Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils

Narrowe, Adrienne B.; Borton, Mikayla A.; Hoyt, David; Smith, Garrett J.; Daly, Rebecca A.; Angle, Jordan C.; Eder, Elizabeth K.; Wong, Allison R.; Wolfe, Richard A.; Pappas, Alexandra; Bohrer, Gil; Miller, Christopher S.; Wrighton, Kelly

doi:10.1128/msystems.00320-19

Cited by 47 publications

(56 citation statements)

References 78 publications

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“…Yet in these soils, temperature (<20 °C) was suggested to be a possible kinetic controller on microbial growth and enzyme activity, thus limiting polyphenol metabolism 19 . To extend these prior studies, we selected plant-covered, mineral soils from a microbially well-studied temperate, freshwater wetland 18 , 20 , thereby eliminating kinetic constraints and expanding our search for these metabolisms across a broader range of soil types. These wetland surface soils contained polyphenols (Supplementary Fig.…”

Section: Resultsmentioning

confidence: 99%

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Decrypting bacterial polyphenol metabolism in an anoxic wetland soil

et al. 2021

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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.

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Section: Resultsmentioning

confidence: 99%

“…These wetland surface soils contained polyphenols (Supplementary Fig. 1 ) and have been shown to be tractable using multi-omics methods 18 , 20 , and thus were used as a model soil for evaluation of anaerobic polyphenol metabolism.…”

Section: Resultsmentioning

confidence: 99%

Decrypting bacterial polyphenol metabolism in an anoxic wetland soil

et al. 2021

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“…1b). Methylotrophic methanogenesis (Narrowe et al, 2019) is neglected in the model. The overall reaction rates are represented as…”

Section: Microbial Functional Group Model For Methane Production and mentioning

confidence: 99%

“…Climate, and specifically patterns in rainfall, also affects emissions from tropical forests. Climate change may increase the frequency and severity of extreme rainfall and drought events, altering the spatial and temporal dynamics of CH 4 emissions through changes in redox dynamics and substrate availability (Silver et al, 1999;Chadwick et al, 2016;Neelin et al, 2006). Thus, accurately estimating CH 4 emissions under a variety of climatic and topographic conditions is important for predicting soil carbon-climate feedbacks in the humid tropical biome.…”

Section: Introductionmentioning

confidence: 99%

Representing methane emissions from wet tropical forest soils using microbial functional groups constrained by soil diffusivity

Sihi

Ortiz

et al. 2021

Biogeosciences

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Abstract. Tropical ecosystems contribute significantly to global emissions of methane (CH4), and landscape topography influences the rate of CH4 emissions from wet tropical forest soils. However, extreme events such as drought can alter normal topographic patterns of emissions. Here we explain the dynamics of CH4 emissions during normal and drought conditions across a catena in the Luquillo Experimental Forest, Puerto Rico. Valley soils served as the major source of CH4 emissions in a normal precipitation year (2016), but drought recovery in 2015 resulted in dramatic pulses in CH4 emissions from all topographic positions. Geochemical parameters including (i) dissolved organic carbon (C), acetate, and soil pH and (ii) hydrological parameters like soil moisture and oxygen (O2) concentrations varied across the catena. During the drought, soil moisture decreased in the slope and ridge, and O2 concentrations increased in the valley. We simulated the dynamics of CH4 emissions with the Microbial Model for Methane Dynamics-Dual Arrhenius and Michaelis–Menten (M3D-DAMM), which couples a microbial functional group CH4 model with a diffusivity module for solute and gas transport within soil microsites. Contrasting patterns of soil moisture, O2, acetate, and associated changes in soil pH with topography regulated simulated CH4 emissions, but emissions were also altered by rate-limited diffusion in soil microsites. Changes in simulated available substrate for CH4 production (acetate, CO2, and H2) and oxidation (O2 and CH4) increased the predicted biomass of methanotrophs during the drought event and methanogens during drought recovery, which in turn affected net emissions of CH4. A variance-based sensitivity analysis suggested that parameters related to aceticlastic methanogenesis and methanotrophy were most critical to simulate net CH4 emissions. This study enhanced the predictive capability for CH4 emissions associated with complex topography and drought in wet tropical forest soils.

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“…can profit from these carbon-excretions, and not other methylotrophs. If the methane-derived carbon products are indeed released into the water column, and are thus freely accessible to other organisms, this could also have implications for the methane cycle from the production side, as these compounds could then be used for methylotrophic methanogenesis (Lovley and Klug, 1983;Narrowe et al, 2019). The lack of physical contact between Methylobacter sp.…”

Section: Spatial Analysis Of the Methylobacter-methylotenera Interactionmentioning

confidence: 99%

Microorganisms and electron acceptors affecting methane oxidation in freshwater and marine systems

Grinsven¹

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Water column stratification is one of the main factors determining electron acceptor availability. In a well-mixed water column, water masses, particulate and dissolved matter and gasses can move freely through the water column, resulting in homogeneous temperature, nutrient, oxygen and other gas concentration profiles, as is illustrated in Fig. 3. Stratified systems, by contrast, consist of two or more layers separated by a steep gradient in temperature or dissolved substances, which limits vertical transport of water, particles and gasses (Fig. 3). The diffusion of atmospheric gasses such as oxygen is limited to the upper water layer, whilst gasses that diffuse from the sediment, such as methane, get trapped in the bottom water layer. The bottom water layer can become oxygen depleted, creating an oxygen gradient within the water column with distinct niches for aerobic and anaerobic microorganisms, including methane producers and oxidizers. Stratification can occur seasonally, as is observed in many lakes, or be permanent, like in the Black Sea. The microbial community within the anoxic zone of the Black Sea is highly adapted to the permanently anoxic conditions (Deuser, 1971). In seasonally stratified systems, however, microorganisms that are able to adapt to the changing conditions may have a competitive advantage, e.g. facultative anaerobes and fast-growing microorganisms. tion of a seasonally stratified aquatic system. In the mixed situation (left side), the water column is homogeneous and well-mixed. The oxic-anoxic interface is located in the sediment. In the stratified situation (right side), two or more water masses exist, separated by an area that is characterized by a steep oxygen gradient, called the oxycline, which forms the oxic-anoxic interface. Methane is produced by methanogenic microorganisms (i.e. archaea) in the anoxic sediments (1), where it may partly already be oxidized. The remaining methane diffuses into the water column, both in the mixed and stratified situation. In the stratified situation, methane may also be produced in the anoxic water column. In the mixed situation, the dissolved, diffused methane that escaped sedimentary methane oxidation can be transported through the whole water column (2), and will reach the surface waters, from where it can be emitted to the atmosphere (3). Water column methane oxidation in the oxic, mixed situation is generally considered to be inhibited by high oxygen concentrations. In the stratified water column, the oxycline acts as a barrier for the dissolved methane, limiting diffusion and trapping methane in the bottom water layer, resulting in an increase in methane concentration over time (4). Methane may be oxidized in the anoxic water column or at the oxycline, or can be released when mixing of the water layers occurs, ending stratification. Microorganisms involved in methane consumption Methane oxidizing bacteria Methane oxidizing organisms were first detected in 1906 by N.L. Söhngen (Söhngen, 1906). In 1970, Whittenbury, Phillips, and Wilkinson c...

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Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils

Cited by 47 publications

References 78 publications

Decrypting bacterial polyphenol metabolism in an anoxic wetland soil

Decrypting bacterial polyphenol metabolism in an anoxic wetland soil

Representing methane emissions from wet tropical forest soils using microbial functional groups constrained by soil diffusivity

Microorganisms and electron acceptors affecting methane oxidation in freshwater and marine systems

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