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Tfaily, M.

Publications and source records attributed to Tfaily, M..

7 recordsLinked to original sources

Virus community response rewires methane-suppressed peat microcosm carbon metabolism

Human activities are accelerating permafrost thaw and subsequent methane emissions from increased microbial activity, prompting microbiome engineering efforts as an emissions mitigation strategy. We recently demonstrated that catechin amendment could drastically reduce methane emissions (>80%) in peat microcosms by enriching catechin-degrading prokaryotes that outcompeted methanogens for hydrogen. However, viral contributions to such microbiome-level responses remain unexplored and we hypothesized that viral dynamics could help shape the microbiome response as nutrient amendments may alter cellular physiology in ways that could induce lytic viral activity. Here, we performed virus ecogenomics analyses of the previously-studied time-resolved multi-omics data collected from catechin-amended peat microcosms. We conservatively identified 900 putatively lytic viral operational taxonomic units (vOTUs), with 41% predicted to infect active host genomes including the most transcriptionally active vOTUs predicted to infect key catechin-degrading genera (Clostridium and undescribed Bacillota JAGFXR01). Notably, a single JAGFXR01-targeting vOTU dominating the viral response (>40% of community viral transcription; 20-156-fold more abundant than its host), which we interpreted as induction resulting in intense lytic activity that could release catechin-degradation intermediates to other community members. Consistent with this, gene expression analysis revealed elevated catechin-intermediate degradation and hydrogenase signals in 34 additional polyphenol-degrading metagenome-assembled genomes. These findings support a model consistent with a viral shunt-like process that extends our previous prokaryote-centric model: viral lysis of fast-growing catechin degraders redistributes phenolic intermediates to diverse phenol-degrading taxa that sustain methane suppression via hydrogen consumption. Beyond carbon-cycling importance in this system, elucidating unintended virus-mediated responses to nutrient and prebiotic interventions will enable more predictable and effective microbiome engineering strategies across soil, ocean, and human ecosystems.

microbiology↗

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

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

microbiology↗

Northern peatland microbial networks exhibit resilience to warming and acquire electron acceptor from soil organic matter

The microbial networks that regulate belowground carbon turnover and respond to climate change drivers in peatlands are 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) extends from surface (10 cm) to 2 m deep into the peat column, with only 3.7% of genomes overlapping with other well-studied peatlands. Unexpectedly, community composition has yet to show a significant response to warming after 3 years, suggesting that metabolically diverse soil microbial networks are resilient to climate change. Surprisingly, the dominant methanogens showed 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, whichtogether with methanogen metabolic flexibility, may explain peat microbiome resilience to warming.

microbiology↗

MetaboDirect: An Analytical Pipeline for the processing of FTICR-MS-based Metabolomics Data

BackgroundMicrobiomes are now recognized as main drivers of ecosystem function ranging from the oceans and soils to humans and bioreactors. However, a grand challenge in microbiome science is to characterize and quantify the chemical currencies of organic matter (i.e. metabolites) that microbes respond to and alter. Critical to this has been the development of Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS), which has drastically increased molecular characterization of complex organic matter samples, but challenges users with hundreds of millions of data points where readily available, user-friendly, and customizable software tools are lacking. ResultsHere, we build on years of analytical experience with diverse sample types to develop MetaboDirect, an open-source, command-line based pipeline for the analysis, visualization, and presentation of metabolomics data by direct injection FTICR-MS after molecular formula assignment has been performed. When compared to all other available FTICR software, MetaboDirect is superior with respect to its compute time as it only requires a single line of code that launches a fully automated framework for the generation and visualization of a wide range of plots, with minimal coding experience required. Among the tools evaluated, MetaboDirect is also uniquely able to automatically generate biochemical transformation networks (ab initio) based on mass differences that provide a comprehensive experimental assessment of metabolite connectives within a given sample or a complex metabolic system, thereby providing important information about the nature of the samples and the set of the microbial reactions or pathways that gave rise to them. Finally, for more experienced users, MetaboDirect allows users to customize plots, outputs, and analyses. ConclusionApplication of MetaboDirect to FTICR-MS-based metabolomics datasets from a marine phage-bacterial infection experiment and a Sphagnum leachate microbiome incubation experiment showcase the exploration capabilities of the pipeline that will enable the FTICR-MS research community to evaluate and interpret their data in greater depth and in less time. It will further advance our knowledge of how microbial communities influence and are influenced by the chemical makeup of the surrounding system. Source code and Users guide of MetaboDirect are freely available through (https://github.com/Coayala/MetaboDirect) and (https://metabodirect.readthedocs.io/en/latest/) respectively.

bioinformatics↗

Plant organic matter inputs exert a strong control on soil organic matter decomposition in a thawing permafrost peatland

Peatlands are a climate critical carbon (C) reservoir that will likely become a C source under continued warming. A strong relationship between plant tissue chemistry and the soil organic matter (SOM) that fuels C gas emissions is inferred, but rarely examined at the molecular level. Here we compared Fourier transform infrared (FT-IR) spectroscopy measurements of solid phase functionalities in plants and SOM to ultra-high-resolution mass spectrometric analyses of plant and SOM water extracts across a palsa-bog-fen thaw and moisture gradient in an Arctic peatland. From these analyses we calculated the C oxidation state (NOSC), a measure which can be used to assess organic matter quality. Palsa plant extracts had the highest NOSC, indicating high quality, while extracts of Sphagnum, which dominated the bog, had the lowest NOSC. The percentage of plant compounds that are less bioavailable and accumulate in the peat, increases from palsa (25%) to fen (41%) to bog (47 %), reflecting the pattern of percent Sphagnum cover. The pattern of NOSC in the plant extracts was consistent with the high number of consumed compounds in the palsa and low number of consumed compounds in the bog. However, in the FT-IR analysis of the solid phase bog peat, carbohydrate content was high implying higher quality SOM. We explain this discrepancy as the result of low solubilization of bog SOM facilitated by the low pH in the bog which makes the solid phase carbohydrates less available to microbial decomposition. Plant-associated lignins and tannins declined in the unsaturated palsa peat indicating decomposition, but accumulated in the bog and fen peat where decomposition was presumably inhibited by the anaerobic conditions. A molecular-level comparison of the aboveground C sources and peat SOM demonstrates that climate-associated vegetation shifts in peatlands are important controls on the mechanisms underlying changing C gas emissions.

ecology↗

Differential effects of redox conditions on the decomposition of litter and soil organic matter

Soil redox conditions exert substantial influence on biogeochemical processes in terrestrial ecosystems. Humid tropical forest soils are often characterized by fluctuating redox dynamics, yet how these dynamics affect patterns in soil versus litter decomposition and associated CO2 fluxes is not well understood. We used a 13C-labeled litter addition to explicitly follow the decomposition of litter-derived vs. native soil-derived organic matter in response to four different soil redox regimes--static oxic or anoxic, and two oscillating treatments--in soil from the Luquillo Experimental Forest, Puerto Rico. We coupled this incubation experiment with high-resolution mass spectrometry to characterize the preferential decomposition of specific classes of organic molecules. CO2 production from litter and soil organic matter (SOM) showed distinctly different responses to redox manipulation. The cumulative production of SOM-derived CO2 was positively correlated with the length of soil exposure to an oxic headspace (r = 0.89, n = 20), whereas cumulative 13C-litter-derived CO2 production was not linked to oxygen availability. The CO2 production rate from litter was highest under static anoxic conditions in the first half of the incubation period, and later dropped to the lowest among all redox treatments. In the consistently anoxic soils, we observed the depletion of more oxidized water-extractable organic matter (especially amino sugars, carbohydrates, and proteins) over time, suggesting that under anaerobic conditions, microbes preferentially used more oxidized litter-derived compounds during the early stages of decomposition. Results from kinetic modeling showed that more frequent anoxic exposure limited the decomposition of a slow-cycling C pool, but not a fast-cycling pool. Overall, our results demonstrate that substrate source--freshly added litter vs. native organic matter--plays an important role in the redox sensitivity of organic matter decomposition. In soil environments that regularly experience redox fluctuations, anaerobic heterotrophs can be surprisingly effective in degrading fresh plant litter.

ecology↗

Riparian vegetation limits oxidation of thermodynamically unfavorable bound-carbon stocks along an aquatic interface

In light of increasing terrestrial carbon (C) transport across aquatic boundaries, the mechanisms governing organic carbon (OC) oxidation along terrestrial-aquatic interfaces are crucial to future climate predictions. Here, we investigate the biochemistry, metabolic pathways, and thermodynamics corresponding to OC oxidation in the Columbia River corridor using ultra-high resolution C characterization. We leverage natural vegetative differences to encompass variation in terrestrial C inputs. Our results suggest that decreases in terrestrial C deposition associated with diminished riparian vegetation induce oxidation of physically -bound OC. We also find that contrasting metabolic pathways oxidize OC in the presence and absence of vegetation and--in direct conflict with the priming concept--that inputs of water-soluble and thermodynamically favorable terrestrial OC protects bound-OC from oxidation. In both environments, the most thermodynamically favorable compounds appear to be preferentially oxidized regardless of which OC pool microbiomes metabolize. In turn, we suggest that the extent of riparian vegetation causes sediment microbiomes to locally adapt to oxidize a particular pool of OC, but that common thermodynamic principles govern the oxidation of each pool (i.e., water-soluble or physically-bound). Finally, we propose a mechanistic conceptualization of OC oxidation along terrestrial-aquatic interfaces that can be used to model heterogeneous patterns of OC loss under changing land cover distributions.\n\nKey pointsO_LIRiparian vegetation protects bound-OC stocks\nC_LIO_LIBiochemical processes associated with OC oxidation vary with vegetation conditions\nC_LIO_LICommon thermodynamic principles underlie OC oxidation regardless of vegetation conditions\nC_LI

ecology↗