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At least 127 records · Page 7

Long-Term Stochasticity Combines With Short-Term Variability in Assembly Processes to Underlie Rice Paddy Sustainability

Revealing temporal patterns of community assembly processes is important for understanding how microorganisms underlie the sustainability of agroecosystem. The ancient terraced rice paddies at Longji provide an ideal platform to study temporal dynamics of agroecosystem sustainability due to their chronosequential records of soil physicochemistry and well-archived microbial information along 630-year rice cultivation. We used statistical null models to evaluate microbial assembly processes along the soil chronosequences of Longji rice paddies through time. Stochastic and deterministic assembly processes jointly governed microbial community composition within successional eras (less than 250 years), and within-era determinism was mainly driven by soil fertility and redox conditions alone or in combination. Conversely, across successional eras (i.e., over 300 years), stochasticity linearly increased with increasing duration between eras and was eventually predominant for the whole 630 years. We suggest that the impact of stochasticity vs. determinism on assembly is timescale-dependent, and we propose that the importance of stochastic assembly of microbial community at longer timescales is due to the gradual changes in soil properties under long-term rice cultivation, which in turn contribute to the sustainability of paddy ecosystem by maintaining a diverse community of microorganisms with multi-functional traits. In total, our results indicate that knowledge on the timescales at which assembly processes govern microbial community composition is key to understanding the ecological mechanisms generating agroecosystem sustainability.

59 BASIC BIOLOGICAL SCIENCES↗

Life and death in the soil microbiome: how ecological processes influence biogeochemistry

We report soil microorganisms shape global element cycles in life and death. Living soil microorganisms are a major engine of terrestrial biogeochemistry, driving the turnover of soil organic matter — Earth’s largest terrestrial carbon pool and the primary source of plant nutrients. Their metabolic functions are influenced by ecological interactions with other soil microbial populations, soil fauna and plants, and the surrounding soil environment. Remnants of dead microbial cells serve as fuel for these biogeochemical engines because their chemical constituents persist as soil organic matter. This non-living microbial biomass accretes over time in soil, forming one of the largest pools of organic matter on the planet. In this Review, we discuss how the biogeochemical cycling of organic matter depends on both living and dead soil microorganisms, their functional traits, and their interactions with the soil matrix and other organisms. With recent omics advances, many of the traits that frame microbial population dynamics and their ecophysiological adaptations can be deciphered directly from assembled genomes or patterns of gene or protein expression. Thus, it is now possible to leverage a trait-based understanding of microbial life and death within improved biogeochemical models and to better predict ecosystem functioning under new climate regimes.

59 BASIC BIOLOGICAL SCIENCES↗

Ecological Trait-Based Digital Categorization of Microbial Genomes for Denitrification Potential

Microorganisms encode proteins that function in the transformations of useful and harmful nitrogenous compounds in the global nitrogen cycle. The major transformations in the nitrogen cycle are nitrogen fixation, nitrification, denitrification, anaerobic ammonium oxidation, and ammonification. The focus of this report is the complex biogeochemical process of denitrification, which, in the complete form, consists of a series of four enzyme-catalyzed reduction reactions that transforms nitrate to nitrogen gas. Denitrification is a microbial strain-level ecological trait (characteristic), and denitrification potential (functional performance) can be inferred from trait rules that rely on the presence or absence of genes for denitrifying enzymes in microbial genomes. Despite the global significance of denitrification and associated large-scale genomic and scholarly data sources, there is lack of datasets and interactive computational tools for investigating microbial genomes according to denitrification trait rules. Therefore, our goal is to categorize archaeal and bacterial genomes by denitrification potential based on denitrification traits defined by rules of enzyme involvement in the denitrification reduction steps. We report the integration of datasets on genome, taxonomic lineage, ecosystem, and denitrifying enzymes to provide data investigations context for the denitrification potential of microbial strains. We constructed an ecosystem and taxonomic annotated denitrification potential dataset of 62,624 microbial genomes (866 archaea and 61,758 bacteria) that encode at least one of the twelve denitrifying enzymes in the four-step canonical denitrification pathway. Our four-digit binary-coding scheme categorized the microbial genomes to one of sixteen denitrification traits including complete denitrification traits assigned to 3280 genomes from 260 bacteria genera. The bacterial strains with complete denitrification potential pattern included Arcobacteraceae strains isolated or detected in diverse ecosystems including aquatic, human, plant, and Mollusca (shellfish). The dataset on microbial denitrification potential and associated interactive data investigations tools can serve as research resources for understanding the biochemical, molecular, and physiological aspects of microbial denitrification, among others. The microbial denitrification data resources produced in our research can also be useful for identifying microbial strains for synthetic denitrifying communities.

59 BASIC BIOLOGICAL SCIENCES↗

The microbial rare biosphere: current concepts, methods and ecological principles

ABSTRACT Our ability to describe the highly diverse pool of low abundance populations present in natural microbial communities is increasing at an unprecedented pace. Yet we currently lack an integrative view of the key taxa, functions and metabolic activity which make-up this communal pool, usually referred to as the ‘rare biosphere’, across the domains of life. In this context, this review examines the microbial rare biosphere in its broader sense, providing an historical perspective on representative studies which enabled to bridge the concept from macroecology to microbial ecology. It then addresses our current knowledge of the prokaryotic rare biosphere, and covers emerging insights into the ecology, taxonomy and evolution of low abundance microeukaryotic, viral and host-associated communities. We also review recent methodological advances and provide a synthetic overview on how the rare biosphere fits into different conceptual models used to explain microbial community assembly mechanisms, composition and function.

Pascoal, Francisco↗

Flooding and ecological restoration promote wetland microbial communities and soil functions on former cranberry farmland

Microbial communities are early responders to wetland degradation, and instrumental players in the reversal of this degradation. However, our understanding of soil microbial community structure and function throughout wetland development remains incomplete. We conducted a survey across cranberry farms, young retired farms, old retired farms, flooded former farms, ecologically restored former farms, and natural reference wetlands with no history of cranberry farming. We investigated the relationship between the microbial community and soil characteristics that restoration intends to maximize, such as soil organic matter, cation exchange capacity and denitrification potential. Among the five treatments considered, flooded and restored sites had the highest prokaryote and microeukaryote community similarity to natural wetlands. In contrast, young retired sites had similar communities to farms, and old retired sites failed to develop wetland microbial communities or functions. Canonical analysis of principal coordinates revealed that soil variables, in particular potassium base saturation, sodium, and denitrification potential, explained 45% of the variation in prokaryote communities and 44% of the variation in microeukaryote communities, segregating soil samples into two clouds in ordination space: farm, old retired and young retired sites on one side and restored, flooded, and natural sites on the other. Heat trees revealed possible prokaryotic ( Gemmatimonadetes ) and microeukaryotic ( Rhizaria ) indicators of wetland development, along with a drop in the dominance of Nucletmycea in restored sites, a class that includes suspected mycorrhizal symbionts of the cranberry crop. Flooded sites showed the strongest evidence of wetland development, with triple the soil organic matter accumulation, double the cation exchange capacity, and seventy times the denitrification potential compared to farms. However, given that flooding does not promote any of the watershed or habitat benefits as ecological restoration, we suggest that flooding can be used to stimulate beneficial microbial communities and soil functions during the restoration waiting period, or when restoration is not an option.

Rubin, Rachel L. (ORCID:0000000284326811)↗

Recovering new viruses from New Mexico soils

Here, we utilized metagenomic and size-filtered virome sequencing to recover 4,157 medium, high, or complete quality viral genomes from soils taken from three high elevation sites in New Mexico, USA. Among recovered viral genomes, 90% were from size-filtered samples, indicating the importance of this enrichment in assessments of complex viromes.

59 BASIC BIOLOGICAL SCIENCES↗

Increasing aggregate size reduces single-cell organic carbon incorporation by hydrogel-embedded wetland microbes

Abstract Microbial degradation of organic carbon in sediments is impacted by the availability of oxygen and substrates for growth. To better understand how particle size and redox zonation impact microbial organic carbon incorporation, techniques that maintain spatial information are necessary to quantify elemental cycling at the microscale. In this study, we produced hydrogel microspheres of various diameters (100, 250, and 500 μm) and inoculated them with an aerobic heterotrophic bacterium isolated from a freshwater wetland (Flavobacterium sp.), and in a second experiment with a microbial community from an urban lacustrine wetland. The hydrogel-embedded microbial populations were incubated with 13C-labeled substrates to quantify organic carbon incorporation into biomass via nanoSIMS. Additionally, luminescent nanosensors enabled spatially explicit measurements of oxygen concentrations inside the microspheres. The experimental data were then incorporated into a reactive-transport model to project long-term steady-state conditions. Smaller (100 μm) particles exhibited the highest microbial cell-specific growth per volume, but also showed higher absolute activity near the surface compared to the larger particles (250 and 500 μm). The experimental results and computational models demonstrate that organic carbon availability was not high enough to allow steep oxygen gradients and as a result, all particle sizes remained well-oxygenated. Our study provides a foundational framework for future studies investigating spatially dependent microbial activity in aggregates using isotopically labeled substrates to quantify growth.

59 BASIC BIOLOGICAL SCIENCES↗

Grassland ecosystem type drives AM fungal diversity and functional guild distribution in North American grasslands

Nutrient exchange forms the basis of the ancient symbiotic relationship that occurs between most land plants and arbuscular mycorrhizal (AM) fungi. Plants provide carbon (C) to AM fungi and fungi provide the plant with nutrients such as nitrogen (N) and phosphorous (P). Nutrient addition can alter this symbiotic coupling in key ways, such as reducing AM fungal root colonization and changing the AM fungal community composition. However, environmental parameters that differentiate ecosystems and drive plant distribution patterns (e.g., pH, moisture), are also known to impact AM fungal communities. Identifying the relative contribution of environmental factors impacting AM fungal distribution patterns is important for predicting biogeochemical cycling patterns and plant-microbe relationships across ecosystems. Here, to evaluate the relative impacts of local environmental conditions and long-term nutrient addition on AM fungal abundance and composition across grasslands, we studied experimental plots amended for 10 years with N, P, or N and P fertilizer in different grassland ecosystem types, including tallgrass prairie, montane, shortgrass prairie, and desert grasslands. Contrary to our hypothesis, we found ecosystem type, not nutrient treatment, was the main driver of AM fungal root colonization, diversity, and community composition, even when accounting for site-specific nutrient limitations. We identified several important environmental drivers of grassland ecosystem AM fungal distribution patterns, including aridity, mean annual temperature, root moisture, and soil pH. This work provides empirical evidence for niche partitioning strategies of AM fungal functional guilds and emphasizes the importance of long-term, large scale research projects to provide ecologically relevant context to nutrient addition studies.

59 BASIC BIOLOGICAL SCIENCES↗

Metabolic capabilities mute positive response to direct and indirect impacts of warming throughout the soil profile

Increasing global temperatures are predicted to stimulate soil microbial respiration. The direct and indirect impacts of warming on soil microbes, nevertheless, remain unclear. This is particularly true for understudied subsoil microbes. Here, we show that 4.5 years of whole-profile soil warming in a temperate mixed forest results in altered microbial community composition and metabolism in surface soils, partly due to carbon limitation. However, microbial communities in the subsoil responded differently to warming than in the surface. Throughout the soil profile—but to a greater extent in the subsoil—physiologic and genomic measurements show that phylogenetically different microbes could utilize complex organic compounds, dampening the effect of altered resource availability induced by warming. We find subsoil microbes had 20% lower carbon use efficiencies and 47% lower growth rates compared to surface soils, which constrain microbial communities. Collectively, our results show that unlike in surface soils, elevated microbial respiration in subsoils may continue without microbial community change in the near-term.

54 ENVIRONMENTAL SCIENCES↗

Propagule Pressure in Microbial Introductions

The use of potentially beneficial microorganisms in agriculture (microbial inoculants) has rapidly accelerated in recent years. For microbial inoculants to be effective as agricultural tools, these organisms must be able to survive and persist in novel environments while not destabilizing the resident community or spilling over into adjacent natural ecosystems. Here, we adapt a macroecological propagule pressure model to a microbial scale and present an experimental approach for testing the role of propagule pressure in microbial inoculant introductions. We experimentally determined the risk-release relationship for an IAA-expressing Pseudomonas simiae inoculant in a model monocot system. We then used this relationship to simulate establishment outcomes under a range of application frequencies (propagule number) and inoculant concentrations (propagule size). Our simulations show that repeated inoculant applications may increase establishment, even when increased inoculant concentration does not alter establishment probabilities. The dataset filed here includes the experimemtal datafile, and a RMarkdown file that includes all the code used in in both the modeling and anaylsis.

agriculture↗

Solutions in microbiome engineering: prioritizing barriers to organism establishment

Abstract Microbiome engineering is increasingly being employed as a solution to challenges in health, agriculture, and climate. Often manipulation involves inoculation of new microbes designed to improve function into a preexisting microbial community. Despite, increased efforts in microbiome engineering inoculants frequently fail to establish and/or confer long-lasting modifications on ecosystem function. We posit that one underlying cause of these shortfalls is the failure to consider barriers to organism establishment. This is a key challenge and focus of macroecology research, specifically invasion biology and restoration ecology. We adopt a framework from invasion biology that summarizes establishment barriers in three categories: (1) propagule pressure, (2) environmental filtering, and (3) biotic interactions factors. We suggest that biotic interactions is the most neglected factor in microbiome engineering research, and we recommend a number of actions to accelerate engineering solutions.

59 BASIC BIOLOGICAL SCIENCES↗

Shrub and sedge rhizosphere communities display distinct affinities toward exudates and soil organic matter degradation: a quantitative stable isotope probing analysis

Warming temperatures are accelerating permafrost thaw and changing tundra vegetation, where woody shrubs are displacing sedges. Shrubs, such as Betula nana, and sedges, such as Eriophorum vaginatum, exhibit distinct life strategies including unique root-associated, or rhizosphere microbial communities. As permafrost thaws it unlocks previously unavailable carbon and nutrient sources resulting in deeper roots and a translocation of rhizosphere communities. Because permafrost microbial communities contain lower diversity and biomass than rhizosphere communities, the coalescence of rhizosphere and permafrost microbial communities could alter soil organic matter (SOM) degradation rates and increase greenhouse gas emissions. To identify metabolic strategies across distinct rhizosphere and permafrost microbial communities we conducted an isotope tracing incubation experiment. We inoculated thawed permafrost with shrub and sedge rhizosphere communities while adding exudates or water daily and compared this to an uninoculated control. After 46 days, we spiked samples with 18O enriched water or 13C enriched exudates and measured isotope incorporation into microbial DNA with quantitative stable isotope probing (qSIP). Our results indicate that exudate additions had little effect on uninoculated permafrost communities but the addition of exudates and rhizosphere inoculants had a compounding effect on respiration rates. We found that soils inoculated with shrub rhizosphere communities contained a mixture of exudate and SOM degraders while soils inoculated with sedge rhizosphere communities contained mainly SOM degraders. Finally, we found that individual microbial taxa exhibited maximum growth rates under specific combinations of microbial inoculant communities and exudate addition treatments. Our results reveal that microbial niches are strongly influenced by substrate preferences and community context, and suggest that a reduction in sedges and an expansion of shrubs may provide a mechanism by which permafrost carbon losses are mitigated through corresponding shifts in microbial communities and their substrate preferences.

Schaefer, Sean R [Natural Resources and Earth Syst↗

Microbially mediated mechanisms underlie soil carbon accrual by conservation agriculture under decade-long warming

Increasing soil organic carbon (SOC) in croplands by switching from conventional to conservation management may be hampered by stimulated microbial decomposition under warming. Here, we test the interactive effects of agricultural management and warming on SOC persistence and underlying microbial mechanisms in a decade-long controlled experiment on a wheat-maize cropping system. Warming increased SOC content and accelerated fungal community temporal turnover under conservation agriculture (no tillage, chopped crop residue), but not under conventional agriculture (annual tillage, crop residue removed). Microbial carbon use efficiency (CUE) and growth increased linearly over time, with stronger positive warming effects after 5 years under conservation agriculture. According to structural equation models, these increases arose from greater carbon inputs from the crops, which indirectly controlled microbial CUE via changes in fungal communities. As a result, fungal necromass increased from 28 to 53%, emerging as the strongest predictor of SOC content. Collectively, our results demonstrate how management and climatic factors can interact to alter microbial community composition, physiology and functions and, in turn, SOC formation and accrual in croplands.

59 BASIC BIOLOGICAL SCIENCES↗

Fast-decaying plant litter enhances soil carbon in temperate forests but not through microbial physiological traits

Abstract Conceptual and empirical advances in soil biogeochemistry have challenged long-held assumptions about the role of soil micro-organisms in soil organic carbon (SOC) dynamics; yet, rigorous tests of emerging concepts remain sparse. Recent hypotheses suggest that microbial necromass production links plant inputs to SOC accumulation, with high-quality (i.e., rapidly decomposing) plant litter promoting microbial carbon use efficiency, growth, and turnover leading to more mineral stabilization of necromass. We test this hypothesis experimentally and with observations across six eastern US forests, using stable isotopes to measure microbial traits and SOC dynamics. Here we show, in both studies, that microbial growth, efficiency, and turnover are negatively (not positively) related to mineral-associated SOC. In the experiment, stimulation of microbial growth by high-quality litter enhances SOC decomposition, offsetting the positive effect of litter quality on SOC stabilization. We suggest that microbial necromass production is not the primary driver of SOC persistence in temperate forests. Factors such as microbial necromass origin, alternative SOC formation pathways, priming effects, and soil abiotic properties can strongly decouple microbial growth, efficiency, and turnover from mineral-associated SOC.

54 ENVIRONMENTAL SCIENCES↗

microTrait: A Toolset for a Trait-Based Representation of Microbial Genomes

Remote sensing approaches have revolutionized the study of macroorganisms, allowing theories of population and community ecology to be tested across increasingly larger scales without much compromise in resolution of biological complexity. In microbial ecology, our remote window into the ecology of microorganisms is through the lens of genome sequencing. For microbial organisms, recent evidence from genomes recovered from metagenomic samples corroborate a highly complex view of their metabolic diversity and other associated traits which map into high physiological complexity. Regardless, during the first decades of this omics era, microbial ecological research has primarily focused on taxa and functional genes as ecological units, favoring breadth of coverage over resolution of biological complexity manifested as physiological diversity. Recently, the rate at which provisional draft genomes are generated has increased substantially, giving new insights into ecological processes and interactions. From a genotype perspective, the wide availability of genome-centric data requires new data synthesis approaches that place organismal genomes center stage in the study of environmental roles and functional performance. Extraction of ecologically relevant traits from microbial genomes will be essential to the future of microbial ecological research. Here, we present microTrait , a computational pipeline that infers and distills ecologically relevant traits from microbial genome sequences. microTrait maps a genome sequence into a trait space, including discrete and continuous traits, as well as simple and composite. Traits are inferred from genes and pathways representing energetic, resource acquisition, and stress tolerance mechanisms, while genome-wide signatures are used to infer composite, or life history, traits of microorganisms. This approach is extensible to any microbial habitat, although we provide initial examples of this approach with reference to soil microbiomes.

Karaoz, Ulas↗

Contrasting geochemical and fungal controls on decomposition of lignin and soil carbon at continental scale

Lignin is an abundant and complex plant polymer that may limit litter decomposition, yet lignin is sometimes a minor constituent of soil organic carbon (SOC). Accounting for diversity in soil characteristics might reconcile this apparent contradiction. Tracking decomposition of a lignin/litter mixture and SOC across different North American mineral soils using lab and field incubations, here we show that cumulative lignin decomposition varies 18-fold among soils and is strongly correlated with bulk litter decomposition, but not SOC decomposition. Climate legacy predicts decomposition in the lab, and impacts of nitrogen availability are minor compared with geochemical and microbial properties. Lignin decomposition increases with some metals and fungal taxa, whereas SOC decomposition decreases with metals and is weakly related with fungi. Decoupling of lignin and SOC decomposition and their contrasting biogeochemical drivers indicate that lignin is not necessarily a bottleneck for SOC decomposition and can explain variable contributions of lignin to SOC among ecosystems.

54 ENVIRONMENTAL SCIENCES↗

Microbial growth under drought is confined to distinct taxa and modified by potential future climate conditions

Climate change increases the frequency and intensity of drought events, affecting soil functions including carbon sequestration and nutrient cycling, which are driven by growing microorganisms. Yet we know little about microbial responses to drought due to methodological limitations. Here, we estimate microbial growth rates in montane grassland soils exposed to ambient conditions, drought, and potential future climate conditions (i.e., soils exposed to 6 years of elevated temperatures and elevated CO 2 levels). For this purpose, we combined 18 O-water vapor equilibration with quantitative stable isotope probing (termed ‘vapor-qSIP’) to measure taxon-specific microbial growth in dry soils. In our experiments, drought caused >90% of bacterial and archaeal taxa to stop dividing and reduced the growth rates of persisting ones. Under drought, growing taxa accounted for only 4% of the total community as compared to 35% in the controls. Drought-tolerant communities were dominated by specialized members of the Actinobacteriota, particularly the genus Streptomyces. Six years of pre-exposure to future climate conditions (3 °C warming and + 300 ppm atmospheric CO 2 ) alleviated drought effects on microbial growth, through more drought-tolerant taxa across major phyla, accounting for 9% of the total community. Our results provide insights into the response of active microbes to drought today and in a future climate, and highlight the importance of studying drought in combination with future climate conditions to capture interactive effects and improve predictions of future soil-climate feedbacks.

54 ENVIRONMENTAL SCIENCES↗