The microbial and molecular characterization of the ectorhizosphere is an important step towards developing a more complete understanding of how the cultivation of biofuel crops can be undertaken in ...nutrient poor environments. The ectorhizosphere of Setaria is of particular interest because the plant component of this plant-microbe system is an important agricultural grain crop and a model for biofuel grasses. Importantly, Setaria lends itself to high throughput molecular studies. As such, we have identified important intra- and interspecific microbial and molecular differences in the ectorhizospheres of three geographically distant Setaria italica accessions and their wild ancestor S. viridis. All were grown in a nutrient-poor soil with and without nutrient addition. To assess the contrasting impact of nutrient deficiency observed for two S. italica accessions, we quantitatively evaluated differences in soil organic matter, microbial community, and metabolite profiles. Together, these measurements suggest that rhizosphere priming differs with Setaria accession, which comes from alterations in microbial community abundances, specifically Actinobacteria and Proteobacteria populations. When globally comparing the metabolomic response of Setaria to nutrient addition, plants produced distinctly different metabolic profiles in the leaves and roots. With nutrient addition, increases of nitrogen containing metabolites were significantly higher in plant leaves and roots along with significant increases in tyrosine derived alkaloids, serotonin, and synephrine. Glycerol was also found to be significantly increased in the leaves as well as the ectorhizosphere. These differences provide insight into how C4 grasses adapt to changing nutrient availability in soils or with contrasting fertilization schemas. Gained knowledge could then be utilized in plant enhancement and bioengineering efforts to produce plants with superior traits when grown in nutrient poor soils.
Stream and river systems transport and process substantial amounts of dissolved organic matter (DOM) from terrestrial and aquatic sources to the ocean, with global biogeochemical implications. ...However, the underlying mechanisms affecting the spatiotemporal organization of DOM composition are under-investigated. To understand the principles governing DOM composition, we leverage the recently proposed synthesis of metacommunity ecology and metabolomics, termed ‘meta-metabolome ecology.’ Applying this novel approach to a freshwater ecosystem, we demonstrated that despite similar molecular properties across metabolomes, metabolite identity significantly diverged due to environmental filtering and variations in putative biochemical transformations. We refer to this phenomenon as ‘thermodynamic redundancy,’ which is analogous to the ecological concept of functional redundancy. We suggest that under thermodynamic redundancy, divergent metabolomes can support equivalent biogeochemical function just as divergent ecological communities can support equivalent ecosystem function. As these analyses are performed in additional ecosystems, potentially generalizable concepts, like thermodynamic redundancy, can be revealed and provide insight into DOM dynamics.
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•Assemblages of metabolites were analyzed using the ‘meta-metabolome ecology’.•Surface and pore water metabolite assemblages were significantly divergent.•Divergent biochemical transformations partially drove surface/pore water differences.•Despite differences, surface and pore water have common thermodynamic properties.•We describe the phenomenon of ‘thermodynamic redundancy’.
Peatlands are among the largest natural sources of atmospheric methane (CH4) worldwide. Microbial processes play a key role in regulating CH4 emissions from peatland ecosystems, yet the complex ...interplay between soil substrates and microbial communities in controlling CH4 emissions as a function of global change remains unclear. Herein, we performed an integrated analysis of multi‐omics data sets to provide a comprehensive understanding of the molecular processes driving changes in greenhouse gas (GHG) emissions in peatland ecosystems with increasing temperature and sulfate deposition in a laboratory incubation study. We sought to first investigate how increasing temperatures (4, 21, and 35°C) impact soil microbiome–metabolome interactions; then explore the competition between methanogens and sulfate‐reducing bacteria (SRBs) with increasing sulfate concentrations at the optimum temperature for methanogenesis. Our results revealed that peat soil organic matter degradation, mediated by biotic and potentially abiotic processes, is the main driver of the increase in CO2 production with temperature. In contrast, the decrease in CH4 production at 35°C was linked to the absence of syntrophic communities and the potential inhibitory effect of phenols on methanogens. Elevated temperatures further induced the microbial communities to develop high growth yield and stress tolerator trait‐based strategies leading to a shift in their composition and function. On the other hand, SRBs were able to outcompete methanogens in the presence of non‐limiting sulfate concentrations at 21°C, thereby reducing CH4 emissions. At higher sulfate concentrations, however, the prevalence of communities capable of producing sufficient low‐molecular‐weight carbon substrates for the coexistence of SRBs and methanogens was translated into elevated CH4 emissions. The use of omics in this study enhanced our understanding of the structure and interactions among microbes with the abiotic components of the system that can be useful for mitigating GHG emissions from peatland ecosystems in the face of global change.
Changing environmental conditions could change microbial activity leading to changes in greenhouse gas emissions. For example, elevated temperatures in peatland ecosystems can induce the microbial communities to develop high growth yield and stress tolerator trait‐based strategies leading to a shift in their composition and function.
Hyporheic zones (HZs)zones of groundwater–surface water mixingare hotspots for dissolved organic matter (DOM) and nutrient cycling that can disproportionately impact aquatic ecosystem functions. ...However, the mechanisms affecting DOM metabolism through space and time in HZs remain poorly understood. To resolve this gap, we investigate a recently proposed theory describing trade-offs between carbon (C) and nitrogen (N) limitations as a key regulator of HZ metabolism. We propose that throughout the extent of the HZ, a single process like aerobic respiration (AR) can be limited by both DOM thermodynamics and N content due to highly variable C/N ratios over short distances (centimeter scale). To investigate this theory, we used a large flume, continuous optode measurements of dissolved oxygen (DO), and spatially and temporally resolved molecular analysis of DOM. Carbon and N limitations were inferred from changes in the elemental stoichiometric ratio. We show sequential, depth-stratified relationships of DO with DOM thermodynamics and organic N that change across centimeter scales. In the shallow HZ with low C/N, DO was associated with the thermodynamics of DOM, while deeper in the HZ with higher C/N, DO was associated with inferred biochemical reactions involving organic N. Collectively, our results suggest that there are multiple competing processes that limit AR in the HZ. Resolving this spatiotemporal variation could improve predictions from mechanistic models, either via more highly resolved grid cells or by representing AR colimitation by DOM thermodynamics and organic N.
Wildfires produce solid residuals that have unique chemical and physical properties compared to unburned materials, which influence their cycling and fate in the natural environment. Visual burn ...severity assessment is used to evaluate post-fire alterations to the landscape in field-based studies, yet muffle furnace methods are commonly used in laboratory studies to assess molecular scale alterations along a temperature continuum. Here, we examined solid and leachable organic matter characteristics from chars visually characterized as low burn severity that were created either on an open air burn table or from low-temperature muffle furnace burns. We assessed how the different combustion conditions influence solid and dissolved organic matter chemistries and explored the potential influence of these results on the environmental fate and reactivity. Notably, muffle furnace chars produced less leachable carbon and nitrogen than open air chars across land cover types. Organic matter produced from muffle furnace burns was more homogeneous than open air chars. This work highlights chemical heterogeneities that exist within a single burn severity category, potentially influencing our conceptual understanding of pyrogenic organic matter cycling in the natural environment, including transport and processing in watersheds. Therefore, we suggest that open air burn studies are needed to further advance our understanding of pyrogenic organic matter’s environmental reactivity and fate.
Exceptionally preserved fossils retain soft tissues and often the biomolecules that were present in an animal during its life. The majority of terrestrial vertebrate fossils are not traditionally ...considered exceptionally preserved, with fossils falling on a spectrum ranging from very well-preserved to poorly preserved when considering completeness, morphology and the presence of microstructures. Within this variability of anatomical preservation, high-quality macro-scale preservation (e.g., articulated skeletons) may not be reflected in molecular-scale preservation (i.e., biomolecules). Excavation of the Hayden Quarry (HQ; Chinle Formation, Ghost Ranch, NM, USA) has resulted in the recovery of thousands of fossilized vertebrate specimens. This has contributed greatly to our knowledge of early dinosaur evolution and paleoenvironmental conditions during the Late Triassic Period (~212 Ma). The number of specimens, completeness of skeletons and fidelity of osteohistological microstructures preserved in the bone all demonstrate the remarkable quality of the fossils preserved at this locality. Because the Hayden Quarry is an excellent example of good preservation in a fluvial environment, we have tested different fossil types (i.e., bone, tooth, coprolite) to examine the molecular preservation and overall taphonomy of the HQ to determine how different scales of preservation vary within a single locality. We used multiple high-resolution mass spectrometry techniques (TOF-SIMS, GC-MS, FT-ICR MS) to compare the fossils to unaltered bone from extant vertebrates, experimentally matured bone, and younger dinosaurian skeletal material from other fluvial environments. FT-ICR MS provides detailed molecular information about complex mixtures, and TOF-SIMS has high elemental spatial sensitivity. Using these techniques, we did not find convincing evidence of a molecular signal that can be confidently interpreted as endogenous, indicating that very good macro- and microscale preservation are not necessarily good predictors of molecular preservation.
Peatlands, which store one third of the terrestrial carbon (C), are subject to large disturbances under a changing climate. It is crucial to understand how microbial and physiochemical factors affect ...the vulnerability of these large C stores to predict climate‐induced greenhouse gas fluxes. Here, we used a combination of mass spectrometry and spectroscopy techniques, to understand sequential biotic and abiotic degradation pathways of Sphagnum fallax leachate in an anaerobic incubation experiment, in the presence and absence of microorganisms. Removal of microorganisms was carried out by passing aqueous samples through 0.2‐µm filters. Our results revealed that S. fallax leachate degradation by abiotic reactions is a significant contributor to CO2 production. Further, abiotic factors, such as low pH, are responsible for partial dissolved organic carbon (DOC) degradation that produces bioavailable compounds that shift microbial metabolic pathways and stimulate respiration in peat bogs. Acid‐catalyzed hydrolysis of Sphagnum‐ produced glycosides can provide the microbial communities with glucose and stimulate microbial respiration of DOC to CO2. These results, while unique to peatlands, demonstrate the importance and underscore the complexity of sequential abiotic and biotic processes on C cycling in peat bogs. It is therefore crucial to incorporate abiotic degradation and sequential below‐ground biotic and abiotic interactions into climate models for a better prediction of the influence of climate change on DOC stability in peatlands. These findings might not be representative of other ecosystems with different environmental conditions including mineral‐rich peatlands and plant matter in surface peat horizons that comprise discrete microbial populations, and DOC composition.
Plain Language Summary
Peatlands store a large amount of carbon (C) in its soil that can be released into the air as CO2. Microorganisms in peatland soil can utilize C and release it into the atmosphere. Abiotic influences (nonmicrobial), such as acidity, can also release C into the atmosphere by complete mineralization and/or by breaking it apart into simpler forms of C for microbial consumption. Here, we incubated dissolved organic carbon leachate from Sphagnum, a dominant vegetation in peatlands, for 70 days and removed microorganisms from one treatment. We found that with no microorganisms, carbon is being released to the air as CO2, and that without microorganisms more CO2 is being released overall. With microorganisms, C is being eaten and transformed differently by microorganisms before being released to the air, which only contributes to ∼10% of the CO2 released in our experiment. We also found that acidity could be cleaving larger forms of C to simpler forms, which these simple forms are more appealing to microorganisms to consume. Therefore, the importance of both abiotic (acidity) and biotic (microorganisms) influences on CO2 production from peatland soils should be considered when predicting ecosystem responses to climate change.
Key Points
Abiotic reactions are a significant contributor to CO2 production in acidic peat bogs
Acid‐catalyzed hydrolysis of complex molecules (e.g., glycosides) results in enhanced availability of glucose for microbial consumption in peat bogs
Abiotic reactions shift microbial metabolic pathways and stimulate respiration in peat bogs
Hyporheic zones (HZs)–zones of groundwater–surface water mixing–are hotspots for dissolved organic matter (DOM) and nutrient cycling that can disproportionately impact aquatic ecosystem functions. ...However, the mechanisms affecting DOM metabolism through space and time in HZs remain poorly understood. To resolve this gap, we investigate a recently proposed theory describing trade-offs between carbon (C) and nitrogen (N) limitations as a key regulator of HZ metabolism. We propose that throughout the extent of the HZ, a single process like aerobic respiration (AR) can be limited by both DOM thermodynamics and N content due to highly variable C/N ratios over short distances (centimeter scale). To investigate this theory, we used a large flume, continuous optode measurements of dissolved oxygen (DO), and spatially and temporally resolved molecular analysis of DOM. Carbon and N limitations were inferred from changes in the elemental stoichiometric ratio. We show sequential, depth-stratified relationships of DO with DOM thermodynamics and organic N that change across centimeter scales. In the shallow HZ with low C/N, DO was associated with the thermodynamics of DOM, while deeper in the HZ with higher C/N, DO was associated with inferred biochemical reactions involving organic N. Collectively, our results suggest that there are multiple competing processes that limit AR in the HZ. In conclusion, resolving this spatiotemporal variation could improve predictions from mechanistic models, either via more highly resolved grid cells or by representing AR colimitation by DOM thermodynamics and organic N.
Coastal terrestrial–aquatic interfaces (TAIs) are dynamic zones of
biogeochemical cycling influenced by salinity gradients. However, there is
significant heterogeneity in salinity influences on TAI ...soil biogeochemical
function. This heterogeneity is perhaps related to unrecognized mechanisms
associated with carbon (C) chemistry and microbial communities. To
investigate this potential, we evaluated hypotheses associated with
salinity-associated shifts in organic C thermodynamics; biochemical
transformations; and nitrogen-, phosphorus-, and sulfur-containing
heteroatom organic compounds in a first-order coastal watershed on the
Olympic Peninsula of Washington, USA. In contrast to our hypotheses,
thermodynamic favorability of water-soluble organic compounds in shallow
soils decreased with increasing salinity (43–867 µS cm−1), as
did the number of inferred biochemical transformations and total heteroatom
content. These patterns indicate lower microbial activity at higher salinity
that is potentially constrained by accumulation of less-favorable organic C.
Furthermore, organic compounds appeared to be primarily marine- or algae-derived
in forested floodplain soils with more lipid-like and protein-like
compounds, relative to upland soils that had more lignin-, tannin-, and
carbohydrate-like compounds. Based on a recent simulation-based study, we
further hypothesized a relationship between C chemistry and the ecological
assembly processes governing microbial community composition. Null modeling
revealed that differences in microbial community composition – assayed using
16S rRNA gene sequencing – were primarily the result of limited exchange of
organisms among communities (i.e., dispersal limitation). This results in
unstructured demographic events that cause community composition to diverge
stochastically, as opposed to divergence in community composition being due
to deterministic selection-based processes associated with differences in
environmental conditions. The strong influence of stochastic processes was
further reflected in there being no statistical relationship between
community assembly processes (e.g., the relative influence of stochastic
assembly processes) and C chemistry (e.g., heteroatom content). This
suggests that microbial community composition does not have a mechanistic or
causal linkage to C chemistry. The salinity-associated gradient in C
chemistry was, therefore, likely influenced by a combination of
spatially structured inputs and salinity-associated metabolic responses of
microbial communities that were independent of community composition. We
propose that impacts of salinity on coastal soil biogeochemistry need to be
understood in the context of C chemistry, hydrologic or depositional dynamics,
and microbial physiology, while microbial composition may have less
influence.
Wildfires produce solid residuals that have unique chemical and physical properties compared to unburned materials, which influence their cycling and fate in the natural environment. Visual burn ...severity assessment is used to evaluate post-fire alterations to the landscape in field-based studies, yet muffle furnace methods are commonly used in laboratory studies to assess molecular scale alterations along a temperature continuum. Here, we examined solid and leachable organic matter characteristics from chars visually characterized as low burn severity that were created either on an open air burn table or from low-temperature muffle furnace burns. We assessed how the different combustion conditions influence solid and dissolved organic matter chemistries and explored the potential influence of these results on the environmental fate and reactivity. Notably, muffle furnace chars produced less leachable carbon and nitrogen than open air chars across land cover types. Organic matter produced from muffle furnace burns was more homogeneous than open air chars. This work highlights chemical heterogeneities that exist within a single burn severity category, potentially influencing our conceptual understanding of pyrogenic organic matter cycling in the natural environment, including transport and processing in watersheds. Furthermore, we suggest that open air burn studies are needed to further advance our understanding of pyrogenic organic matter’s environmental reactivity and fate.
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