Organic carbon (OC) concentrations in subsurface sediments are typically 10 to 200 times lower than in surface soils, posing a distinct challenge for characterization. In this study, a range of chemical extractions were evaluated for extraction of natural organic matter (NOM) from two low-carbon (< 0.2%) alluvial sediments. The OC extraction efficiency followed the order pyrophosphate (PP) > NaOH > HCl, hydroxylamine hydrochloride > dithionite, water. A NOM extraction and purification scheme was developed using sequential extraction with water (MQ) and sodium pyrophosphate at pH 10 (PP), combined with purification by dialysis and solid phase extraction in order to isolate different fractions of sediment-associated NOM. Characterization of these pools of NOM for metal content and by Fourier transform infrared spectroscopy (FITR) showed that the water soluble fraction (MQ-SPE) had a higher fraction of aliphatic and carboxylic groups, while the PP-extractable NOM (PP-SPE and PP > 1kD) had higher fractions of C[dbnd]C groups and higher residual metals. This trend from aliphatic to more aromatic is also supported by the specific UV absorbance at 254 nm (SUVA254) (3.5 vs 5.4 for MQ-SPE and PP-SPE, respectively) and electrospray ionization Fourier transform ion cyclotron resonance spectrometry (ESI-FTICR-MS) data which showed a greater abundance of peaks in the low O/C and high H/C region (0–0.4 O/C, 0.8–2.0 H/C) for the MQ-SPE fraction of NOM. Radiocarbon measurements yielded standard radiocarbon ages of 1020, 3095, and 9360 years BP for PP-SPE, PP > 1kD, and residual (non-extractable) OC fractions, indicating an increase in NOM stability correlated with greater metal complexation, apparent molecular weight, and aromaticity.

Floodplains are critical terrestrial-aquatic interfaces that act as hotspots of organic carbon (OC) cycling, regulating ecosystem carbon storage as well as export to riverine systems. Within floodplain sediments, regular flooding and textural gradients interact to create dynamic redox conditions. While anaerobic protection of OC upon burial is a well-recognized carbon storage mechanism in redox-active floodplain sediments, the impact of protective mineral-organic associations is relatively unknown. Here we determined the quantitative importance and chemical composition of mineral-organic associations along well-defined redox gradients emerging from textural variations and depth within meander sediments of the subalpine East River watershed (Gothic, CO). We characterized mineral-organic associations using a combination of sequential extractions, physical fractionation, and high-resolution mass spectrometry. Across the meander, we found that mineral-associated OC constitutes a significant fraction of total OC, and that extractable iron (Fe) and aluminum (Al) phases as well as high-density isolates were strongly correlated with total OC content, suggesting that mineral-organic associations are quantitatively important for floodplain sediment OC protection. Our mass spectrometry results showed OC associated with increasingly ordered Fe and Al phases are relatively enriched in low-molecular weight, oxidized, aromatic compounds. Surprisingly, however, total OC content showed weak or no correlation with indicators of anaerobic protection, such as relatively bioavailable OC pools (water-extractable and particulate OC) or the molecular weight and oxidation state of OC. Overall, this work highlights that protection of OC bound to reactive mineral phases─in addition to anaerobic protection─can play a quantitatively important role in controlling soil carbon storage in redox-active floodplain sediments.

Organic matter decomposition in soils and terrestrial sediments has a prominent role in the global carbon cycle. Carbon stocks in anoxic environments, such as wetlands and the subsurface of floodplains, are large and presumed to decompose slowly. The degree of microbial respiration in anoxic environments is typically thought to depend on the energetics of available terminal electron acceptors such as nitrate or sulfate; microbes couple the reduction of these compounds to the oxidation of organic carbon. However, it is also possible that the energetics of the organic carbon itself can determine whether it is decomposed. Here we examined water-soluble organic carbon by Fourier-transform ion-cyclotron-resonance mass spectrometry to compare the chemical composition and average nominal oxidation state of carbon-A metric reflecting whether microbial oxidation of organic matter is thermodynamically favourable-in anoxic (sulfidic) and oxic (non-sulfidic) floodplain sediments. We observed distinct minima in the average nominal oxidation state of water-soluble carbon in sediments exhibiting anoxic, sulfate-reducing conditions, suggesting preservation of carbon compounds with nominal oxidation states below the threshold that makes microbial sulfate reduction thermodynamically favourable. We conclude that thermodynamic limitations constitute an important complement to other mechanisms of carbon preservation, such as enzymatic restrictions and mineral association, within anaerobic environments.

Oscillating redox conditions are a common feature of humid tropical forest soils, driven by an ample supply and dynamics of reductants, high moisture, microbial oxygen consumption, and finely textured clays that limit diffusion. However, the net result of variable soil redox regimes on iron (Fe) mineral dynamics and associated carbon (C) forms and fluxes is poorly understood in tropical soils. Using a 44-day redox incubation experiment with humid tropical forest soils from Puerto Rico, we examined patterns in Fe and C transformations under four redox regimes: static anoxic, "flux 4-day" (4d oxic, 4d anoxic), "flux 8-day" (8d oxic, 4d anoxic) and static oxic. Prolonged anoxia promoted reductive dissolution of Fe-oxides, and led to an increase in soluble Fe(II) and amorphous Fe oxide pools. Preferential dissolution of the less-crystalline Fe pool was evident immediately following a shift in bulk redox status (oxic to anoxic), and coincided with increased dissolved organic C, presumably due to acidification or direct release of organic matter (OM) from dissolving Fe(III) mineral phases. The average nominal oxidation state of water-soluble C was lowest under persistent anoxic conditions, suggesting that more reduced organic compounds were metabolically unavailable for microbial consumption under reducing conditions. Anoxic soil compounds had high H/C values (and were similar to lignin-like compounds) whereas oxic soil compounds had higher O/C values, akin to tannin- and cellulose-like components. Cumulative respiration derived from native soil organic C was highest in static oxic soils. These results show how Fe minerals and Fe-OM interactions in tropical soils are highly sensitive to variable redox effects. Shifting soil oxygen availability rapidly impacted exchanges between mineral-sorbed and aqueous C pools, increased the dissolved organic C pool under anoxic conditions implying that the periodicity of low-redox events may control the fate of C in wet tropical soils.

Microorganisms play vital roles in modulating organic matter decomposition and nutrient cycling in soil ecosystems. The enzyme latch paradigm posits microbial degradation of polyphenols is hindered in anoxic peat leading to polyphenol accumulation, and consequently diminished microbial activity. This model assumes that polyphenols are microbially unavailable under anoxia, a supposition that has not been thoroughly investigated in any soil type. Here, we use anoxic soil reactors amended with and without a chemically defined polyphenol to test this hypothesis, employing metabolomics and genome-resolved metaproteomics to interrogate soil microbial polyphenol metabolism. Challenging the idea that polyphenols are not bioavailable under anoxia, we provide metabolite evidence that polyphenols are depolymerized, resulting in monomer accumulation, followed by the generation of small phenolic degradation products. Further, we show that soil microbiome function is maintained, and possibly enhanced, with polyphenol addition. In summary, this study provides chemical and enzymatic evidence that some soil microbiota can degrade polyphenols under anoxia and subvert the assumed polyphenol lock on soil microbial metabolism.

Phosphorus is a scarce nutrient in many tropical ecosystems, yet how soil microbial communities cope with growth-limiting phosphorus deficiency at the gene and protein levels remains unknown. Here, we report a metagenomic and metaproteomic comparison of microbial communities in phosphorus-deficient and phosphorus-rich soils in a 17-year fertilization experiment in a tropical forest. The large-scale proteogenomics analyses provided extensive coverage of many microbial functions and taxa in the complex soil communities. A greater than fourfold increase in the gene abundance of 3-phytase was the strongest response of soil communities to phosphorus deficiency. Phytase catalyses the release of phosphate from phytate, the most recalcitrant phosphorus-containing compound in soil organic matter. Genes and proteins for the degradation of phosphorus-containing nucleic acids and phospholipids, as well as the decomposition of labile carbon and nitrogen, were also enhanced in the phosphorus-deficient soils. In contrast, microbial communities in the phosphorus-rich soils showed increased gene abundances for the degradation of recalcitrant aromatic compounds, transformation of nitrogenous compounds and assimilation of sulfur. Overall, these results demonstrate the adaptive allocation of genes and proteins in soil microbial communities in response to shifting nutrient constraints.

Peatlands are climate critical carbon (C) reservoirs that could 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, whereas 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 high 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 condensed aromatics, tannins, and lignin-like compounds declined in the unsaturated palsa peat indicating decomposition, but lignin-like compounds 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.

Background

The circadian clock regulates plant metabolic functions and is an important component in plant health and productivity. Rhizosphere bacteria play critical roles in plant growth, health, and development and are shaped primarily by soil communities. Using Illumina next-generation sequencing and high-resolution mass spectrometry, we characterized bacterial communities of wild-type (Col-0) Arabidopsis thaliana and an acyclic line (OX34) ectopically expressing the circadian clock-associated cca1 transcription factor, relative to a soil control, to determine how cycling dynamics affected the microbial community. Microbial communities associated with Brachypodium distachyon (BD21) were also evaluated.

Results

Significantly different bacterial community structures (P = 0.031) were observed in the rhizosphere of wild-type plants between light and dark cycle samples. Furthermore, 13% of the community showed cycling, with abundances of several families, including Burkholderiaceae, Rhodospirillaceae, Planctomycetaceae, and Gaiellaceae, exhibiting fluctuation in abundances relative to the light cycle. However, limited-to-no cycling was observed in the acyclic CCAox34 line or in soil controls. Significant cycling was also observed, to a lesser extent, in Brachypodium. Functional gene inference revealed that genes involved in carbohydrate metabolism were likely more abundant in near-dawn, dark samples. Additionally, the composition of organic matter in the rhizosphere showed a significant variation between dark and light cycles.

Conclusions

The results of this study suggest that the rhizosphere bacterial community is regulated, to some extent, by the circadian clock and is likely influenced by, and exerts influences, on plant metabolism and productivity. The timing of bacterial cycling in relation to that of Arabidopsis further suggests that diurnal dynamics influence plant-microbe carbon metabolism and exchange. Equally important, our results suggest that previous studies done without relevance to time of day may need to be reevaluated with regard to the impact of diurnal cycles on the rhizosphere microbial community.

Permafrost thaw is a major potential feedback source to climate change as it can drive the increased release of greenhouse gases carbon dioxide (CO₂ ) and methane (CH₄ ). This carbon release from the decomposition of thawing soil organic material can be mitigated by increased net primary productivity (NPP) caused by warming, increasing atmospheric CO₂ , and plant community transition. However, the net effect on C storage also depends on how these plant community changes alter plant litter quantity, quality, and decomposition rates. Predicting decomposition rates based on litter quality remains challenging, but a promising new way forward is to incorporate measures of the energetic favorability to soil microbes of plant biomass decomposition. We asked how the variation in one such measure, the nominal oxidation state of carbon (NOSC), interacts with changing quantities of plant material inputs to influence the net C balance of a thawing permafrost peatland. We found: (1) Plant productivity (NPP) increased post-thaw, but instead of contributing to increased standing biomass, it increased plant biomass turnover via increased litter inputs to soil; (2) Plant litter thermodynamic favorability (NOSC) and decomposition rate both increased post-thaw, despite limited changes in bulk C:N ratios; (3) these increases caused the higher NPP to cycle more rapidly through both plants and soil, contributing to higher CO₂ and CH₄  fluxes from decomposition. Thus, the increased C-storage expected from higher productivity was limited and the high global warming potential of CH₄ contributed a net positive warming effect. Although post-thaw peatlands are currently C sinks due to high NPP offsetting high CO₂ release, this status is very sensitive to the plant community's litter input rate and quality. Integration of novel bioavailability metrics based on litter chemistry, including NOSC, into studies of ecosystem dynamics, is needed to improve the understanding of controls on arctic C stocks under continued ecosystem transition.