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Nuccio, E. E.

Publications and source records attributed to Nuccio, E. E..

16 recordsLinked to original sources

Assessing the Potential of Switchgrass (Panicum virgatum L.) for Storing Carbon Belowground: Insights from a Multi-Site US Study

Agricultural intensification depletes belowground carbon (C) stocks, partly due to the exclusion of deep-rooted perennial species from landscapes where they were once dominant. Reintroducing deep-rooted perennials to cultivated land may help to mitigate SOC loss and restore ecosystem function. We quantified the effect of replacing shallow-rooted annual crops with a deep-rooted perennial grass, switchgrass (Panicum virgatum L.), by comparing 10 to 30 year-old switchgrass stands with paired annual row crop fields across the central and eastern USA. We hypothesized that switchgrass would store more root C and SOC than neighboring shallow-rooted annual crops, and that these effects would extend deeper than 30 cm. We also evaluated whether switchgrass stimulates decomposition of SOC at depth using radiocarbon (14C) to quantify replacement of slow cycling isotopically depleted SOC. Finally, we explored whether the effect of switchgrass on SOC is moderated by soil chemical and physical properties. While the effect of switchgrass on SOC in the surface 100 cm was positive at most sites, the average effect was highly uncertain and statistically indistinguishable from zero (mean difference in SOC = 0.6 kg C m-2 [95% CI -0.8 to +1.9 kg C m-2]). By contrast, we found that root biomass C was consistently more deeply distributed and more abundant under switchgrass, yielding an estimated additional 0.6 kg C m-2 in the surface 100 cm of soil under switchgrass [95% CI +0.5 to +0.7 kg C m-2]. 14C measurements suggested that root C inputs were adding to existing SOC without stimulating decomposition. The effect of switchgrass on belowground C was not strongly related to any of the environmental factors that we evaluated. Our observations show that root biomass C can contribute substantially to belowground C stocks when deep-rooted perennial grasses replace shallow-rooted annual crops.

ecology↗

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↗

Arbuscular mycorrhiza convey significant plant carbon to a diverse hyphosphere microbial food web and mineral-associated organic matter

O_LIArbuscular mycorrhizal fungi (AMF) transport substantial plant carbon (C) that serves as a substrate for other soil organisms, a precursor of soil organic matter (SOM), and a driver of soil microbial dynamics. Using two-chamber microcosms where an air gap isolated AMF from roots, we 13CO2-labeled Avena barbata for six weeks and measured. the C Rhizophagus intraradices transferred to SOM and hyphosphere microorganisms. C_LIO_LINanoSIMS imaging, IRMS, 13C NMR, and SOM density fractionation showed hyphae and roots had similar 13C enrichment. AMF transferred 0.77 mg C per g of soil (increasing total C by 2%); 33% was found in occluded or mineral-associated pools, primarily as carbohydrates. C_LIO_LIIn the AMF hyphosphere, there was no overall change in community diversity but 36 bacterial ASVs significantly changed in relative abundance. With stable isotope probing (SIP)-enabled shotgun sequencing, we found taxa from the Solibacterales, Sphingobacteriales, Myxococcales and Nitrososphaerales (ammonium oxidizing archaea) were highly enriched in AMF-imported 13C (>20 atom%). Mapping 13C-enriched metagenome-assembled genomes to total ASVs showed at least 92 bacteria and archaea were significantly 13C-enriched. C_LIO_LIOur results illustrate the quantitative impact of hyphal C transport on the formation of potentially protective SOM pools and indicate microbial roles in the AMF hyphosphere soil food web. C_LI

microbiology↗

Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development

Interactions between plant roots and rhizosphere bacteria mediate nitrogen (N)-cycling processes and create habitats rich in low molecular weight (growing roots, rhizosphere) and complex organic molecules (decaying root litter, detritusphere) compared to bulk soil. Microbial N-cycling is regulated by a diverse suite of genes from many interconnected metabolic pathways; but most studies of soil N-cycling gene expression have focused on single pathways. Currently, we lack a comprehensive understanding of the interplay between soil N-cycling gene regulation, spatial habitat and time. Here we present an analysis of a replicated time series of soil metatranscriptomes; we followed multiple N transformations in four soil habitats (rhizosphere, detritusphere, mixed rhizo-/detriusphere, bulk soil) over a period of active root growth for the annual grass, Avena fatua. The presence of root litter and living roots significantly altered the trajectory of N-cycling gene expression. Across soil habitats, the most highly expressed N-transformation genes were related to extracellular proteases, ammonium assimilation into microbial biomass via glutamate synthase, and ammonium oxidation. Upregulation of bacterial assimilatory nitrate reduction in the rhizosphere suggests that rhizosphere bacteria were actively competing with roots for nitrate. Simultaneously, bacterial ammonium assimilatory pathways were upregulated in both rhizosphere and detritusphere soil, which could have limited N availability to plants. The detritusphere supported dissimilatory processes DNRA and denitrification. Expression of ammonium oxidation genes was almost exclusively performed by three phylotypes of Thaumarchaeota and was upregulated in unamended bulk soil. Unidirectional ammonium assimilation and its regulatory genes (glutamine synthetase/glutamate synthase, or GS/GOGAT) were upregulated in soil surrounding relatively young roots and more highly decayed root litter, suggesting N may have been limiting in these habitats (the GS/GOGAT pathway is known to be activated under low N availability). We did not detect expression of N-fixation or anammox genes. Our comprehensive metatranscriptomic time-series of organic and inorganic N-cycling in rhizosphere, detritusphere, and bulk soil, indicates that differences in C and inorganic N availability control contemporaneous transcription of N-cycling pathways in soil microhabitats that exist in close spatial proximity. Contribution to the fieldPlant roots modulate microbial nitrogen cycling by regulating the supply of root-derived carbon and nitrogen uptake. These differences in resource availability cause distinct micro-habitats to develop: soil near living roots (rhizosphere), decaying roots (detritusphere), near both (rhizo/detritusphere), or outside the direct influence of roots (bulk). While many genes control the microbial processes involved in the nitrogen cycle, most research has focused on single genes and pathways, neglecting the interactive effects these pathways have on each other. The processes controlled by these pathways determine consumption and production of N by soil microorganisms. We followed the expression of N-cycling genes in the primary four soil microhabitats over a period of active root growth for an annual grass. We found that the presence of root litter and living roots significantly altered gene expression involving in multiple nitrogen pathways. We also found populations with genes for multiple pathways, where expression was likely shaped by available forms of carbon and by competition with plants for inorganic nitrogen. Phylogenetic differences in spatial and temporal expression of the soil microbial N-pathway genes ultimately regulate N-availability to plants.

ecology↗

HT-SIP: A semi-automated Stable Isotope Probing pipeline identifies interactions in the hyphosphere of arbuscular mycorrhizal fungi

BackgroundLinking the identity of wild microbes with their ecophysiological traits and environmental functions is a key ambition for microbial ecologists. Of many techniques that strive to meet this goal, Stable Isotope Probing--SIP--remains the most comprehensive for studying whole microbial communities in situ. In DNA-SIP, active microorganisms that take up an isotopically heavy substrate build heavier DNA, which can be partitioned by density into multiple fractions and sequenced. However, SIP is relatively low throughput and requires significant hands-on labor. We designed and tested a semi-automated DNA-SIP pipeline to support well-replicated, temporally-resolved amplicon or metagenomics experiments that enable studies of dynamic microbial communities over space and time. To test this pipeline, we assembled SIP-metagenome assembled genomes (MAGs) from the hyphosphere zone surrounding arbuscular mycorrhizal fungi (AMF), in combination with a 13CO2 plant labelling study. ResultsOur semi-automated pipeline for DNA fractionation, cleanup, and nucleic acid quantification of SIP density gradients requires six times less hands-on labor compared to manual SIP and allows 16 samples to be processed simultaneously. Automated density fractionation increased the reproducibility of SIP gradients and reduced variation compared to manual fractionation, and we show adding a non-ionic detergent to the gradient buffer improved SIP DNA recovery. We then tested this pipeline on samples from a highly-constrained soil microhabitat with significant ecological importance, the AMF fungal hyphosphere. Processing via our quantitative SIP pipeline confirmed the AMF Rhizophagus intraradices and its associated microbiome were highly 13C enriched, even though the soils overall enrichment was only 1.8 atom% 13C. We assembled 212 13C-enriched hyphosphere MAGs, and the hyphosphere taxa that assimilated the most AMF-derived 13C (range 10-33 atom%) were from the phlya Myxococcota, Fibrobacterota, Verrucomicrobiota, and the ammonia oxidizing archaeon genus Nitrososphaeara. ConclusionsOur semi-automated SIP approach decreases operator time and errors and improves reproducibility by targeting the most labor-intensive steps of SIP--fraction collection and cleanup. Here, we illustrate this approach in a unique and understudied soil microhabitat--generating MAGs of active microbes living in the AMF hyphosphere (without plant roots). Their phylogenetic composition and gene content suggest predation, decomposition, and ammonia oxidation may be key processes in hyphosphere nutrient cycling.

microbiology↗

Quantitative stable-isotope probing (qSIP) with metagenomics links microbial physiology and activity to soil moisture in Mediterranean-climate grassland ecosystems

The growth and physiology of soil microorganisms, which play vital roles in biogeochemical cycling, are likely dependent on current and prior soil moisture levels. Here, we developed and applied a genome-resolved metagenomic implementation of quantitative stable isotope probing (qSIP) to an H218O labeling experiment to determine which microbial community members, and with what capacities, are growing under in situ conditions. qSIP enabled measurement of taxon-specific growth because isotopic incorporation into microbial DNA requires production of new genome copies. We studied three Mediterranean grassland soils across a rainfall gradient to evaluate the hypothesis that historic precipitation levels are an important factor controlling trait selection. We used qSIP-informed genome-resolved metagenomics to resolve an active subset of soil community members and identify the ecophysiological traits that characterize them. Higher year-round precipitation levels correlated with higher activity and growth rates of flagellar motile microorganisms. In addition to bacteria that were heavily isotopically labeled, we identified abundant isotope-labeled phages suggesting phage-induced cell lysis likely contributed to necromass production at all three sites. Further, there was a positive correlation between phage activity and the activity of putative phage hosts. Contrary to our expectations, the capabilities to decompose the diverse complex carbohydrates common in soil necromass or oxidize methanol and carbon monoxide were broadly distributed across active and inactive bacteria in all three soils, implying that these traits are not highly selected for by historical precipitation.

microbiology↗

Mycorrhizal fungi stabilize bacterial growth and diversity in water-limited soils

Drought disrupts soil microbial activity and many biogeochemical processes. Although plant-associated fungi can support plant performance and nutrient cycling during drought, their effects on nearby drought-exposed soil microbial communities are not well resolved. We used H 18O quantitative stable isotope probing (qSIP) and 16S rRNA gene profiling to investigate bacterial community dynamics following water limitation in the hyphospheres of two distinct fungal lineages (Rhizophagus irregularis and Serendipita bescii) grown with the bioenergy model grass Panicum hallii. In uninoculated soil, a history of water limitation resulted in significantly lower bacterial growth potential and growth efficiency, as well as lower diversity in the actively growing bacterial community. In contrast, both fungal lineages had a protective effect on hyphosphere bacterial communities exposed to water limitation: bacterial growth potential, growth efficiency, and the diversity of the actively growing bacterial community were not suppressed by a history of water limitation in soils inoculated with either fungus. Despite their similar effects at the community level, the two fungal lineages did elicit different taxon-specific responses, and bacterial growth potential was greater in R. irregularis- compared in S. bescii- inoculated soils. Several of the bacterial taxa that responded positively to fungal inocula belong to lineages that are considered drought-susceptible. Overall, H 18O qSIP highlighted treatment effects on bacterial community structure that were less pronounced using traditional 16S rRNA gene profiling. Together, these results indicate that fungal-bacterial synergies may support bacterial resilience to moisture limitation.

ecology↗

Soil depth gradients in microbial growth kinetics under deeply- vs. shallow-rooted plants

AO_SCPLOWBSTRACTC_SCPLOWClimate-smart land management practices that replace shallow-rooted annual crop systems with deeply-rooted perennial plants can contribute to soil carbon sequestration. However, deep soil carbon accrual may be influenced by active microbial biomass and their capacity to assimilate fresh carbon at depth. Incorporating active microbial biomass, dormancy and growth in microbially-explicit models can improve our ability to predict soils capacity to store carbon. But, so far, the microbial parameters that are needed for such modeling are poorly constrained, especially in deep soil layers. Here, we investigated whether a change in crop rooting depth affects microbial growth kinetics in deep soils compared to surface soils. We used a lab incubation experiment and growth kinetics model to estimate how microbial parameters vary along 240 cm of soil depth in profiles under shallow- (soy) and deeply-rooted plants (switchgrass) 11 years after plant cover conversion. We also assessed resource origin and availability (total organic carbon, 14C, dissolved organic carbon, specific UV absorbance, total nitrogen, total dissolved nitrogen) along the soil profiles to examine associations between soil chemical and biological parameters. Even though root biomass was higher and rooting depth was deeper under switchgrass than soy, resource availability and microbial growth parameters were generally similar between vegetation types. Instead, depth significantly influenced soil chemical and biological parameters. For example, resource availability, and total and relative active microbial biomass decreased with soil depth. Decreases in the relative active microbial biomass coincided with increased lag time (response time to external carbon inputs) along the soil profiles. Even at a depth of 210-240 cm, microbial communities were activated to grow by added resources within a day. Maximum specific growth rate decreased to a depth of 90 cm and then remained consistent in deeper layers. Our findings show that > 10 years of vegetation and rooting depth changes may not be long enough to alter microbial growth parameters, and suggest that at least a portion of the microbial community in deep soils can grow rapidly in response to added resources. Our study determined microbial growth parameters that can be used in microbially-explicit models to simulate carbon dynamics in deep soil layers.

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↗

Community RNA-Seq: Multi-kingdom responses to living versus decaying root inputs in soil

Roots are the primary source of organic carbon inputs to most soils. Decomposition is a multi-trophic process involving multiple kingdoms of microbial life, but typically microbial ecology studies focus on one or two major lineages in isolation. We used Illumina shotgun RNA sequencing to conduct PCR-independent SSU rRNA community analysis ("community RNA-Seq") to simultaneously study the bacteria, archaea, fungi, and microfauna surrounding both living and decomposing roots of the annual grass, Avena fatua. Plants were grown in 13CO2-labeled microcosms amended with 15N-root litter. We identified rhizosphere substrate preferences for 13C-exudates versus 15N-litter using NanoSIMS microarray imaging (Chip-SIP). When litter was available, rhizosphere and bulk soil had significantly more Amoebozoa, which are potentially important yet often overlooked top-down drivers of detritusphere community dynamics and nutrient cycling. Bulk soil containing litter was depleted in Actinobacteria but had significantly more Bacteroidetes and Proteobacteria. While Actinobacteria were abundant in the rhizosphere, Chip-SIP showed Actinobacteria preferentially incorporated litter relative to root exudates, indicating this groups more prominent role in detritus elemental cycling in the rhizosphere. Our results emphasize that decomposition is a multi-trophic process involving cross-kingdom interactions, and the trajectory of carbon through this soil food web likely impacts the fate of carbon in soil.

microbiology↗

Transcription of protease and chitinase genes provides a window onto macromolecular organic nitrogen decomposition in soil

Nitrogen (N) commonly limits terrestrial plant growth partly because most soil-N is present as macromolecular organic compounds and not directly available to plants. Soil microbes degrade these large N-containing substrates to gradually release plant-available inorganic-N throughout the growing season, potentially meeting plant demand. Knowing which microbes are responsible for release of organic N, as well as their spatiotemporal patterns of activity, can enable microbial management strategies that increase plant access to soil-N and reduce dependency on fertilizer-N. We used time-resolved metatranscriptomes to follow taxonomy-resolved differential expression of N-depolymerizing enzymes. Taxonomic groups show adaptations based on extracellular proteases to specialized habitats in soil characterized by presence (Betaproteobacteria) or absence (Thaumarcheota) of live roots and root detritus (Deltaproteobacteria and Fungi). A similar increase of eukaryotic chitinases near root detritus hints at predation of fungi. Others demonstrate temporal patterns such as increasing expression over time, implying increased competitiveness with substrate depletion (Chloroflexi). Phylotypes from the same genus can have different potential benefits to the plant based on protease expression (e.g., Janthinobacterium), which should be considered when designing bioaugmentation. We identify one Janthinobacterium phylotype and two Burkholderiales that may be candidates for bioaugmentation near young roots and a Rhizobacter which could benefit mature roots.

microbiology↗

Unexpected diversity of CPR bacteria and nanoarchaea in the rare biosphere of rhizosphere-associated grassland soil

Candidate Phyla Radiation (CPR) bacteria and nanoarchaea populate most ecosystems, but are rarely detected in soil. We concentrated particles less than 0.2 m from grassland soil, enabling targeted metagenomic analysis of these organisms, which are almost totally unexplored in soil. We recovered a diversity of CPR bacteria and some nanoarchaea sequences, but no sequences from other cellular organisms. The sampled sequences include Doudnabacteria (SM2F11) and Pacearchaeota, organisms not previously reported in soil, as well as Saccharibacteria, Parcubacteria and Microgenomates. CPR and DPANN (an acronym of the names of the first included archaea phyla) enrichments of 100-1000-fold were achieved compared to bulk soil, in which we estimate these organisms comprise about 1 to 100 cells per gram of soil. Like most CPR and DPANN sequenced to date, we predict these microorganisms live symbiotic, anaerobic lifestyles. However, Saccharibacteria, Parcubacteria, and Doudnabacteria genomes sampled here also encode ubiquinol oxidase operons that may have been acquired from other bacteria, likely during adaptation to aerobic soil environments. We posit that although present at low abundance, CPR bacteria and DPANN archaea could impact overall soil microbial community function by modulating host organism abundances and activity.

microbiology↗

Conversion of marginal land into switchgrass conditionally accrues soil carbon and reduces methane consumption

Switchgrass (Panicum virgatum L.) is a perennial C4 grass native to tallgrass prairies of the Central US, and a promising bioenergy feedstock. Switchgrass can be cultivated on soils with low nutrient contents and its rooting depth, of up to 2 m, has brought attention to the crop as a potential mechanism to sequester and build soil carbon (C). Switchgrass, therefore, offers multifaceted benefits on degraded soils by enhancing soil organic matter content. However, to evaluate the sustainability of switchgrass-based biofuel production, it is crucial to understand the impacts of land conversion and switchgrass establishment on biotic/abiotic characteristics of various soils. In this study, we characterized the ecosystem-scale consequences of switchgrass growing at two highly-eroded, Dust Bowl remnant field sites from Oklahoma US, with silt-loam (SL) or clay-loam (CL) soil textures having low nitrogen (N), phosphorus (P), and C contents. Paired plots at each site, including fallow control and switchgrass-cultivated, were assessed. Our results indicated that switchgrass significantly increased soil C at the SL site and reduced microbial diversity at the CL site. The CL site exhibited significantly higher CO2 flux and higher respiration from switchgrass plots. Strikingly, switchgrass significantly reduced the CH4 consumption by an estimated 39% for the SL site and 47% for the CL site. Structural equation modeling identified soil temperature, P content, and soil moisture levels as the most influential factors regulating both CO2 and CH4 fluxes. CO2 flux was also influenced by microbial biomass while CH4 flux was influenced by microbial diversity. Together, our results suggest that site selection by soil type is a crucial factor in improving soil C stocks and mitigating greenhouse gas (GHG) fluxes, especially considering our finding that switchgrass reduced methane consumption, implying that carbon balance considerations should be accounted for to fully evaluate the sustainability of switchgrass cultivation.

molecular biology↗

Microbial extracellular polysaccharide production and aggregate stability controlled by Switchgrass (Panicum virgatum) root biomass and soil water potential

Deep-rooting perennial grasses are promising feedstock for biofuel production, especially in marginal soils lacking organic material, nutrients, and/or that experience significant water stress. Perennial grass roots can alter surrounding soil conditions and influence microbial activities, particularly the production of extracellular polymeric substances composed primarily of extracellular polysaccharides (EPS). These polymers can alleviate cellular moisture and nutrient stress, and enhance soil characteristics through improved water retention and aggregate stability, the latter of which may in turn enhance carbon persistence. In this study we used a 13CO2 tracer greenhouse experiment to examine the effect of switchgrass cultivation on the production and origin of EPS in a marginal soil with five fertilization/water treatments (control, +N, +NP, +P, low water). Soils with both added nitrogen and phosphorus had the highest root biomass, EPS and percentage of water-stable soil aggregates. Multiple linear regression analyses revealed root biomass was the most important determinant for soil EPS production, potentially by controlling carbon supply and diurnal changes in soil water potential. Path analysis highlighted the role of soil water potential were and EPS on with water-stable soil aggregates, indicating that EPS concentration and soil aggregation have similar drivers in this soil. High mannose content confirmed the microbial origin of EPS. 13CO2 labeling indicated that 0.18% of newly fixed plant carbon was incorporated into EPS. Analysis of field samples suggests that EPS is significantly enhanced under long-term switchgrass cultivation. Our results demonstrate that switchgrass cultivation can promote microbial production of EPS, providing a mechanism to enhance sustainability of marginal soils.

microbiology↗

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↗

Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil

Viruses impact nearly all organisms on Earth, with ripples of influence in agriculture, health and biogeochemical processes. However, very little is known about RNA viruses in an environmental context, and even less is known about their diversity and ecology in the most complex microbial system, soil. Here, we assembled 48 individual metatranscriptomes from four habitats within a soil sampled over a 22-day time series: rhizosphere alone, detritosphere alone, a combination of the two, and unamended soil (four time points and three biological replicates per time point). We resolved the RNA viral community, uncovering a high diversity of viral sequences. We also investigated possible host organisms by analyzing metatranscriptome marker gene content. Based on viral phylogeny, much of the diversity was Narnaviridae that parasitize fungi or Leviviridae that infect Proteobacteria. Both host and viral communities appear to be highly dynamic, and rapidly diverged depending on experimental conditions. The viral communities were structured based on the presence of litter, while putative hosts appeared to be impacted by both the presence of litter and roots. A clear time signature from Leviviridae and their hosts indicated that viruses were replicating. With this time-resolved analysis, we show that RNA viruses are diverse, abundant and active in soil. Their replication causes host cell death, mobilizing carbon in a process that represents a largely overlooked component of carbon cycling in soil.

microbiology↗