Unrecognized controls on microbial functioning in Blue Carbon ecosystems: The role of mineral enzyme stabilization and allochthonous substrate supply

Tidal wetlands are effective carbon sinks, mitigating climate change through the long‐term removal of atmospheric CO2. Studies along surface‐elevation and thus flooding‐frequency gradients in tidal wetlands are often used to understand the effects of accelerated sea‐level rise on carbon sequestration, a process that is primarily determined by the balance of primary production and microbial decomposition. It has often been hypothesized that rates of microbial decomposition would increase with elevation and associated increases in soil oxygen availability; however, previous studies yield a wide range of outcomes and equivocal results. Our mechanistic understanding of the elevation–decomposition relationship is limited because most effort has been devoted to understanding the terminal steps of the decomposition process. A few studies assessed microbial exo‐enzyme activities (EEAs) as initial and rate‐limiting steps that often reveal important insight into microbial energy and nutrient constraints. The present study assessed EEAs and microbial abundance along a coastal ecotone stretching a flooding gradient from tidal flat to high marsh in the European Wadden Sea. We found that stabilization of exo‐enzymes to mineral sediments leads to high specific EEAs at low substrate concentrations in frequently flooded, sediment‐rich zones of the studied ecotone. We argue that the high background activity of a mineral‐associated enzyme pool provides a stable decomposition matrix in highly dynamic, frequently flooded zones. Furthermore, we demonstrate that microbial communities are less nutrient limited in frequently flooded zones, where inputs of nutrient‐rich marine organic matter are higher. This was reflected in both increasing exo‐enzymatic carbon versus nutrient acquisition and decreasing fungal versus bacterial abundance with increasing flooding frequency. Our findings thereby suggest two previously unrecognized mechanisms that may contribute to stimulated microbial activity despite decreasing oxygen availability in response to accelerated sea‐level rise

Subsurface aeration of tidal wetland soils: Root-system structure and aerenchyma connectivity in Spartina (Poaceae)

International audienceRoot-aerenchyma in wetland plants facilitate transport of oxygen from aboveground sources (atmosphere and photosynthesis) to belowground roots and rhizomes, where oxygen can leak out and oxygenate the otherwise anoxic soils. In salt marshes, the soil oxygenation capacity varies among different Spartina-taxa, but little is known about structural pattern and connectivity of root-aerenchyma that facilitates this gas transport. Both environmental conditions and ploidy level play a role for the root-system morphology. Root-system morphology of polyploid Spartina-taxa was studied, quantifying root-tissue volume and root-aerenchyma volume of hexaploid Spartina alterniflora, Spartina maritima, and Spartina × townsendii as well as dodecaploid Spartina anglica from different habitats. Computed tomography (CT)-scan image analysis was applied to quantify the volume of roots and aerenchyma, and to determine the root-system structure (ratio of aerenchyma to root-tissue volumes) and aerenchyma connectivity. On average, Spartina-roots accounted for 12% (v/v) and root-aerenchyma accounted for 1% (v/v) of the soil volume in the pioneer marsh. About 90% (v/v) of all roots were associated with aerenchyma. Root-system structures of S. × townsendii and S. anglica differed and showed clear responses to habitat conditions, such as flooding regime and redox potential. The development of large well-connected aerenchyma fragments were specifically shown in S. anglica and to a minor extend in S. maritima. Aerenchyma in S. alterniflora and S. × townsendii consisted only of smaller fragments. Spartina-dominated tidal marsh soils show high connectivity with the atmosphere via root-aerenchyma. The high ploidy level in S. anglica comes along with high connectivity in root-aerenchyma

The Overlooked Hybrid: Geographic Distribution and Niche Differentiation Between Spartina Cytotypes (Poaceae) in Wadden Sea Salt Marshes

Whole genome duplications (WGDs) lead to polyploid specimens and are regarded as major drivers for speciation and diversification in plants. One prevalent problem when studying WGDs is that effects of polyploidization in ancient polyploids cannot be disentangled from the consequences of selective evolutionary forces. Cytotypic differences in distribution, phenotypic appearance and in response to surface elevation (determined by HOF-modeling) were identified in a relatively young taxa-group of a hexaploid F₁-hybrid (Spartina× townsendii H. Groves & J. Groves, Poaceae) and its dodecaploid descendent (Spartina anglica C.E. Hubbard, Poaceae) using vegetation assessments (1029 plots; 1 × 1 m²) from the European Wadden Sea mainland salt marshes, including elevational and mean high tidal (MHT) data. While the F₁-hybrid was mainly present in the eastern part of the Wadden Sea, its dodecaploid descendent occurred in the entire Wadden Sea area. The Spartina cytotypes differed in phenotypes (median of Spartina cover: hexaploid = 25% vs. dodecaploid = 12%) and in elevational niche-optimum (hexaploid = − 49.5 cm MHT vs. dodecaploid = 8.0 cm MHT). High ploidy levels correlated with establishment success in Spartina along geographic gradients but did not seem to increase the capacity to cope with abiotic severity downwards the elevational gradient in salt marshes

Top‐down control of carbon sequestration: grazing affects microbial structure and function in salt marsh soils

Tidal wetlands have been increasingly recognized as long‐term carbon sinks in recent years. Work on carbon sequestration and decomposition processes in tidal wetlands focused so far mainly on effects of global‐change factors such as sea‐level rise and increasing temperatures. However, little is known about effects of land use, such as livestock grazing, on organic matter decomposition and ultimately carbon sequestration. The present work aims at understanding the mechanisms by which large herbivores can affect organic matter decomposition in tidal wetlands. This was achieved by studying both direct animal–microbe interactions and indirect animal–plant–microbe interactions in grazed and ungrazed areas of two long‐term experimental field sites at the German North Sea coast. We assessed bacterial and fungal gene abundance using quantitative PCR, as well as the activity of microbial exo‐enzymes by conducting fluorometric assays. We demonstrate that grazing can have a profound impact on the microbial community structure of tidal wetland soils, by consistently increasing the fungi‐to‐bacteria ratio by 38–42%, and therefore potentially exerts important control over carbon turnover and sequestration. The observed shift in the microbial community was primarily driven by organic matter source, with higher contributions of recalcitrant autochthonous (terrestrial) vs. easily degradable allochthonous (marine) sources in grazed areas favoring relative fungal abundance. We propose a novel and indirect form of animal–plant–microbe interaction: top‐down control of aboveground vegetation structure determines the capacity of allochthonous organic matter trapping during flooding and thus the structure of the microbial community. Furthermore, our data provide the first evidence that grazing slows down microbial exo‐enzyme activity and thus decomposition through changes in soil redox chemistry. Activities of enzymes involved in C cycling were reduced by 28–40%, while activities of enzymes involved in N cycling were not consistently affected by grazing. It remains unclear if this is a trampling‐driven direct grazing effect, as hypothesized in earlier studies, or if the effect on redox chemistry is plant mediated and thus indirect. This study improves our process‐level understanding of how grazing can affect the microbial ecology and biogeochemistry of semi‐terrestrial ecosystems that may help explain and predict differences in C turnover and sequestration rates between grazed and ungrazed systems

Plant traits affect vertical accretion of salt marshes

The current climate crisis is associated with rising sea levels, which raises the concerning prospect of losing coastal ecosystems, such as salt marshes. Where inland migration is impossible, salt marshes will only persist if their vertical accretion exceeds the rate of sea-level rise. Positive vertical accretion is mainly driven by sedimentation, whereas negative vertical accretion is driven by erosion and soil compaction, among others. These processes can be influenced by abiotic and biotic factors. The biotic factors, best described by plant functional traits of the salt-marsh vegetation, are, however, not well understood. We assembled a large dataset of 336 plots with vertical accretion time series and plant abundances and coupled it with trait data from salt marsh species of the German Wadden Sea, covering natural unmanaged, anthropogenic unmanaged, and grazed marshes. By using multiple logistic regression analyses, we studied the effects of plant functional traits and distance to the marsh edge on vertical accretion. Mean vertical accretion was in the range of recent sea level rise, except for plots on elevated grazed marshes. There were, however, pronounced local differences in vertical accretion. Positive accretion increased with distance to marsh edge and increasing leaf and stem roughness, described by specific stem length, canopy height, stem mass, leaf mass and leaf area. Except on grazed marshes, leaf traits contributed more strongly to the explanation of positive accretion than stem traits. Negative accretion by e.g., erosion was facilitated by low specific root length and low root and rhizome mass, i.e., lower anchoring capacity. To better assess coastal resilience to sea level rise, our findings suggest (i) to include these effect traits in models and experimental analyses of salt marsh vertical accretion and (ii) to consider effects of vegetation roughness on accretion in salt marsh management schemes

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Computed tomography (CT) scan image analysis: Data of CT-scan images, root system structure, and root aerenchyma connectivity of Spartina (Poaceae) soil cores from tidal wetlands

Soil cores from tidal Spartina-marshes were sampled in 2018 in the European Wadden Sea, Sönke-Nissen-Koog, Germany, as well as at the Atlantic coast, Brittany, France, and scanned by a Toshiba Aquilion 64 computer tomograph (CT) at the Klinikum Bremen-Mitte (Bremen, Germany) using an X-ray source voltage of 120 kV and a current of 600 mA. Images were reconstructed using Toshiba's patented helical cone beam reconstruction technique and are provided as grey-scale image in DICOM-format that contains the X-ray attenuation of the sample material measured in standardized Hounsfield Units (HU; Hounsfield, 1979). The resulting CT-image stacks (d = 18 cm, h = 23 cm) have a resolution of 0.35 mm in x-direction and y-direction and of 0.5 mm in z-direction (0.3 mm reconstruction unit). The CT-scan images were analyzed by processing the data with the ZIB edition of the Amira software (version 2019.35; Stalling et al., 2005; http://amira.zib.de). The root-systems of Spartina plants were reconstructed by means of marker-controlled watershed segmentation followed by automated skeleton analysis. The root-tissue and root-aerenchyma were distinguished using a segmentation threshold of -500 HU for root-tissue. The volumes of root-tissue and root-aerenchyma were quantified (MaterialStatistics module; statistics per slice per label) and aerenchyma fragment volumes inside larger rhizomes (minimum radius of 0.7 mm and minimum of 70 mm length) were calculated