Discerning Microbially Mediated Processes During Redox Transitions in Flooded Soils Using Carbon and Energy Balances

Boye, Kristin; Herrmann, Anke M.; Schaefer, Michael V.; Tfaily, Malak M.; Fendorf, Scott

doi:10.3389/fenvs.2018.00015

Cited by 16 publications

(12 citation statements)

References 48 publications

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“…Organic substrate serves as sources of both carbon (biomass yielding) and energy (energy yielding) for microorganisms, and microbial growth efficiency stops when the combustion heats of substrate and biomass are equal ( 42 ). A thermodynamically favorable substrate is supposed to be correlated with higher CUE (i.e., higher biomass yielding [ 43 ]) and hence higher SOM content as a result ( 44 ). Specifically, in an environment with an organic substrate of high thermodynamic quality, greater diversity is expected to increase microbial transformation efficiency and consequently generate more microbially derived SOM ( 10 , 21 , 22 ).…”

Section: Discussionmentioning

confidence: 99%

Evaluation of Microbe-Driven Soil Organic Matter Quantity and Quality by Thermodynamic Theory

Zhang

Feng

et al. 2021

mBio

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Microbial communities, coupled with substrate quality and availability, regulate the stock (formation versus mineralization) of soil organic matter (SOM) in terrestrial ecosystems. However, our understanding of how soil microbes interact with contrasting substrates influencing SOM quantity and quality is still very superficial. Here, we used thermodynamic theory principles and Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS) to evaluate the linkages between dissolved organic matter (DOM [organic substrates in soil that are readily available]), thermodynamic quality, and microbial communities. We investigated soils from subtropical paddy ecosystems across a 1,000-km gradient and comprising contrasting levels of SOM content and nutrient availability. Our region-scale study suggested that soils with a larger abundance of readily accessible resources (i.e., lower Gibbs free energy) supported higher levels of microbial diversity and higher SOM content. We further advocated a novel phylotype-level microbial classification based on their associations with OM quantities and qualities and identified two contrasting clusters of bacterial taxa: phylotypes that are highly positively correlated with thermodynamically favorable DOM and larger SOM content versus those which are associated with less-favorable DOM and lower SOM content. Both groups are expected to play critical roles in regulating SOM contents in the soil. By identifying the associations between microbial phylotypes of different life strategies and OM qualities and quantities, our study indicates that thermodynamic theory can act as a proxy for the relationship between OM and soil microbial communities and should be considered in models of soil organic matter preservation. IMPORTANCE Microbial communities are known to be important drivers of organic matter (OM) accumulation in terrestrial ecosystems. However, despite the importance of these soil microbes and processes, the mechanisms behind these microbial-SOM associations remain poorly understood. Here, we used the principles of thermodynamic theory and novel Fourier transform ion cyclotron resonance mass spectrometry techniques to investigate the links between microbial communities and dissolved OM (DOM) thermodynamic quality in soils across a 1,000-km gradient and comprising contrasting nutrient and C contents. Our region-scale study provided evidence that soils with a larger amount of readily accessible resources (i.e., lower Gibbs free energy) supported higher levels of microbial diversity and larger SOM content. Moreover, we created a novel phylotype-level microbial classification based on the associations between microbial taxa and DOM quantities and qualities. We found two contrasting clusters of bacterial taxa based on their level of association with thermodynamically favorable DOM and SOM content. Our study advances our knowledge on the important links between microbial communities and SOM. Moreover, by identifying the associations between microbial phylotypes of different life strategies and OM qualities and quantities, our study indicates that thermodynamic theory can act as a proxy for the relationship between OM and soil microbial communities. Together, our findings support that the association between microbial species taxa and substrate thermodynamic quality constituted an important complement explanation for soil organic matter preservation.

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Section: Discussionmentioning

confidence: 99%

Evaluation of Microbe-Driven Soil Organic Matter Quantity and Quality by Thermodynamic Theory

Zhang

Feng

et al. 2021

mBio

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“…Dictated by thermodynamics, fermentation characteristically occurs under strongly reducing conditions (e.g., CO 2 , sulfate) where alternative terminal electron acceptors (e.g., nitrate, nitrite, sulfate, FeIII) have been depleted. The oxidation state of OM itself can also indicate the extent to which it is decomposed ( Boye et al, 2017 , 2018 ). An abundance of low (more negative) NOSC C compounds may favor less thermodynamically favorable microbial processes such as fermentation and acetogenesis ( Ye et al, 2014 ; Ewing et al, 2015a ; Boye et al, 2018 ).…”

Section: Discussionmentioning

confidence: 99%

“…The oxidation state of OM itself can also indicate the extent to which it is decomposed ( Boye et al, 2017 , 2018 ). An abundance of low (more negative) NOSC C compounds may favor less thermodynamically favorable microbial processes such as fermentation and acetogenesis ( Ye et al, 2014 ; Ewing et al, 2015a ; Boye et al, 2018 ). Our data indicate increased pooling of reduced C and SCFAs in the oldest samples ( Figure 2 ), suggesting that less thermodynamically favorable C is preserved in ancient permafrost.…”

Section: Discussionmentioning

confidence: 99%

Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence

et al. 2020

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Permafrost is an extreme habitat yet it hosts microbial populations that remain active over millennia. Using permafrost collected from a Pleistocene chronosequence (19 to 33 ka), we hypothesized that the functional genetic potential of microbial communities in permafrost would reflect microbial strategies to metabolize permafrost soluble organic matter (OM) in situ over geologic time. We also hypothesized that changes in the metagenome across the chronosequence would correlate with shifts in carbon chemistry, permafrost age, and paleoclimate at the time of permafrost formation. We combined high-resolution characterization of water-soluble OM by Fourier-transform ion-cyclotron-resonance mass spectrometry (FT-ICR MS), quantification of organic anions in permafrost water extracts, and metagenomic sequencing to better understand the relationships between the molecular-level composition of potentially bioavailable OM, the microbial community, and permafrost age. Both age and paleoclimate had marked effects on both the molecular composition of dissolved OM and the microbial community. The relative abundance of genes associated with hydrogenotrophic methanogenesis, carbohydrate active enzyme families, nominal oxidation state of carbon (NOSC), and number of identifiable molecular formulae significantly decreased with increasing age. In contrast, genes associated with fermentation of short chain fatty acids (SCFAs), the concentration of SCFAs and ammonium all significantly increased with age. We present a conceptual model of microbial metabolism in permafrost based on fermentation of OM and the buildup of organic acids that helps to explain the unique chemistry of ancient permafrost soils. These findings imply long-term in situ microbial turnover of ancient permafrost OM and that this pooled biolabile OM could prime ancient permafrost soils for a larger and more rapid microbial response to thaw compared to younger permafrost soils.

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“…The unique peaks were plotted on van Krevelen diagrams, as described above, using R (version 3.6.1) to observe biochemical compound class differences. Further, Gibbs free energy (GFE) was calculated, as described previously in Boye et al (2018), for all unique peaks assigned a molecular formula. Briefly, each assigned molecular formula was used to calculate the nominal oxidation state of C (NOSC) according to the following equation:…”

Section: Unique Mass Comparisons and Gibbs Free Energymentioning

confidence: 99%

Coupled Biotic-Abiotic Processes Control Biogeochemical Cycling of Dissolved Organic Matter in the Columbia River Hyporheic Zone

et al. 2021

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A critical component of assessing the impacts of climate change on watershed ecosystems involves understanding the role that dissolved organic matter (DOM) plays in driving whole ecosystem metabolism. The hyporheic zone—a biogeochemical control point where ground water and river water mix—is characterized by high DOM turnover and microbial activity and is responsible for a large fraction of lotic respiration. Yet, the dynamic nature of this ecotone provides a challenging but important environment to parse out different DOM influences on watershed function and net carbon and nutrient fluxes. We used high-resolution Fourier-transform ion cyclotron resonance mass spectrometry to provide a detailed molecular characterization of DOM and its transformation pathways in the Columbia river watershed. Samples were collected from ground water (adjacent unconfined aquifer underlying the Hanford 300 Area), Columbia river water, and its hyporheic zone. The hyporheic zone was sampled at five locations to capture spatial heterogeneity within the hyporheic zone. Our results revealed that abiotic transformation pathways (e.g., carboxylation), potentially driven by abiotic factors such as sunlight, in both the ground water and river water are likely influencing DOM availability to the hyporheic zone, which could then be coupled with biotic processes for enhanced microbial activity. The ground water profile revealed high rates of N and S transformations via abiotic reactions. The river profile showed enhanced abiotic photodegradation of lignin-like molecules that subsequently entered the hyporheic zone as low molecular weight, more degraded compounds. While the compounds in river water were in part bio-unavailable, some were further shown to increase rates of microbial respiration. Together, river water and ground water enhance microbial activity within the hyporheic zone, regardless of river stage, as shown by elevated putative amino-acid transformations and the abundance of amino-sugar and protein-like compounds. This enhanced microbial activity is further dependent on the composition of ground water and river water inputs. Our results further suggest that abiotic controls on DOM should be incorporated into predictive modeling for understanding watershed dynamics, especially as climate variability and land use could affect light exposure and changes to ground water essential elements, both shown to impact the Columbia river hyporheic zone.

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Discerning Microbially Mediated Processes During Redox Transitions in Flooded Soils Using Carbon and Energy Balances

Cited by 16 publications

References 48 publications

Evaluation of Microbe-Driven Soil Organic Matter Quantity and Quality by Thermodynamic Theory

Evaluation of Microbe-Driven Soil Organic Matter Quantity and Quality by Thermodynamic Theory

Life at the Frozen Limit: Microbial Carbon Metabolism Across a Late Pleistocene Permafrost Chronosequence

Coupled Biotic-Abiotic Processes Control Biogeochemical Cycling of Dissolved Organic Matter in the Columbia River Hyporheic Zone

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