic potential for aromatic hydrocarbon breakdown. Our study suggests that limestones represent ideal archives for genetic records of past microbial communities, due to their specific conditions facilitating long-term DNA preservation.

microbiology↗

Groundwater bacterial communities evolve over time, exhibiting oscillating similarity patterns in response to recharge

Time series analyses are a crucial tool for uncovering the patterns and processes shaping microbial communities and their functions, especially in aquatic ecosystems. Subsurface aquatic environments are perceived to be more stable than oceans and lakes, due to the lack of sunlight, the absence of photosysnthetically-driven primary production, low temperature variations, and oligotrophic conditions. However, periodic groundwater recharge should affect the structure and succession of groundwater microbiomes. To disentangle the long-term temporal changes in groundwater bacterial communities of shallow fractured bedrock community, and identify the drivers of the observed patterns, we analysed bacterial 16S rRNA gene sequencing data for samples collected monthly from three groundwater wells over a six-year period (n=230) along a hillslope recharge area. We show that the bacterial communities in the groundwater of limestone-mudstone alternations were not stable over time and showed oscillating dissimilarity patterns which corresponded to periods of groundwater recharge. Further, we observed an increase in dissimilarity over time (generalized additive model P < 0.001) indicating that the successive recharge events result in communities that are increasingly more dissimilar to the initial reference time point. The sampling period was able to explain up to 29.5% of the variability in bacterial community composition and the impact of recharge events on the groundwater microbiome was linked to the strength of the recharge and local environmental selection. Many groundwater bacteria originated from the recharge-related sources (mean = 66.5%, SD = 15.1%) and specific bacterial taxa were identified as being either enriched or repressed during recharge events. Overall, similar to surface aquatic environments, groundwater microbiomes vary through time, though we revealed groundwater recharges as unique driving factors for these patterns. The high temporal resolution employed here highlights the complex dynamics of bacterial communities in groundwater and demonstrated that successive shocks disturb the bacterial communities, leading to decreased similarity to the initial state over time.

microbiology↗

Sulfur-fueled chemolithoautotrophs replenish organic carbon inventory in groundwater

The current understanding of organic carbon inputs into ecosystems lacking photosynthetic primary production is predicated on data and inferences derived almost entirely from metagenomic analyses. The elevated abundances of putative chemolithoautotrophs in groundwaters suggest that dark CO2 fixation is an integral component of subsurface trophic webs. To understand the impact of autotrophically-fixed carbon, the flux of CO2-derived carbon through various subpopulations of subsurface microbiota must first be resolved, both quantitatively and temporally. Here, we implement novel stable isotope cluster analysis to render a time-resolved and quantitative evaluation of 13CO-derived carbon flow through a groundwater microbiome stimulated with reduced sulfur compounds. We demonstrate that mixotrophs, not obligate chemolithoautotrophs, were the most abundant active organisms in groundwater microcosms. Species of Hydrogenophaga, Polaromonas, Dechloromonas, and other metabolically versatile mixotrophs drove the recycling of organic carbon and, when chance afforded, supplemented their carbon requirements via chemolithoautotrophy and uptake of available organic compounds. Mixotrophic activity facilitated the replacement of 43 and 80% of total microbial carbon stores with 13C in just 21 and 70 days, respectively. This opportunistic "utilize whatever pathways net the greatest advantage in fitness" strategy may explain the great abundances of mixotrophs in other oligotrophic habitats, like the upper ocean and boreal lakes.

microbiology↗

Drought and rewetting events enhance nitrate leaching and seepage-mediated translocation of microbes from beech forest soils

Nitrification in forest soils is often associated with increased leaching of nitrate to deeper soil layers with potential impacts on groundwater resources, further enhanced under scenarios of anthropogenic atmospheric nitrogen deposition and predicted weather extremes. We aimed to disentangle the relationships between soil nitrification potential, seepage-mediated nitrate leaching and the vertical translocation of nitrifiers in soils of a temperate mixed beech forest in central Germany before, during and after the severe summer drought 2018. Leaching of nitrate assessed below the litter layer and in 4, 16 and 30 cm soil depth showed high temporal and vertical variation with maxima at 16 and 30 cm during and after the drought period. Maximum of soil potential nitrification activity of 4.4 mg N kg-1 d-1 only partially coincided with maximum nitrate leaching of 10.5 kg N ha-2. Both ammonia oxidizing bacteria (AOB) and ammonia oxidizing archaea (AOA) were subject to translocation by seepage, and AOB decreased at least by half and AOA increased by one to three orders of magnitude in their abundance in seepage with increasing soil depth. On the level of the total bacterial population, an increasing trend with depth was also observed for Cand. Patescibacteria while Bacteroidetes were strongly mobilized from the litter layer but poorly transported further down. Despite stable population densities in soil over time, abundances of AOA, AOB and total bacteria in seepage increased by one order of magnitude after the onset of autumn rewetting. Predicted future higher frequency of drought periods in temperate regions may result in more frequent seepage-mediated seasonal flushes of nitrate and bacteria from forest soils. Moreover, the observed translocation patterns point to taxon-specific differences in the susceptibility to mobilization, suggesting that only selected topsoil derived microbial groups are likely to affect subsoil or groundwater microbial communities and their functional potential.

microbiology↗

Canopy position has a stronger effect than tree species identity on phyllosphere bacterial diversity in a floodplain hardwood forest

The phyllosphere is a challenging microbial habitat in which microorganisms can flourish on organic carbon released by plant leaves but are also exposed to harsh environmental conditions. Here, we assessed the relative importance of canopy position - top, mid, and bottom at a height between 31 m and 20 m - and tree species identity for shaping the phyllosphere microbiome in a floodplain hardwood forest. Leaf material was sampled from three tree species - maple (Acer pseudoplatanus L.), oak (Quercus robur L.), and lime (Tilia cordata MILL.) - at the Leipzig canopy crane facility (Germany). Estimated bacterial species richness (Chao1) and bacterial abundances approximated by quantitative PCR of 16S rRNA genes exhibited clear vertical trends with a strong increase from the top to the mid and bottom position of the canopy. 30 Operational Taxonomic Units (OTUs) formed the core microbiome, which accounted for 77% of all sequence reads. These core OTUs showed contrasting trends in their vertical distribution within the canopy, pointing to different ecological preferences and tolerance to presumably more extreme conditions at the top position of the canopy. Co-occurrence analysis revealed distinct tree species-specific OTU networks, and 55-57% of the OTUs were unique to each tree species. Overall, the phyllosphere microbiome harbored surprisingly high fractions of Actinobacteria of up to 46%. Our results clearly demonstrate strong effects of the position in the canopy on phyllosphere bacterial communities in a floodplain hardwood forest and - in contrast to other temperate or tropical forests - a strong predominance of Actinobacteria.

microbiology↗