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Quantifying the inhibitory impact of soluble phenolics on anaerobic carbon mineralization in a thawing permafrost peatland

['Alexandra B. Cory', 'Department Of Earth', 'Ocean', 'Atmospheric Science', 'Florida State University', 'Tallahassee', 'Fl', 'United States Of America', 'Jeffrey P. Chanton', 'Robert G. M. Spencer']

Date: 2022-02 

The mechanisms controlling the extraordinarily slow carbon (C) mineralization rates characteristic of Sphagnum-rich peatlands (“bogs”) are not fully understood, despite decades of research on this topic. Soluble phenolic compounds have been invoked as potentially significant contributors to bog peat recalcitrance due to their affinity to slow microbial metabolism and cell growth. Despite this potentially significant role, the effects of soluble phenolic compounds on bog peat C mineralization remain unclear. We analyzed this effect by manipulating the concentration of free soluble phenolics in anaerobic bog and fen peat incubations using water-soluble polyvinylpyrrolidone (“PVP”), a compound that binds with and inactivates phenolics, preventing phenolic-enzyme interactions. CO 2 and CH 4 production rates (end-products of anaerobic C mineralization) generally correlated positively with PVP concentration following Michaelis-Menten (M.M.) saturation functions. Using M.M. parameters, we estimated that the extent to which phenolics inhibit anaerobic CO 2 production was significantly higher in the bog—62 ± 16%—than the fen—14 ± 4%. This difference was found to be more substantial with regards to methane production—wherein phenolic inhibition for the bog was estimated at 54 ± 19%, while the fen demonstrated no apparent inhibition. Consistent with this habitat difference, we observed significantly higher soluble phenolic content in bog vs. fen pore-water. Together, these findings suggest that soluble phenolics could contribute to bogs’ extraordinary recalcitrance and high (relative to other peatland habitats) CO 2 :CH 4 production ratios.

Funding: Grant 1 Recipient: V.I.R. Grant number: DE-SC0010580 Funding Source: the Genomic Science Program of the United States Department of Energy Office of Biological and Environmental Research Grants URL: https://genomicscience.energy.gov/ Grant 2 Recipient: V.I.R. Grant number: DE-SC0016440 Funding Source: the Genomic Science Program of the United States Department of Energy Office of Biological and Environmental Research Grants URL: https://genomicscience.energy.gov/ Grant 3 Recipient: V.I.R. Grant Number: 2022070 Funding Source: the EMERGE Biology Integration Institute of the National Science Foundation URL: https://www.nsf.gov/funding/pgm_summ.jsp?pims_id=505684 The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2022 Cory et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

Due to the enormous quantity of carbon (C) contained in peatlands—current estimates ranging from ~530–1,175 Pg globally (equivalent to ~60% - 134% of current atmospheric C stores) [1–3]—shifts in peatland C cycling have potentially significant impacts on the global climate. Most peatlands are CO 2 sinks and CH 4 sources [4–6]. The former process is cooling to the climate, while the latter has a warming effect. While peatland C deposition has had a significant cooling effect on the climate through much of the Holocene, this effect has diminished over the last ~150 years. Estimates of present climatic impacts range from slightly cooling (-0.7 W x m-2; instantaneous box-model estimate) [7] to slightly warming (+0.6 Pg CO 2 -equiv y–1; field flux estimate) [5].

This regime shift is the result of climate change-induced disruptions to the peatland system including water table shifts, permafrost thaw, and increased frequency of fire and drought [8–10]. Acute anthropogenic disturbances (e.g., drainage and burning) have also created significant C balance disruptions and will likely continue to do so without political intervention [5]. Together, these disruptions may speed up rates of CO 2 and CH 4 production via decomposition, thereby shifting peatlands into significant drivers of warming. It is thus imperative that we incorporate an accurate assessment of peatland-climate dynamics into global climate models. To do so, we must understand the underlying biogeochemical processes responsible for peat C mineralization.

Due to the extent of water saturation typically observed in peatlands, most of the peat column decomposes anaerobically [11]. The resulting anoxia precludes oxic respiration and the generally nutrient-depleted conditions characteristic of peatlands hinder respiration via inorganic terminal electron acceptors (“TEAs”) [11]. As such, anaerobic decomposition is limited primarily to three low energy-yielding processes (1) hydrolysis (breakdown of complex organic compounds into simple compounds), (2) fermentation, and (3) methanogenesis. Though slow, anaerobic decay has the potential to significantly impact the climate due to the production of methane (which has a global warming potential of 45 times that of CO 2 on a 100-year timescale [12]. This study will, therefore, focus on the mechanisms controlling anaerobic decomposition in peatlands which, for the sake of brevity, will be henceforth referred to as “decomposition” or “C mineralization”.

Peatland permafrost thaw results in a mosaic of habitat types with differing hydrological and pH regimes that have significant effects on decomposition rates [13–17]. Of particular significance is the shift from Sphagnum-rich (“bog”) to sedge-dominated (“fen”) habitats—the former being known for extraordinarily slow decomposition rates and high CO 2 :CH 4 production ratios—and the latter characterized by relatively quicker decomposition and lower CO 2 :CH 4 ratios [16, 18]. Certain abiotic factors partially explain the slower decomposition rates typically observed in bogs, such as lower pH (~4.5 in bogs, 7–8 in fens; [19]) and availability of TEAs. However, they do not fully account for the much slower decomposition rates observed in bogs [11, 20, 21].

Soluble phenolics have been invoked as potentially significant inhibitors of bog decomposition due to (1) the abundance of bog dissolved organic matter (“DOM”) with high (relative to fen) aromaticity, molecular weight, and O/C ratios—indicative of high soluble phenolic content [22] and (2) the propensity of soluble phenolics to suppress microbial metabolism and inhibit cell growth [22–27]. Metabolic disruptions are attributed to phenolic-enzyme interactions (bonding and/or adsorption), which limit enzyme activity [28–33]. Disruptions to cell growth and function are attributed to phenolic-membrane interactions, which can cause membrane injury and increased permeability [34]. The latter is associated with increased influx of extracellular compounds—some of which can be toxic to micro-organisms—and increased efflux of intracellular components that are necessary for cell growth, such as proteins, potassium, and phosphates [34–38].

Though the inhibitory effects of soluble phenolics are generally accepted, the extent to which they inhibit C mineralization in bogs remains unclear [9, 24, 25, 39, 40]. Studies to date have focused heavily on the potential for soluble phenolics to inhibit enzymatic hydrolysis. These studies have yielded conflicting results, ranging from inconsequential [39, 40] to significant inhibition of hydrolysis [9, 24, 25]. To clarify the impacts of soluble phenolics on bog C mineralization, it is necessary to consider all three stages of bog decomposition (hydrolysis, fermentation, and methanogenesis). There are three reasons for this need: (1) inhibition of fermentation and methanogenesis by soluble phenolics has been observed [27, 35, 41, 42]; (2) evidence of simple sugar buildup in bog peat indicates that C mineralization rates are sometimes not limited by hydrolysis (which produces simple sugars), but rather fermentation and/or methanogenesis (which collectively consume simple sugars) [43]; and (3) there is not always a significant relationship between respiration rates and hydrolytic enzyme activities [44].

Studies that consider the impacts of soluble phenolics on all three stages of bog decomposition are scant. Suppression of CO 2 and CH 4 production—end-products to all three stages—has been observed in incubated peat amended with phenolic-rich DOM [45]. Though it is feasible that soluble phenolics caused this inhibition, the presence of other potentially inhibitory DOM compounds precludes definitive affirmation of this effect [45]. Suppression of aerobic respiration by soluble phenolics has been observed in an aerobic incubation experiment [9], but only after the addition of respiration substrates (C and nutrients). This finding suggests that the potentially inhibitory impacts of soluble phenolics are inconsequential in substrate-limited settings. Given that substrate supply varies in response to site-specific factors—such as vegetation and climate—it is necessary to broaden assessments regarding the impact of soluble phenolics on C mineralization to more sites. Moreover, given the climatically significant role of anaerobic decomposition, [11], it is necessary to apply these assessments to anaerobic conditions.

We analyzed the relationship between in situ soluble phenolic content and anaerobic C mineralization rates in a bog and fen site within a Swedish permafrost peatland (Stordalen Mire). We used the cumulative production of CO 2 and CH 4 (the end-products of C mineralization in anaerobic bog environments) to determine C mineralization rates. Using the methods of [46], we manipulated the concentration of free soluble phenolics using water-soluble polyvinylpyrrolidone (“PVP”). This synthetic polymer “inactivates” soluble phenolics via binding and precipitation, preventing phenolic-enzyme interactions from occurring [47]. To maximize this inactivation, we sought to saturate our incubations with PVP. As the concentration necessary to achieve saturation in our incubations was unknown, additions were undertaken across a wide concentration range.

We hypothesized that increasing PVP concentration would increase C mineralization rates in the bog without the addition of respiration substrates because substantial buildup of simple sugars has been observed in bog pore-water from our study site [43]. We hypothesized that the bog would contain higher soluble phenolic content than the fen, given prior observations that bogs possess higher O/C ratios, greater aromaticity, and higher molecular weights—suggesting higher (potentially inhibitory) phenolic content [22]. We hypothesized that higher soluble phenolic content would cause a stronger inhibitory effect on bog vs. fen C mineralization.

We hypothesized that the relationship between PVP concentration and C mineralization rates would follow a Michaelis-Menten saturation function (Fig 1). By examining the effects of PVP saturation on C mineralization, we sought to quantify the extent to which soluble phenolics inhibit bog and fen C mineralization. We expect these to be minimum estimates given that (1) even in PVP-saturated conditions, a minute portion of free soluble phenolics likely persist [47] and (2) of these persisting soluble phenolics, some could feasibly continue interacting with enzymes, leading to continued inhibition of C mineralization.

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TIFF original image Download: Fig 1. Hypothesized relationship between polyvinylpyrrolidone (PVP) concentration vs. C mineralization. C mineralization rate (measured by CO 2 and CH 4 production) corresponds to the primary y axis (solid black line). Assumed active soluble phenol content corresponds to the secondary y axis (dotted grey line). Addition of PVP was hypothesized to positively impact CO 2 and CH 4 production rates by inactivating soluble phenolics which would otherwise inhibit C decomposition. This relationship was expected to follow a Michaelis-Menten saturation curve. After reaching a point of PVP saturation (red line), further increases in PVP concentration were expected to yield no significant changes in C mineralization rates. https://doi.org/10.1371/journal.pone.0252743.g001

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