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At least 217 records · Page 12

Composition and metabolism of microbial communities in soil pores

Delineation of microbial habitats within the soil matrix and characterization of their environments and metabolic processes are crucial to understand soil functioning, yet their experimental identification remains persistently limited. We combined single- and triple-energy X-ray computed microtomography with pore specific allocation of 13 C labeled glucose and subsequent stable isotope probing to demonstrate how long-term disparities in vegetation history modify spatial distribution patterns of soil pore and particulate organic matter drivers of microbial habitats, and to probe bacterial communities populating such habitats. Here we show striking differences between large (30-150 µm Ø) and small (4-10 µm Ø) soil pores in (i) microbial diversity, composition, and life-strategies, (ii) responses to added substrate, (iii) metabolic pathways, and (iv) the processing and fate of labile C. We propose a microbial habitat classification concept based on biogeochemical mechanisms and localization of soil processes and also suggests interventions to mitigate the environmental consequences of agricultural management.

59 BASIC BIOLOGICAL SCIENCES↗

Asgard archaea modulate potential methanogenesis substrates in wetland soil

The roles of Asgard archaea in eukaryogenesis and marine biogeochemical cycles are well studied, yet their contributions in soil ecosystems remain unknown. Of particular interest are Asgard archaeal contributions to methane cycling in wetland soils. To investigate this, we reconstructed two complete genomes for soil-associated Atabeyarchaeia, a new Asgard lineage, and a complete genome of Freyarchaeia, and predicted their metabolism in situ. Metatranscriptomics reveals expression of genes for [NiFe]-hydrogenases, pyruvate oxidation and carbon fixation via the Wood-Ljungdahl pathway. Also expressed are genes encoding enzymes for amino acid metabolism, anaerobic aldehyde oxidation, hydrogen peroxide detoxification and carbohydrate breakdown to acetate and formate. Overall, soil-associated Asgard archaea are predicted to include non-methanogenic acetogens, highlighting their potential role in carbon cycling in terrestrial environments.

59 BASIC BIOLOGICAL SCIENCES↗

Genome-guided isolation of the hyperthermophilic aerobe Fervidibacter sacchari reveals conserved polysaccharide metabolism in the Armatimonadota

Few aerobic hyperthermophilic microorganisms degrade polysaccharides. Here, we describe the genome-enabled enrichment and optical tweezer-based isolation of an aerobic polysaccharide-degrading hyperthermophile, Fervidibacter sacchari, previously ascribed to candidate phylum Fervidibacteria. F. sacchari uses polysaccharides and monosaccharides for growth at 65–87.5°C and expresses 191 carbohydrate-active enzymes (CAZymes) according to RNA-Seq and proteomics, including 31 with unusual glycoside hydrolase domains (GH109, GH177, GH179). Fluorescence in-situ hybridization and nanoscale secondary ion mass spectrometry confirmed rapid assimilation of 13 C-starch in spring sediments. Purified GHs were optimally active at 80–100°C on ten different polysaccharides. Finally, we propose reassigning Fervidibacteria as a class within phylum Armatimonadota, along with 18 other species, and show that a high number and diversity of CAZymes is a hallmark of the phylum, in both aerobic and anaerobic lineages. Our study establishes Fervidibacteria as hyperthermophilic polysaccharide degraders in terrestrial geothermal springs and suggests a broad role for Armatimonadota in polysaccharide catabolism.

59 BASIC BIOLOGICAL SCIENCES↗

Northern peatland microbial communities exhibit resistance to warming and acquire electron acceptors from soil organic matter

The response of microbial communities that regulate belowground carbon turnover to climate change drivers in peatlands is poorly understood. Here, we leverage a whole ecosystem warming experiment to elucidate the key processes of terminal carbon decomposition and community responses to temperature rise. Our dataset of 697 metagenome-assembled genomes (MAGs) represents the microbial community from the surface (10 cm) to 2 m deep into the peat column, with only 3.7% of genomes overlapping with other well-studied peatlands. Community composition has yet to show a significant response to warming after 3 years, suggesting that metabolically diverse soil microbial communities are resistant to climate change. Surprisingly, abundant and active methanogens in the genus Candidatus Methanoflorens, Methanobacterium , and Methanoregula show the potential for both acetoclastic and hydrogenotrophic methanogenesis. Nonetheless, the predominant pathways for anaerobic carbon decomposition include sulfate/sulfite reduction, denitrification, and acetogenesis, rather than methanogenesis based on gene abundances. Multi-omics data suggest that organic matter cleavage provides terminal electron acceptors, which together with methanogen metabolic flexibility, may explain peat microbiome composition resistance to warming.

54 ENVIRONMENTAL SCIENCES↗

Carbon monoxide oxidation expands the known metabolic capacity in anaerobic methanotrophic consortia

Consortia of anaerobic methane-oxidizing archaea (ANME-2) and sulphate-reducing bacteria (SRB) represent globally relevant syntrophic associations capable of growing with minimal amounts of free energy and can persist when methane becomes limiting. Carbon monoxide (CO) has been reported in seep environments and represents a thermodynamically favourable alternative electron donor due to its low reduction potential. Here, we show that environmental ANME-SRB consortia can oxidize CO in the absence of methane, in anoxic microcosm experiments using a combination of stable isotope geochemical tracers, metatranscriptomics, and single cell activity measurements (FISH–nanoSIMS). The oxidation of CO was coupled with sulphate-reduction by syntrophic consortia, and, in the absence of sulphate, through CO 2 reduction to methane by ANME-2. Under these conditions, the production of methane was one ninth the rate of methanotrophy coupled to sulphate-reduction. Paired single cell FISH-nanoSIMS analysis of anabolic activity indicates that CO respiration appears to support cell maintenance rather than active growth, consistent with the observed down-regulation of energy generating complexes in ANME (e.g., mtr, rnf, etc.). The versatile capability of CO oxidation by anaerobic methanotrophic consortia broadens our understanding of carbon cycling in methane seeps and highlights potential mechanisms of resilience by methanotrophic archaea under changing geochemical regimes.

03 NATURAL GAS↗

Soil microbiome predictability increases with spatial and taxonomic scale

Soil microorganisms shape ecosystem function, yet it remains an open question whether we can predict the composition of the soil microbiome in places before observing it. Furthermore, it is unclear whether the predictability of microbial life exhibits taxonomic- and spatial-scale dependence, as it does for macrobiological communities. Here, we leverage multiple large-scale soil microbiome surveys to develop predictive models of bacterial and fungal community composition in soil, then test these models against independent soil microbial community surveys from across the continental United States. We find remark- able scale dependence in community predictability. The predictability of bacterial and fungal communities increases with the spatial scale of observation, and fungal predictability increases with taxonomic scale. These patterns suggest that there is an increasing importance of deterministic versus stochastic processes with scale, consistent with findings in plant and animal communities, suggesting a general scaling relationship across biology. Biogeochemical functional groups and high-level taxonomic groups of microorganisms were equally predictable, indicating that traits and taxonomy are both powerful lenses for understanding soil communities. Here, by focusing on out-of-sample prediction, these findings suggest an emerging generality in our understanding of the soil microbiome, and that this understanding is fundamentally scale dependent

Biogeography↗

Viral but not bacterial community successional patterns reflect extreme turnover shortly after rewetting dry soils

As central members of soil trophic networks, viruses have the potential to drive substantial microbial mortality and nutrient turnover. Pinpointing viral contributions to terrestrial ecosystem processes remains a challenge, as temporal dynamics are difficult to unravel in the spatially and physicochemically heterogeneous soil environment. In Mediterranean grasslands, the first rainfall after seasonal drought provides an ecosystem reset, triggering microbial activity during a tractable window for capturing short-term dynamics. In this report we simulated precipitation in microcosms from four distinct dry grassland soils and generated 144 viromes, 84 metagenomes and 84 16S ribosomal RNA gene amplicon datasets to characterize viral, prokaryotic and relic DNA dynamics over 10 days. Vastly different viral communities in each soil followed remarkably similar successional trajectories. Wet-up triggered a significant increase in viral richness, followed by extensive compositional turnover. Temporal succession in prokaryotic communities was much less pronounced, perhaps suggesting differences in the scales of activity captured by viromes (representing recently produced, ephemeral viral particles) and total DNA. Still, differences in the relative abundances of Actinobacteria (enriched in dry soils) and Proteobacteria (enriched in wetted soils) matched those of their predicted phages, indicating viral predation of dominant bacterial taxa. Rewetting also rapidly depleted relic DNA, which subsequently reaccumulated, indicating substantial new microbial mortality in the days after wet-up, particularly of the taxa putatively under phage predation. Production of abundant, diverse viral particles via microbial host cell lysis appears to be a conserved feature of the early response to soil rewetting, and results suggest the potential for ‘Cull-the-Winner’ dynamics, whereby viruses infect and cull but do not decimate dominant host populations.

54 ENVIRONMENTAL SCIENCES↗

Effect of tectonic processes on biosphere–geosphere feedbacks across a convergent margin

The subsurface is among Earth’s largest biomes, but the extent to which microbial communities vary across tectonic plate boundaries or interact with subduction-scale geological processes remains unknown. Here we compare bacterial community composition with deep-subsurface geochemistry from 21 hot springs across the Costa Rican convergent margin. We find that cation and anion compositions of the springs reflect the dip angle and position of the underlying tectonic structure and also correlate with the bacterial community. Co-occurring microbial cliques related to cultured chemolithoautotrophs that use the reverse tricarboxylic acid cycle (rTCA) as well as abundances of metagenomic rTCA genes correlate with concentrations of slab-volatilized carbon. This, combined with carbon isotope evidence, suggests that fixation of slab-derived CO2 into biomass may support a chemolithoautotrophy-based subsurface ecosystem. We calculate that this forearc subsurface biosphere could sequester 1.4 × 10 9 to 1.4 × 10 10 mol of carbon per year, which would decrease estimates of the total carbon delivered to the mantle by 2 to 22%. Furthermore, based on the observed correlations, we suggest that distribution and composition of the subsurface bacterial community are probably affected by deep tectonic processes across the Costa Rican convergent margin and that, by sequestering carbon volatilized during subduction, these chemolithoautotrophic communities could in turn impact the geosphere.

54 ENVIRONMENTAL SCIENCES↗

Wildfire-dependent changes in soil microbiome diversity and function

Abstract Forest soil microbiomes have crucial roles in carbon storage, biogeochemical cycling and rhizosphere processes. Wildfire season length, and the frequency and size of severe fires have increased owing to climate change. Fires affect ecosystem recovery and modify soil microbiomes and microbially mediated biogeochemical processes. To study wildfire-dependent changes in soil microbiomes, we characterized functional shifts in the soil microbiota (bacteria, fungi and viruses) across burn severity gradients (low, moderate and high severity) 1 yr post fire in coniferous forests in Colorado and Wyoming, USA. We found severity-dependent increases of Actinobacteria encoding genes for heat resistance, fast growth, and pyrogenic carbon utilization that might enhance post-fire survival. We report that increased burn severity led to the loss of ectomycorrhizal fungi and less tolerant microbial taxa. Viruses remained active in post-fire soils and probably influenced carbon cycling and biogeochemistry via turnover of biomass and ecosystem-relevant auxiliary metabolic genes. Our genome-resolved analyses link post-fire soil microbial taxonomy to functions and reveal the complexity of post-fire soil microbiome activity.

59 BASIC BIOLOGICAL SCIENCES↗

Hyperactive nanobacteria with host-dependent traits pervade Omnitrophota

Abstract Candidate bacterial phylum Omnitrophota has not been isolated and is poorly understood. We analysed 72 newly sequenced and 349 existing Omnitrophota genomes representing 6 classes and 276 species, along with Earth Microbiome Project data to evaluate habitat, metabolic traits and lifestyles. We applied fluorescence-activated cell sorting and differential size filtration, and showed that most Omnitrophota are ultra-small (~0.2 μm) cells that are found in water, sediments and soils. Omnitrophota genomes in 6 classes are reduced, but maintain major biosynthetic and energy conservation pathways, including acetogenesis (with or without the Wood-Ljungdahl pathway) and diverse respirations. At least 64% of Omnitrophota genomes encode gene clusters typical of bacterial symbionts, suggesting host-associated lifestyles. We repurposed quantitative stable-isotope probing data from soils dominated by andesite, basalt or granite weathering and identified 3 families with high isotope uptake consistent with obligate bacterial predators. We propose that most Omnitrophota inhabit various ecosystems as predators or parasites.

59 BASIC BIOLOGICAL SCIENCES↗

Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest

Drought impacts on microbial activity can alter soil carbon fate and lead to the loss of stored carbon to the atmosphere as CO 2 and volatile organic compounds (VOCs). Here we examined drought impacts on carbon allocation by soil microbes in the Biosphere 2 artificial tropical rainforest by tracking 13 C from position-specific 13 C-pyruvate into CO 2 and VOCs in parallel with multi-omics. During drought, efflux of 13 C-enriched acetate, acetone and C 4 H 6 O 2 (diacetyl) increased. These changes represent increased production and buildup of intermediate metabolites driven by decreased carbon cycling efficiency. Simultaneously, 13 C-CO 2 efflux decreased, driven by a decrease in microbial activity. However, the microbial carbon allocation to energy gain relative to biosynthesis was unchanged, signifying maintained energy demand for biosynthesis of VOCs and other drought-stress-induced pathways. Overall, while carbon loss to the atmosphere via CO 2 decreased during drought, carbon loss via efflux of VOCs increased, indicating microbially induced shifts in soil carbon fate.

59 BASIC BIOLOGICAL SCIENCES↗

Life history strategies of soil bacterial communities across global terrestrial biomes

The life history strategies of soil microbes determine their metabolic potential and their response to environmental changes. Yet these strategies remain poorly understood. Here we use shotgun metagenomes from terrestrial biomes to characterize overarching covariations of the genomic traits that capture dominant life history strategies in bacterial communities. The emerging patterns show a triangle of life history strategies shaped by two trait dimensions, supporting previous theoretical and isolate-based studies. The first dimension ranges from streamlined genomes with simple metabolisms to larger genomes and expanded metabolic capacities. As metabolic capacities expand, bacterial communities increasingly differentiate along a second dimension that reflects a trade-off between increasing capacities for environmental responsiveness or for nutrient recycling. Random forest analyses show that soil pH, C:N ratio and precipitation patterns together drive the dominant life history strategy of soil bacterial communities and their biogeographic distribution. Finally, our findings provide a trait-based framework to compare life history strategies of soil bacteria.

59 BASIC BIOLOGICAL SCIENCES↗

Predictions of rhizosphere microbiome dynamics with a genome-informed and trait-based energy budget model

Abstract Soil microbiomes are highly diverse, and to improve their representation in biogeochemical models, microbial genome data can be leveraged to infer key functional traits. By integrating genome-inferred traits into a theory-based hierarchical framework, emergent behaviour arising from interactions of individual traits can be predicted. Here we combine theory-driven predictions of substrate uptake kinetics with a genome-informed trait-based dynamic energy budget model to predict emergent life-history traits and trade-offs in soil bacteria. When applied to a plant microbiome system, the model accurately predicted distinct substrate-acquisition strategies that aligned with observations, uncovering resource-dependent trade-offs between microbial growth rate and efficiency. For instance, inherently slower-growing microorganisms, favoured by organic acid exudation at later plant growth stages, exhibited enhanced carbon use efficiency (yield) without sacrificing growth rate (power). This insight has implications for retaining plant root-derived carbon in soils and highlights the power of data-driven, trait-based approaches for improving microbial representation in biogeochemical models.

59 BASIC BIOLOGICAL SCIENCES↗

$\mathrm{COBRA}$ improves the completeness and contiguity of viral genomes assembled from metagenomes

Viruses are often studied using metagenome-assembled sequences, but genome incompleteness hampers comprehensive and accurate analyses. Contig Overlap Based Re-Assembly (COBRA) resolves assembly breakpoints based on the de Bruijn graph and joins contigs. Here we benchmarked COBRA using ocean and soil viral datasets. COBRA accurately joined the assembled sequences and achieved notably higher genome accuracy than binning tools. From 231 published freshwater metagenomes, we obtained 7,334 bacteriophage clusters, ~83% of which represent new phage species. Notably, ~70% of these were circular, compared with 34% before COBRA analyses. We expanded sampling of huge phages (≥200 kbp), the largest of which was curated to completion (717 kbp). Improved phage genomes from Rotsee Lake provided context for metatranscriptomic data and indicated the in situ activity of huge phages, whiB-encoding phages and cysC- and cysH-encoding phages. COBRA improves viral genome assembly contiguity and completeness, thus the accuracy and reliability of analyses of gene content, diversity and evolution.

54 ENVIRONMENTAL SCIENCES↗

A global atlas of soil viruses reveals unexplored biodiversity and potential biogeochemical impacts

Historically neglected by microbial ecologists, soil viruses are now thought to be critical to global biogeochemical cycles. However, our understanding of their global distribution, activities and interactions with the soil microbiome remains limited. Here we present the Global Soil Virus Atlas, a comprehensive dataset compiled from 2,953 previously sequenced soil metagenomes and composed of 616,935 uncultivated viral genomes and 38,508 unique viral operational taxonomic units. Rarefaction curves from the Global Soil Virus Atlas indicate that most soil viral diversity remains unexplored, further underscored by high spatial turnover and low rates of shared viral operational taxonomic units across samples. By examining genes associated with biogeochemical functions, we also demonstrate the viral potential to impact soil carbon and nutrient cycling. This study represents an extensive characterization of soil viral diversity and provides a foundation for developing testable hypotheses regarding the role of the virosphere in the soil microbiome and global biogeochemistry.

59 BASIC BIOLOGICAL SCIENCES↗

A call for caution in the biological interpretation of viral auxiliary metabolic genes

Virus-encoded auxiliary metabolic genes (AMGs) are non-essential genes that increase viral fitness by maintaining or manipulating host metabolism during infection. AMGs are intriguing from an evolutionary perspective, as most viral genomes are highly compact and have limited coding capacity for accessory genes. Advances in viral (meta)genomics have expanded the detection of putative AMGs from viruses in diverse environments. However, this has also led to many instances of misannotation due to the limitations of annotation tools, resulting in misinterpretations about the roles of some viral genes. Here, we highlight studies that support claims about AMGs with more than just function predictions for guidance on best practices. We then propose the adoption of an expanded, inclusive view of all genes auxiliary to core viral functions with the term ‘auxiliary viral genes’ (AVGs), alongside an associated eco-evolutionary framework for considering the types of analyses that can better support claims made about AVGs.

Environmental microbiology↗