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Karaoz, U.

Publications and source records attributed to Karaoz, U..

11 recordsLinked to original sources

The long-term application of composted organic wastes caused a lasting increase in vineyard soil health and multifunctionality

As a consequence of climate change and unsustainable management practices, agricultural soils in the Mediterranean region are often degraded. The application of composted organic wastes is traditionally considered a beneficial practice to improve soil health. We studied the permanence of the beneficial effects of the long-term (20 years) application of composted organic wastes, versus mineral fertilization or no fertilization, on Mediterranean vineyard soil health. To this aim, four years after ceasing fertilization, a comprehensive analysis of soil physicochemical and biological properties, including prokaryotic diversity and functional traits by genome-centric metagenomics, was conducted to ascertain whether the beneficial effects of organic fertilization were maintained 4 years after its end. In general, but not always, soils treated with composted organic wastes showed significantly higher values of many physicochemical and biological properties (e.g., organic matter, Olsen phosphorus and extractable potassium), resulting in improved soil multifunctionality. However, despite such statistical significance, the quantitative magnitude of many of those differences was small. Fertilization regimes had a lasting strong influence on soil prokaryotic communities, as 70% of the 200 metagenome-assembled genomes and 86% of the prokaryotic functional traits showed significant differences among treatments. Organic amendments promoted nitrifying taxa such as Nitrosocosmicus oleophilus and Nitrospira japonica. In minerally-fertilized soils, resource acquisition and stress tolerance strategies were fostered among prokaryotic communities, possibly due to resource limitation and soil degradation, respectively. Stress tolerance traits were lower under organic fertilization, likely due to the improved soil properties and functions. The results obtained suggest that soil functions are influenced by microbial genes involved in nitrogen and carbon cycling, underscoring the central role of microbial metabolism in sustaining soil health and ecosystem functioning. This study demonstrates the lasting benefits of composted organic amendments in promoting soil multifunctionality in vineyard soils.

genomics↗

Coordinated organic and inorganic nitrogen transformations fuel soil microbial blooms and increase nitrogen retention during snowmelt

Snowmelt in high-elevation watersheds triggers a microbial bloom and crash that affects nitrogen (N) export. Predicting watershed N dynamics as snowpack declines is a challenge because the mechanisms that underlie this microbial bloom and crash are uncertain. Using a multi-omic approach, we show that the dynamic molecular properties of dissolved organic N, plus high gene expression for peptidases that recycle microbial biomass, suggested that microbial turnover provided N for biosynthesis during the microbial bloom. Amino acid fermentation by Bradyrhizobia produced organic acids that also fueled denitrification and dissimilatory nitrate reduction to ammonia (DNRA) during snowmelt. Nitrification in spring was driven by Spring-Adapted Nitrososphaerales, which utilized ammonium derived from osmolyte degradation by Winter-Adapted Solirubrobacteraceae. High DNRA gene expression after snowmelt suggested significant nitrate retention, increasing watershed N retention potential. However, declining snowfall may compromise microbial regulation of soil N retention, with implications for watershed N export.

microbiology↗

Virus diversity and activity is driven by snowmelt and host dynamics in a high-altitude watershed soil ecosystem

Viruses, including phages, impact nearly all organisms on Earth, including microbial communities and their associated biogeochemical processes. In soils, highly diverse viral communities have been identified, with a global distribution seemingly driven by multiple biotic and abiotic factors, especially soil temperature and moisture. However, our current understanding of the stability of soil viral communities across time, and their response to strong seasonal change in environmental parameters remains limited. Here, we investigated the diversity and activity of environmental DNA and RNA viruses, including phages, across dynamics seasonal changes in a snow-dominated mountainous watershed by examining paired metagenomes and metatranscriptomes. We identified a large number of DNA and RNA viruses taxonomically divergent from existing environmental viruses, including a significant proportion of RNA viruses target fungal hosts and a large and unsuspected diversity of positive single-stranded RNA phages (Leviviricetes), highlighting the under-characterization of the global soil virosphere. Among these, we were able to distinguish subsets of active phages which changed across seasons, consistent with a "seed-bank" viral community structure in which new phage activity, for example replication and host lysis, is sequentially triggered by changes in environmental conditions. Zooming in at the population level, we further identified virus-host dynamics matching two existing ecological models: "Kill-The-Winner" which proposes that lytic phages are actively infecting abundant bacteria, and "Piggyback-The-Persistent" which argues that when the host is growing slowly it is more beneficial to remain in a lysogenic state. The former was associated with summer months of high and rapid microbial activity, and the latter to winter months of limited and slow host growth. Taken together, these results suggest that the high diversity of viruses in soils is likely associated with a broad range of host interaction types each adapted to specific host ecological strategies and environmental conditions. Moving forward, while as our understanding of how environmental and host factors drive viral activity in soil ecosystems progresses, integrating these viral impacts in complex natural microbiome models will be key to accurately predict ecosystem biogeochemistry.

microbiology↗

Influence of root cortical aerenchyma on the rhizosphere microbiome of field-grown maize

The root anatomical phenotype root cortical aerenchyma (RCA) decreases the metabolic cost of soil exploration and improves plant growth under drought and low soil fertility. RCA may also change the microenvironment of rhizosphere microorganisms by increasing oxygen availability or by reducing carbon rhizodeposition. We tested the hypothesis that plants with contrasting expression of RCA have different rhizosphere prokaryotic communities. Maize inbreds were grown in two field sites, Limpopo Province, South Africa and Pennsylvania, USA, and their rhizosphere soil sampled at flowering. High- and low-nitrogen fertilization was imposed as separate treatments in the experiment in South Africa. The rhizosphere microbial composition of plants with contrasting RCA was characterized by metabarcoding of the 16S rRNA genes. Geographic location was the most important factor related to the composition of rhizosphere microbial communities. In the site in South Africa, RCA explained greater percent of variance (9%) in the composition of microbial communities than genotype (7%). Although other root anatomical and architectural phenotypes were studied as possible cofactors affecting the microbial composition, RCA was among the best significant explanatory variables for the South African site although it was neutral in the Pennsylvania site. High-RCA rhizospheres significantly enriched OTUs of the families Burkholderiaceae (in South Africa) and Bacillaceae (in USA), compared to low-RCA plants, and OTUs of the families Beijerinckiaceae and Sphingomonadaceae were enriched at the two nitrogen levels in high RCA plants in South Africa. Our results are consistent with the hypothesis that RCA is an important factor for rhizosphere microbial communities, especially under suboptimal nitrogen conditions.

plant biology↗

Life history strategies and niches of soil bacteria emerge from interacting thermodynamic, biophysical, and metabolic traits

Efficient biochemical transformation of belowground carbon by microorganisms plays a critical role in determining the long-term fate of soil carbon. As plants assimilate carbon from the atmosphere, up to 50% is exuded into the area surrounding growing roots, where it may be transformed into microbial biomass and subsequently stabilized through mineral associations. However, due to a hierarchy of interacting microbial traits, it remains elusive how emergent life-history strategies of microorganisms influence the processing of root exudate carbon. Here, by combining theory-based predictions of substrate uptake kinetics for soil bacteria and a new genome-informed trait-based dynamic energy budget model, we predicted life history traits and trade-offs of a broad range of soil bacteria growing on 82 root exudate metabolites. The model captured resource-dependent trade-offs between growth rate (power) and growth efficiency (yield) that are fundamental to microbial fitness in communities. During early phases of plant development, growth rates of bacteria were largely constrained by maximum growth potential, highlighting the predictive power of genomic traits during nutrient-replete soil conditions. In contrast, selection for efficiency was important later in the plant growing season, where the model successfully predicted microbial substrate preferences for aromatic organic acids and plant hormones. The predicted carbon-use efficiencies for growth on organics acids were much higher than typical values observed in soil. These predictions provide mechanistic underpinning for the apparent efficiency of the microbial route to mineral stabilization in the rhizosphere and add an additional layer of complexity to rhizosphere microbial community assembly.

ecology↗

Metabolic traits and the niche of bulk soil bacteria in a Mediterranean grassland

Soil microorganisms have adapted to compete and exploit different metabolic niches in their physically and chemically diverse environment via evolution and acquisition of distinct physiological and biochemical traits. As the interface for most carbon and nutrient exchange between plants and microorganisms, the rhizosphere has received substantial attention. By comparison, what is commonly termed bulk-soil (soil free of living roots) represents a far greater volume and surface area throughout the season, and substantially higher taxonomic and phylogenetic diversity; the traits and activity of its inhabitants may also have a significant impact on overall soil function. We used a combination of comparative genomics and exoproteomics to identify metabolic traits of bacteria adapted to life in bulk soil and compared these with traits of bacteria living in the rhizosphere of wild oat, Avena barbata. In bulk soil bacteria, we observed: (i) greater investment in extracellular polymer-degrading enzyme production; (ii) greater potential for secretion (presence of signal peptides) of polymer-degrading enzymes; (iii) production of accessory proteins (carbohydrate binding modules) fused with glycoside hydrolases that enhance substrate affinity, stabilize, and increase reaction rates of polymer degrading enzymes; and (iv) organization of polymer degradation machinery within gene clusters that facilitate co-transcription of enzymes, transcription factors and transporters for polymer depolymerization products. Together, these findings suggest that unlike rhizosphere-adapted bacteria--which specialize on small molecules released primarily as root exudates--bulk soil-adapted bacteria have evolved to exploit plant polymers. This biochemically costly strategy may be mitigated by protein-level adaptations that enhance the efficiency of extracellular enzyme-mediated substrate acquisition. IMPORTANCEPlant-soil-microbe interactions are dynamic and complex, with significant implications for ecosystem functioning. Microbial traits, such as nutrient acquisition and growth yield, combined with soil and climate parameters, impact major biogeochemical processes and can define the future fate of soil carbon. Diverse soil microorganisms occupy different physical habitats within soil and exploit distinct niches by expressing different metabolic traits. Identifying and quantifying traits that underlie their fitness and function is key for understanding and predicting how soil carbon transformation and stabilization will change in the future or can be managed through intervention.

microbiology↗

The snowmelt niche differentiates three microbial life strategies that influence soil nitrogen availability during and after winter

Soil microbial biomass can reach its annual maximum pool size beneath the winter snowpack and is known to decline abruptly following snowmelt in seasonally snow-covered ecosystems. Observed differences in winter versus summer microbial taxonomic composition also suggests that phylogenetically conserved traits may permit winter-versus summer-adapted microorganisms to occupy distinct niches. In this study, we sought to identify archaea, bacteria, and fungi that are associated with the soil microbial bloom overwinter and the subsequent biomass collapse following snowmelt at a high-altitude watershed in central Colorado, USA. Archaea, bacteria, and fungi were categorized into three life strategies (Winter-Adapted, Snowmelt-Specialist, Spring-Adapted) based on changes in abundance during winter, the snowmelt period, and after snowmelt in spring. We calculated indices of phylogenetic relatedness (archaea and bacteria) or assigned functional attributes (fungi) to organisms within life strategies to infer whether phylogenetically conserved traits differentiate Winter-Adapted, Snowmelt-Specialist, and Spring-Adapted groups. We observed that the soil microbial bloom was correlated in time with a pulse of snowmelt infiltration, which commenced 65 days prior to soils becoming snow-free. A pulse of nitrogen (N, as nitrate) occurred after snowmelt, along with a collapse in the microbial biomass pool size, and an increased abundance of nitrifying archaea and bacteria (e.g., Thaumarchaeota, Nitrospirae). Winter- and Spring-Adapted archaea and bacteria were phylogenetically clustered, suggesting that phylogenetically conserved traits allow Winter- and Spring-Adapted archaea and bacteria to occupy distinct niches. In contrast, Snowmelt-Specialist archaea and bacteria were phylogenetically overdispersed, suggesting that the key mechanism(s) of the microbial biomass crash are likely to be density-dependent (e.g., trophic interactions, competitive exclusion) and affect organisms across a broad phylogenetic spectrum. Saprotrophic fungi were the dominant functional group across fungal life strategies, however, ectomycorrhizal fungi experienced a large increase in abundance in spring. If well-coupled plant-mycorrhizal phenology currently buffers ecosystem N losses in spring, then changes in snowmelt timing may alter ecosystem N retention potential. Overall, we observed that the snowmelt separates three distinct soil niches that are occupied by ecologically distinct groups of microorganisms. This ecological differentiation is of biogeochemical importance, particularly with respect to the mobilization of nitrogen during winter, before and after snowmelt.

microbiology↗

Sympatric and allopatric differentiation delineate population structure in a free-living terrestrial bacterium

In free-living bacteria and archaea, the equivalent of the biological species concept does not exist, creating several barriers to the study of the processes contributing to microbial diversification. As such, microorganisms are often operationally defined using conserved marker genes (i.e., 16S rRNA gene) or whole-genome measurements (i.e., ANI) to interpret intra-specific processes. However, as in eukaryotes, investigations into microbial populations must consider the potential for interacting genotypes among individuals that are subjected to similar environmental selective pressures. Therefore, we isolated 26 strains within a single bacterial ecotype (equivalent to a eukaryotic species definition) from a common habitat (leaf litter) across a regional climate gradient and asked whether the genetic diversity in a free-living soil bacterium (Curtobacterium) was consistent with patterns of allopatric or sympatric differentiation. By examining patterns of gene flow, our results indicate that microbial populations are delineated by gene flow discontinuities and exhibit evidence for population-specific adaptation. We conclude that the genetic structure within this bacterium is due to both adaptation within localized microenvironments (isolation-by-environment) as well as dispersal limitation between geographic locations (isolation-by-distance).

evolutionary biology↗

Niche differentiation is spatially and temporally regulated in the rhizosphere

The rhizosphere is a hotspot for microbial C transformations, and the origin of root polysaccharides and polymeric carbohydrates that are important precursors to soil organic matter. However, the ecological mechanisms that underpin rhizosphere carbohydrate depolymerization are poorly understood. Using Avena fatua, a common annual grass, we analyzed time-resolved metatranscriptomes to compare microbial function in rhizosphere, detritusphere, and combined rhizosphere-detritusphere habitats. Population transcripts were binned with a unique reference database generated from soil isolate and single amplified genomes, metagenomes, and stable isotope probing metagenomes. While soil habitat significantly affected both community composition and overall gene expression, succession of microbial functions occurred at a faster time scale than compositional changes. Using hierarchical clustering of upregulated decomposition gene expression, we identified four distinct microbial guilds populated by taxa whose functional succession patterns suggest specialization for substrates provided by fresh growing roots, decaying root detritus, the combination of live and decaying root biomass, or aging root material. Carbohydrate depolymerization genes were consistently upregulated in the rhizosphere, and both taxonomic and functional diversity were high in the combined rhizosphere-detritusphere--suggesting coexistence of rhizosphere guilds is facilitated by niche differentiation. Metatranscriptome-defined guilds provide a framework to model rhizosphere succession and its consequences for soil carbon cycling.

ecology↗

Metagenomics reveals niche partitioning within the phototrophic zone of a microbial mat

Hypersaline photosynthetic microbial mats are stratified microbial communities known for their taxonomic and metabolic diversity and strong light-driven day-night environmental gradients. In this study of the upper photosynthetic zone of hypersaline microbial mats of Elkhorn Slough, California (USA), we show how reference-based and reference-free methods can be used to meaningfully assess microbial ecology and genetic partitioning in these complex microbial systems. Mapping of metagenome reads to the dominant Cyanobacteria observed in the system, Coleofasciculus (Microcoleus) chthonoplastes, was used to examine strain variants within these metagenomes. Highly conserved gene subsystems indicate a core genome for the species, and a number of variant genes and subsystems suggest strain level differentiation, especially for carbohydrate utilization. Metagenome sequence coverage binning was used to assess ecosystem partitioning of remaining microbes. Functional gene annotation of these bins (primarily of Proteobacteria, Bacteroidetes, and Cyanobacteria) recapitulated the known biogeochemical functions in microbial mats using a genetic basis, and also revealed evidence of novel functional diversity within the Gemmatimonadetes and Gammaproteobacteria. Combined, these two approaches show how genetic partitioning can inform biogeochemical partitioning of the metabolic diversity within microbial ecosystems.

microbiology↗

Linking soil biology and chemistry using bacterial isolate exometabolite profiles

Sequencing provides a window into microbial community structure and metabolic potential; however, linking these data to exogenous metabolites that microorganisms process and produce (the exometabolome) remains challenging. Previously, we observed strong exometabolite niche partitioning among bacterial isolates from biological soil crust (biocrust). Here we examine native biocrust to determine if these patterns are reproduced in the environment. Overall, most soil metabolites displayed the expected relationship (positive or negative correlation) with four dominant bacteria following a wetting event and across biocrust developmental stages. For metabolites that were previously found to be consumed by an isolate, 78% were negatively correlated with the abundance of in situ isolate phylotypes whereas for released metabolites, 73% were positively correlated. Our results demonstrate that metabolite profiling, sequencing and exometabolomics can be successfully integrated to functionally link metagenomes and microbial community structure with environmental chemistry.

microbiology↗