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Trubl, G.

Publications and source records attributed to Trubl, G..

9 recordsLinked to original sources

Microbial communities in tropical soils are highly resilient to fluctuating redox conditions

Many wet tropical soils alternate frequently between fully oxygenated and anaerobic conditions, constraining the terminal electron acceptors available for microbial metabolism, and the mineral-organic matter interactions that regulate many aspects of soil carbon (C) cycling. However, it is still unclear how fluctuating soil redox conditions influence the microbial community composition and if microbially mediated C flux is sensitive to extended oxic or anoxic periods like those observed during drought and flooding respectively. Using a 44-day redox manipulation of tropical soils that experience daily-to-weekly oxygen (O2) fluctuations in the field, we measured how different redox regimes shape soil biogeochemistry and microbial and metabolite composition. Replicate microcosms were exposed to four treatments (static oxic, static anoxic, high frequency fluctuation (4 day oxic/4 day anoxic), or low frequency fluctuation (8 day oxic/4 day anoxic)) regimes, and harvested for microbial, metabolite, carbon dioxide (CO2) flux, and biogeochemical assays at multiple timepoints. Oxic and fluctuating redox conditions caused the microbial community to shift in a manner correlated with soil iron content and directly orthogonal to communities from anoxic soils. The identity of both iron oxidizers and iron reducers was distinct in static anoxic soils but was resilient to redox fluctuation and prolonged O2 exposure. The total amount of CO2 respired was similar across all four redox regimes. Water-extractable organic matter composition was distinct across redox treatments, with anoxic soils accumulating higher levels of carbohydrate-, proteins-, amino sugar-, and lignin-like compounds consistent with reduced enzymatic decomposition and release of mineral-associated organic matter via iron reduction, while oxic soils showed elevated lipid- and unsaturated hydrocarbon-like compounds indicative of greater microbial biomass turnover. The microbial community adapted to dynamic redox conditions and the results substantiate cycling of distinct C compounds under varying redox conditions resulting from varying bioavailability (driven by mineral-OM dynamics) and/or shifted microbial metabolism.

microbiology↗

Divergent successional patterns and infection dynamics in virion and transcriptionally active soil viral communities following phosphorus amendment and wet-up

Viruses are key regulators of terrestrial carbon, nitrogen, and phosphorus cycling, yet how environmental perturbations structure viral activity remains poorly resolved. Rewetting of seasonally dry soils triggers rapid microbial and viral responses, but the relationships between virion-associated and transcriptionally active viral communities, and the role of phosphorus in these dynamics, remain unclear. Here, we integrated viromics, metatranscriptomics, environmental DNA (eDNA), and amplicon sequencing to track viral succession and virus-host interactions over three weeks following soil rewetting, with and without phosphorus amendment. We identified 13,840 viral populations (vOTUs), of which 3,803 were transcriptionally active, representing ongoing infections. Wet-up significantly altered virion and transcriptionally active viral communities, while phosphorus selectively influenced prokaryotic and transcriptionally active viral communities but not virion composition. Virus-host linkages were predicted for 32% of vOTUs, with transcriptionally active bacteriophages infecting Actinomycetota increasing under phosphorus amendment. Following wet-up, virion abundance decreased [~]3-fold while virocells increased [~]5-fold, indicating a shift from viral persistence in dry soils to active infection. Phosphorus further enhanced virocell abundance. eDNA captured rapid viral turnover and revealed transient dynamics not resolved by viromes or metatranscriptomes alone. Together, these results demonstrate that soil viral communities are structured by distinct but complementary molecular pools that operate over different ecological timescales. Wet-up activates a reservoir of persistent virions, while phosphorus availability regulates infection dynamics and host-virus coupling. These findings highlight viruses as dynamic drivers of microbial turnover and nutrient cycling following environmental perturbation, advancing a more predictive understanding of soil ecosystem responses to changing resource availability.

ecology↗

Tracking Persistence and Dynamics of Active Soil Viruses with SIP-Viromics

Viruses are abundant and ecologically important in soils, yet the persistence and production dynamics of extracellular virions remain poorly understood. We applied a genome-resolved stable isotope probing viromics (SIP-viromics) approach, combining H 18O labeling with viral metagenomics, to track virion turnover in seasonally dry grassland soils following rewetting. We identified 354 viral populations (vOTUs) using individual-sample and combined metagenome assemblies. Only 22% of vOTUs exhibited significant 18O enrichment, indicating active replication and new virion production during the 1-week incubation; the majority (78%) persisted without detectable replication, consistent with a viral seed bank. Active vOTUs accounted for 4.76-5.15% of total virions per gram of soil, with viral loads ranging from 3.15 x 1010 to 6.59 x 1010 virions per gram. Probabilistic and deterministic sensitivity analyses spanning viral DNA fraction and genome length reinforced that persistent virions represented the majority of the extracellular viral pool post-wet-up, regardless of parameter assumptions. Host predictions linked both active and persistent vOTUs primarily to Actinomycetota and Pseudomonadota--bacterial groups known to rapidly resuscitate following rewetting--suggesting that some viruses exhibit rapid turnover while others persist over longer timescales, forming a stable viral pool capable of reinitiating infections during favorable conditions. These results demonstrate that SIP-viromics can distinguish newly produced from persistent virions and reveal host-associated patterns of lytic infection and virion production. Our findings advance understanding of soil virus-host interactions and highlight the ecological role of persistent virions as a genetic reservoir contributing to microbial turnover and biogeochemical cycling following environmental disturbance. ImportanceUnderstanding the persistence and production dynamics of soil viruses is critical for elucidating their roles in microbial community dynamics and nutrient cycling, yet these processes have remained largely uncharacterized due to methodological limitations. By integrating stable isotope probing with viromics, this study provides a robust framework for directly distinguishing newly produced from persistent virions in situ. Unlike conventional viromics, which only catalogs viral diversity, SIP-viromics enables quantification of active viral replication and persistence under natural soil conditions. Our results demonstrate that most virions in a seasonally dry soil persisted through a rewetting event, with active replication limited to a minority of viral populations. Persistent virions were primarily linked to dominant bacterial groups, indicating that host ecophysiology and environmental stability strongly influence lytic infection. Collectively, these findings highlight viruses as long-term reservoirs of genetic material, capable of shaping microbial dynamics and ecosystem processes over time. This work establishes SIP-viromics as a powerful approach for studying virus-host interactions and their ecological significance in terrestrial environments.

microbiology↗

Virus-mediated recycling of chemoautotrophic biomass

Aquatic environments absorb [~]2.5 gigatonnes of atmospheric carbon each year1, more than the carbon stored in the atmosphere, soils, and all biomass combined. Primary producers transform this dissolved inorganic carbon into biomass that can subsequently flow into other trophic levels, or be released back into the environment through viral lysis. While there is substantial knowledge about the diversity and activity of viruses infecting photoautotrophic primary producers, little is known about viruses infecting chemoautotrophs, representing a gap in our understanding of key microbial processes driving global carbon cycles. Here, we combine metagenomics with 12/13C stable isotopic probing mesocosm experiments in a marine-derived meromictic pond to quantify lineage-specific carbon cycling activity to identify key microbial populations driving carbon cycling. We then tracked the flow of carbon from active chemoautotrophs to their viruses and found evidence supporting virus-mediated recycling of chemoautotrophic biomass through the production of viral particles. In particular, active populations of hydrogen/sulfur-oxidizing chemoautotrophs (Thiomicrorhabdus, Hydrogenovibrio, Sulfurimonas, Sulfurovum) were targeted by viruses. Considering the widespread distribution of chemoautotrophs on Earth, we postulate that this previously overlooked component of the microbial carbon cycle is a globally relevant process that has implications for our planets carbon cycle. This work provides the foundation for revealing the role of viral lysis in chemoautotrophic primary production and builds toward biogeochemical models that incorporate viral recycling of chemoautotrophic biomass. Summary statementThe diversity, mechanisms, and processes governing microbial primary production and the recycling of autotrophic biomass are fundamental to our planets carbon cycle. These processes have implications for carbon sequestration, ocean biogeochemistry, and the overall balance of carbon dioxide in the atmosphere. Beneath the Earths sunlit layer, primary production is driven by microbial chemoautotrophs that derive energy from the oxidation of reduced compounds, such as hydrogen and sulfur, to form the base of the food web. Growing evidence suggests that aquatic ecosystems fueled by chemoautotrophy are widely distributed on Earth, ranging from beneath ice shelves to coastal upwelling regions to oxygen minimum zones, deep-sea hydrothermal vents and cold seeps, groundwater, and meromictic ponds and lakes2-7. Studying microbial processes regulating chemoautotrophic primary production and the recycling of chemoautotrophic biomass is fundamental to our understanding of global carbon cycles. While the diversity, function, and activity of viruses targeting photoautotrophs have been well-described across aquatic ecosystems8, we have little understanding of viruses involved in the recycling of chemoautotrophic biomass. Viruses are a major source of cellular mortality and carbon cycling in aquatic environments9-11. Viral lysis is estimated to transform [~]150 gigatonnes of carbon annually from biomass back into the environment, equivalent to [~]25 times that of the oceans biological carbon pump12,13. Despite recognition of the important role of viruses in aquatic habitats, there is a large gap in our understanding of the impact of viruses on globally distributed chemoautotrophs2,4,5,14-18. In this study, we show that viruses are not merely passive players but active agents recycling carbon fixed by productive chemoautotrophs, fundamentally reshaping how we view carbon and nutrient cycling in redox-active ecosystems.

microbiology↗

Phosphate amendment drives bloom of RNA viruses after soil wet-up

Soil rewetting after a dry period results in a surge of activity and succession in both microbial and DNA virus communities. Less is known about the response of RNA viruses to soil rewetting--while they are highly diverse and widely distributed in soil, they remain understudied. We hypothesized that RNA viruses would show temporal succession following rewetting and that phosphate amendment would influence their trajectory, as viral proliferation may cause phosphorus limitation. Using 39 time-resolved metatranscriptomes and amplicon data, 2,190 RNA viral populations were identified across five phyla, with 37% of these predicted to infect bacteria (26%) or fungi (11%). Only 1.2% of viral populations had annotated capsid genes, suggesting most persist via intracellular replication without a free virion phase. Phosphate amendment altered RNA viral community composition within the first week and amended vs. unamended communities remained distinguishable for up to three weeks. While the overall host community remained stable, certain bacterial populations showed reduced abundance in phosphate-amended soils, likely due to increased viral lysis, as RNA bacteriophages, particularly Leviviricetes, proliferated significantly. Notably, 60% of the viruses with increased abundance under phosphate amendment belonged to basal Lenarviricota clades rather than well-known groups like Leviviricetes. We estimate RNA bacteriophage infections may affect 107-109 bacteria per gram of soil, aligning with the total bacterial population (107-1010 g-1 soil), suggesting that RNA phages significantly influence bacterial communities post-wet-up, with phosphorus availability modulating this effect. HighlightsO_LISoil wet-up influences RNA virus dynamics for over a week C_LIO_LIThe majority of hosts predicted for RNA viruses were bacteria and fungi C_LIO_LIPhosphate amendment preferentially supports Lenarviricota over other RNA viruses C_LIO_LI60% of vOTUs that responded to phosphate were from unknown bacteriophage clades C_LIO_LIMost soil bacteria are predicted to be infected by RNA bacteriophages within a week C_LI

microbiology↗

Soil redox drives virus-host community dynamics and plant biomass degradation in tropical rainforest soils

BackgroundWet tropical forest soils store a vast amount of organic carbon and cycle over a third of terrestrial net primary production. The microbiomes of these soils have a global impact on greenhouse gases and tolerate a remarkably dynamic redox environment--driven by high availability of reductant, high soil moisture, and fine-textured soils that limit oxygen diffusion. Yet tropical soil microbiomes, particularly virus-host interactions, remain poorly characterized, and we have little understanding of how they will shape future soil carbon cycling as high-intensity drought and precipitation events make soil redox conditions less predictable. ResultsTo investigate the effects of shifting soil redox conditions on active viral communities and virus-microbe interactions, we conducted a 44-day redox manipulation experiment using soils from the Luquillo Experimental Forest, Puerto Rico, amended with 13C-enriched plant biomass. We sequenced 10 bulk metagenomes and 85 stable isotope probing targeted metagenomes generated by extracting whole community DNA, performing density fractionation, and conducting shotgun sequencing. Viral and microbial genomes were assembled resulting in 5,420 viral populations (vOTUs) and 927 medium-to-high-quality metagenome-assembled genomes across 25 bacterial phyla. Notably, over half (54%) of the vOTUs were 13C-enriched, highlighting their active role in microbial degradation of plant litter. These active vOTUs primarily infected bacterial phyla Pseudomonadota, Acidobacteriota, and Actinomycetota, and 57% were unique to a particular redox treatment. The anoxic samples exhibited the most distinct viral communities, with an increased potential for modulating host metabolism by carrying redox-specific glycoside hydrolases. However, over a third of the vOTUs were present in all redox conditions, suggesting selection for cosmopolitan viruses occurs in these soils that naturally experience dynamic redox conditions. ConclusionsOur study demonstrates how redox conditions shape viral communities and virus-host interactions in soils. By applying different DNA assembly methods on stable isotope probing targeted metagenomes and incubating soils under various redox regimes, we identified distinct viral populations and observed significant variations in viral community composition and function. These findings highlight the specialized roles of viruses in microbial carbon degradation under diverse environmental conditions, providing important insights into their contributions to carbon cycling and the broader implications for climate change.

microbiology↗

Population ecology and potential biogeochemical impacts of ssDNA and dsDNA soil viruses along a permafrost thaw gradient

Climate change is disproportionately warming northern peatlands, which may release large carbon stores via increased microbial activity. While there are many unknowns about such microbial responses, virus roles are especially poorly characterized with studies to date largely restricted to "bycatch" from bulk metagenomes. Here, we used optimized viral particle purification techniques on 20 samples along a highly contextualized peatland permafrost thaw gradient, extracted and sequenced viral particle DNA using two library kits to capture single-stranded (ssDNA) and double-stranded (dsDNA) virus genomes (40 total viromes), and explored their diversity and potential ecosystem impacts. Both kits recovered similar dsDNA virus numbers, but only one also captured thousands of ssDNA viruses. Combining these data, we explored population-level ecology using genomic representation from 9,560 viral operational taxonomic units (vOTUs); nearly a 4-fold expansion from permafrost-associated soils, and 97% of which were novel when compared against large datasets from soils, oceans, and the human gut. In silico predictions identified putative hosts for 44% (4,149 dsDNA + 17 ssDNA) of the identified vOTUs spanning 2 eukaryotic, 12 archaeal, and 30 bacterial phyla. The recovered vOTUs encoded 1,684 putative auxiliary metabolic genes (AMGs) and other metabolic genes carried by [~]10% of detected vOTUs, of which 46% were related to carbon processing and 644 were novel. These AMGs grouped into five functional categories and 11 subcategories, and nearly half (47%) of the AMGs were involved in carbon utilization. Of these, 112 vOTUs encoded 123 glycoside hydrolases spanning 15 types involved in the degradation of polysaccharides (e.g., cellulose) to monosaccharides (e.g., galactose), or further monosaccharide degradation, which suggests virus involvement in myriad metabolisms including fermentation and central carbon metabolism. These findings expand the scope of viral roles in microbial carbon processing and suggest viruses may be critical for understanding the fate of soil organic carbon in peatlands.

microbiology↗

Active viral population dynamics in frozen Arctic peat soil revealed with H218O stable isotope probing metagenomics

Winter carbon loss in northern ecosystems is estimated to be greater than the average growing season carbon uptake. However, most ecosystem carbon measurements neglect winter months since carbon losses (primarily driven by microbial decomposers) are assumed to be negligible at low temperatures. We used stable isotope probing (SIP) targeted metagenomics to reveal the genomic potential of active soil microbial populations under winter conditions, with an emphasis on viruses and virus-host dynamics. Peat soils from the Bonanza Creek LTER site in Alaska were incubated under subzero anoxic conditions with H218O for 184 and 370 days. We identified 46 bacterial populations (MAGs; spanning 9 bacterial phyla) and 243 viral populations (vOTUs) that actively took up 18O and produced significant CO2 throughout the incubation. Active hosts, predicted for 33% of the active vOTUs, were some of the most abundant MAGs and capable of fermentation and organic matter degradation. Approximately three-quarters of the active vOTUs carried auxiliary metabolic genes that spanned five functional categories, including carbon utilization, highlighting the potential impact of viruses in this peat soils microbial biogeochemistry. These results illustrate significant bacterial and viral activity and interactions occur in frozen soils, revealing viruses are a major community-structuring agent throughout winter months.

microbiology↗

Soil viruses are underexplored players in ecosystem carbon processing

Rapidly thawing permafrost harbors ~30-50% of global soil carbon, and the fate of this carbon remains unknown. Microorganisms will play a central role in its fate, and their viruses could modulate that impact via induced mortality and metabolic controls. Because of the challenges of recovering viruses from soils, little is known about soil viruses or their role(s) in microbial biogeochemical cycling. Here, we describe 53 viral populations (vOTUs) recovered from seven quantitatively-derived (i.e. not multiple-displacement-amplified) viral-particle metagenomes (viromes) along a permafrost thaw gradient. Only 15% of these vOTUs had genetic similarity to publicly available viruses in the RefSeq database, and ~30% of the genes could be annotated, supporting the concept of soils as reservoirs of substantial undescribed viral genetic diversity. The vOTUs exhibited distinct ecology, with dramatically different distributions along the thaw gradient habitats, and a shift from soil-virus-like assemblages in the dry palsas to aquatic-virus-like in the inundated fen. Seventeen vOTUs were linked to microbial hosts (in silico), implicating viruses in infecting abundant microbial lineages from Acidobacteria, Verrucomicrobia, and Deltaproteoacteria, including those encoding key biogeochemical functions such as organic matter degradation. Thirty-one auxiliary metabolic genes (AMGs) were identified, and suggested viral-mediated modulation of central carbon metabolism, soil organic matter degradation, polysaccharide-binding, and regulation of sporulation. Together these findings suggest that these soil viruses have distinct ecology, impact host-mediated biogeochemistry, and likely impact ecosystem function in the rapidly changing Arctic.

microbiology↗