Elsevier

Ecological Engineering

Volume 114, 15 April 2018, Pages 104-114
Ecological Engineering

Temporal dynamics of CO2 and CH4 loss potentials in response to rapid hydrological shifts in tidal freshwater wetland soils

https://doi.org/10.1016/j.ecoleng.2017.06.041Get rights and content

Highlights

  • Soil redox rather than antecedent moisture regime drives microbially-mediated biogeochemical transformation of dominant electron acceptors.

  • Acetate-dependent sulfate and iron reduction may govern anaerobic carbon metabolism and constrain methanogenesis under wet conditions.

  • Shifts in metabolite and electron acceptor pools provide indirect evidence for potential for co-occurrence of competitive processes.

Abstract

Earth System Models predict climate extremes that will impact regional and global hydrology. Aquatic-terrestrial transition zones like wetlands are subjected to the immediate consequence of climate change with shifts in the magnitude and dynamics of hydrologic flow. Such fluctuating hydrology can alter the nature and rate of biogeochemical transformations and significantly impact the carbon balance of the ecosystem. We tested the impacts of fluctuating hydrology and, specifically, the role of antecedent moisture conditions in determining the dominant carbon loss mechanisms in soils sampled from a tidal freshwater wetland system in the lower Columbia River, WA, USA. Our objective was to understand shifts in biogeochemical processes in response to changing soil moisture, based on soil respiration and methane production rates, and to elucidate such responses based on the observed electron acceptor and metabolite profiles under laboratory conditions. Metabolomics and biogeochemical process rates provided evidence that soil redox was the principal factor driving metabolic function. Fluctuating redox conditions altered terminal electron acceptor and donor availability and recovery strengths of their concentrations in soil such that a disproportionate release of carbon dioxide stemmed from alternative anaerobic degradation processes like sulfate and iron reduction compared to carbon loss due to methanogenesis. Our results show that extended and short-term saturation created conditions conducive to increasing metabolite availability for anaerobic decomposition processes, with a significant lag in methanogenesis. In contrast, extended drying caused a cellular-level stress response and rapid recycling of alternate electron acceptors.

Graphical abstract

Schematic representation of plausible soil organic carbon degradation pathways in response to fluctuating moisture conditions in a wetland soil. Pathways were selected based on electron acceptor and metabolite profiles. CH2O is used to represent organic matter.

Colored boxes represent measured concentrations of electron donors and acceptors that increased significantly in response to a treatment. Blue box indicates significantly higher concentrations at the end of dry-wet cycle; Gold box indicates significantly higher concentrations at the end of wet-dry cycle; Red box indicates significantly higher concentrations under continuous saturation; Green box indicates no statistical difference between dry-wet and saturation conditions. Grey boxes are species that were not measured. Box with dotted outlines indicate pathway for which thermodynamic consideration was important. Boxes with solid outlines indicate for which no thermodynamic constrain could be estimated. Asterisk (*) Indicates abbreviated forms: TEA = terminal electron acceptor; SCFA = short chain fatty acid.

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Introduction

Tidally-driven freshwater coastal vegetated wetland systems are currently estimated to store 870 million metric ton or approximately 1 Pg C within the top 1 m of soil, are highly vulnerable to carbon (C) loss through greenhouse gasses like carbon dioxide (CO2) and methane (CH4), as result of reduced precipitation and/or sea-level rise (Kirwan et al., 2013, Kirwan and Megonigal, 2013). Notably, the quantitative uncertainties in estimates of CH4 emissions from vegetated coastal wetlands are ∼30%, respectively (EPA, 2017). The directionality and magnitude of changes in C source-sink strengths of these soils remain uncertain as global climate continues to change.

Earth system models predict frequent extreme weather events with longer dry spells or more variable precipitation intensities at regional and global scales (Jentsch et al., 2007, IPCC, 2013), which will significantly influence terrestrial biogeochemical transformations. Soil microbial communities carry out key ecosystem functions, including biogeochemical cycling of major elements like sulfur and iron coupled to the C cycle. These coupled-C processes can be significantly impacted by changes in the abiotic environment, e.g. reduced oxygen availability in saturated soils or complete aeration of soil due to drought. Although well-known functional guilds of bacteria and archaea drive these processes, we lack understanding of their interrelationships to hydrology-driven shifts in the availability of substrate/metabolites and electron acceptors. Predictions of soil C efflux based on current-climate observations will be invalid under altered precipitation regimes without a mechanistic knowledge of key microbially-mediated C-loss processes, at the level of metabolic pathways, to be able to constrain uncertainties (Wieder et al., 2013, Martiny et al., 2017).

The emissions of carbon dioxide (CO2) and/or methane (CH4) are driven by local soil conditions, however the responses vary widely. For example, as non-linear gradients in terminal electron acceptors (TEAs) and substrate concentrations develop over time, ecosystems may experience either rapid losses in C as carbon dioxide (CO2) and/or methane (CH4) or experience delays in response to wetting/drying (Joos et al., 2010). As oxygen is depleted upon abrupt wetting or over an extended saturation period, soil respiration is generally predicted to proceed by sequential consumption of nitrate, manganese, iron, and sulfate and ultimately, methanogenesis. How quickly these competitive processes develop from an initial pool of TEAs and substrate concentrations, and if and how they are switched or become limited as moisture regimes shift are underexplored in wetland soils understood. As shifts in TEAs and products of microbial metabolism are integral to determining the temporal dynamics of measured processes, they will, in turn, determine the dominant C loss mechanisms from a soil system. Recent studies ascribe soil C efflux responses to moisture perturbations to “soil moisture legacy effects” (Evans and Wallenstein, 2012, Banerjee et al., 2016) contingent on the extremity and duration of the perturbation. The few studies on the impact of shifting precipitation regimes (extreme wetting and drying) on soil microbiome have focused on upland systems by analyzing microbial community composition (Kieft et al., 1987, Xiang et al., 2008, Evans and Wallenstein, 2012, Barnard et al., 2015) or have concentrated on identifying statistical associations between the microbial and chemical data, e.g. electron acceptor concentrations (Cong et al., 2015). Here, using controlled laboratory incubations, we investigated the degree to which extreme moisture conditions could alter process rates. We developed a conceptual model of competing processes using TEA and metabolite profiles, and the thermodynamic potentials of key processes. Our goal was to use these data types to examine the potential for unquantifiable pathways key to C cycling and/or stress response with rapidly fluctuating moisture, and identify factors that govern the dominant C loss processes in hydrologically influenced soil systems.

We sought to investigate how limitations in TEAs and metabolites central to anaerobic C cycling control the relative dominance of sulfate reduction, iron reduction and methanogenesis in these ecosystems. We hypothesized that (i) an extended saturation will create a “legacy” of conditions primed to increased C loss via methanogenesis (ii) drying of previously saturated soils will induce aerobic C oxidation pathways, and cause osmolytes production, and (iii) wetting of previously dry soil will result in a lag phase in the onset of anaerobic microbial metabolism. Thus, we used controlled laboratory incubations of soils from a tidal wetland in southwestern Washington State (USA) to investigate the degree to which extreme moisture conditions could alter process rates, TEAs, metabolite profiles and thermodynamic potential of competing processes. These data types revealed the potential for unquantifiable pathways key to C cycling and/or stress responses to rapidly fluctuating moisture; from this we developed a conceptual model of the key biogeochemical processes based on observed and estimated stoichiometric relationships between metabolite profiles and TEAs in response to antecedent soil moisture. Such a model construct based on controlled laboratory studies provide process knowledge at a resolution otherwise difficult to obtain from field-based observations.

Section snippets

Site description and soil collection

One of the largest remaining wetland complexes on the West Coast of the continental United States is on the lower Columbia River and estuary, a 234 km, tidal-fluvial continuum between the Pacific Ocean and Bonneville Dam. The freshwater wetland site is at the widest part of the lowland Columbia near the ocean, at river-kilometer 37 on Grays Bay. The difference between the maximum higher high and minimum lower low for the sampling year (1 Jan–31 Dec 2015) was 3.44 m based on predicted water levels

Soil respiration

The rate of CO2 evolution in the Wet-Dry samples increased gradually over time during the wet phase reaching a maximum on day 21 (2.48 μmol g−1 d−1) after which a gradual decline in rate was observed with the exception of a large increase at 6.73 μmol g−1 d−1 on day 33 (Fig. 1a). Overall, CO2-C loss under wet conditions was significantly higher than under dry conditions. Cumulative CO2 loss during the wet phase of the Wet-Dry treatment was 7.72 μmol g−1 dwt., more than twice the amount lost during the

Discussion

We had challenged the paradigm of soil moisture “legacy effect” that antecedent soil moisture conditions determine the dominant C loss pathways in an altered moisture regime. This would mean that energetically favorable oxidative reactions persist upon re-wetting dry soils while anaerobic C loss pathways would drive C loss upon drying previously saturated soils. Because moisture and redox conditions are intricately related, our effort was to deconvolute them by tracking changes in TEA and

Conclusion

We chose a tidally influenced coastal wetland system as our study site based on the premise that the microbially-driven biogeochemical processes will be primed to the rapidly fluctuating water levels at the site, and by extension primed to select the energetically favorable metabolic pathways related to carbon cycling. Our objective was not to extrapolate the results to the field or ecosystem scale, but to generate a pathway level understanding of the key processes driving C loss mechanisms to

Acknowledgements

This research is part of the Microbiomes in Transition Initiative at Pacific Northwest National Laboratory (PNNL). It was conducted under the Laboratory Directed Research and Development Program at PNNL, a multi-program national laboratory operated by Battelle for the U.S. Department of Energy under Contract DE-AC05-76RL01830. A portion of this research was performed using EMSL, a DOE Office of Science user facility sponsored by the Department of Energy's Office of Biological and Environmental

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