Abstract Methane (CH 4 ) emissions from wetland ecosystems are controlled by redox conditions in the soil, which are currently underrepresented in Earth system models. Plant-mediated radial oxygen loss (ROL) can increase soil O 2 availability, affect local redox conditions, and cause heterogeneous distribution of redox-sensitive chemical species at the root scale, which would affect CH 4 emissions integrated over larger scales. In this study, we used a subsurface geochemical simulator (PFLOTRAN) to quantify the effects of incorporating either spatially homogeneous ROL or more complex heterogeneous ROL on model predictions of porewater solute concentration depth profiles (dissolved organic carbon, methane, sulfate, sulfide) and column integrated CH 4 fluxes for a tidal coastal wetland. From the heterogeneous ROL simulation, we obtained 18% higher column averaged CH 4 concentration at the rooting zone but 5% lower total CH 4 flux compared to simulations of the homogeneous ROL or without ROL. This difference is because lower CH 4 concentrations occurred in the same rhizosphere volume that was directly connected with plant-mediated transport of CH 4 from the rooting zone to the atmosphere. Sensitivity analysis indicated that the impacts of heterogeneous ROL on model predictions of porewater oxygen and sulfide concentrations will be more important under conditions of higher ROL fluxes or more heterogeneous root distribution (lower root densities). Despite the small impact on predicted CH 4 emissions, the simulated ROL drastically reduced porewater concentrations of sulfide, an effective phytotoxin, indicating that incorporating ROL combined with sulfur cycling into ecosystem models could potentially improve predictions of plant productivity in coastal wetland ecosystems.
Journal Article Global Change and the Carbon Balance of Arctic Ecosystems: Carbon/nutrient interactions should act as major constraints on changes in global terrestrial carbon cycling Get access Gaius R. Shaver, Gaius R. Shaver Search for other works by this author on: Oxford Academic Google Scholar W. D. Billings, W. D. Billings Search for other works by this author on: Oxford Academic Google Scholar F. Stuart Chapin, III, F. Stuart Chapin, III Search for other works by this author on: Oxford Academic Google Scholar Anne E. Giblin, Anne E. Giblin Search for other works by this author on: Oxford Academic Google Scholar Knute J. Nadelhoffer, Knute J. Nadelhoffer Search for other works by this author on: Oxford Academic Google Scholar W. C. Oechel, W. C. Oechel Search for other works by this author on: Oxford Academic Google Scholar E. B. Rastetter E. B. Rastetter Search for other works by this author on: Oxford Academic Google Scholar BioScience, Volume 42, Issue 6, June 1992, Pages 433–441, https://doi.org/10.2307/1311862 Published: 01 June 1992
Redox processes, aqueous and solid-phase chemistry, and pH dynamics are key drivers of subsurface biogeochemical cycling in terrestrial and wetland ecosystems but are typically not included in terrestrial carbon cycle models. These omissions may introduce errors when simulating systems where redox interactions and pH fluctuations are important, such as wetlands where saturation of soils can produce anoxic conditions and coastal systems where sulfate inputs from seawater can influence biogeochemistry. Integrating cycling of redox-sensitive elements could therefore allow models to better represent key elements of carbon cycling and greenhouse gas production. We describe a model framework that couples the Energy Exascale Earth System Model (E3SM) Land Model (ELM) with PFLOTRAN biogeochemistry, allowing geochemical processes and redox interactions to be integrated with land surface model simulations. We implemented a reaction network including aerobic decomposition, fermentation, sulfate reduction, sulfide oxidation, and methanogenesis as well as pH dynamics along with iron oxide and iron sulfide mineral precipitation and dissolution. We simulated biogeochemical cycling in tidal wetlands subject to either saltwater or freshwater inputs driven by tidal hydrological dynamics. In simulations with saltwater tidal inputs, sulfate reduction led to accumulation of sulfide, higher dissolved inorganic carbon concentrations, lower dissolved organic carbon concentrations, and lower methane emissions than simulations with freshwater tidal inputs. Model simulations compared well with measured porewater concentrations and surface gas emissions from coastal wetlands in the Northeastern United States. These results demonstrate how simulating geochemical reaction networks can improve land surface model simulations of subsurface biogeochemistry and carbon cycling.
Abstract Sulfur-oxidizing and sulfate-reducing bacteria in salt marsh sediments are major controllers of ecosystem-scale carbon cycling. Cross-site comparisons of S-cycling communities are difficult given the rampant uncultured microbial diversity in sediment, yet comparisons are essential for revealing biogeographic, phylogenetic and functionally significant variation. Here, we use deep shotgun metagenomic sequencing data to construct and compare metagenome-assembled genomes (MAGs) of sulfur-cycling bacteria from Massachusetts and Alabama salt marshes that contrast in seasonality and sediment organic matter content. Samples were collected from sediments under Sporobolus alterniflorus and Sporobolus pumilus in separate MA vegetation zones, and under Sporobolus alterniflorus and Juncus roemerianus co-rooted in AL marsh. We grouped metagenomic data by plant species and site and identified 38 MAGs that included pathways for dissimilatory sulfate reduction or sulfide oxidation. Phylogenetic analyses indicated that 30 of the 38 were affiliated with uncultivated lineages. Read-mapping to MAGs showed significant differentiation of AL and MA samples, differentiation of samples taken in S. alterniflorus and S. pumilus vegetation zones in MA, but no differentiation of samples taken under S. alterniflorus and J. roemerianus that were rooted together in AL marsh. Pangenomic analyses of eight ubiquitous MAGs also detected site- and vegetation-specific genomic features, including varied sulfur-cycling operons, carbon fixation pathways, fixed single nucleotide variants, and active diversity-generating retroelements. This genetic diversity, detected at multiple scales even within uncultured groups, suggests evolutionary relationships affected by distance and local environment, and demonstrates differential microbial capacities for sulfur and carbon cycling in salt marsh sediments. Importance Salt marshes are known for their significant carbon storage capacity, and sulfur cycling is closely linked with the ecosystem-scale carbon cycling in these ecosystems. Sulfate reducers are the major decomposers in salt marsh systems, and sulfur-oxidizing bacteria remove sulfide, a toxic byproduct of sulfate reduction, supporting the productivity of marsh plants. To date, the complexity of coastal environments, heterogeneity of the rhizosphere, high microbial diversity and uncultured majority hindered our understanding of the genomic diversity of sulfur-cycling microbes in salt marshes. Here we use comparative genomics to overcome these challenges and provide an in-depth characterization of microbial diversity in salt marshes. We characterize sulfur-cycling communities across distinct sites and plant species and uncover extensive genomic diversity at the taxon level and specific genomic features present in MAGs affiliated with sulfur-cycling uncultivated lineages. Our work provides insights into the partnerships in salt marshes and a roadmap for multiscale analyses of diversity in complex biological systems.
Coastal marine macrophytes exhibit some of the highest rates of primary productivity in the world. They have been found to host a diverse set of microbes, many of which may impact the biology of their hosts through metabolisms that are unique to microbial taxa. Here, we characterized the metabolic functions of macrophyte-associated microbial communities using metagenomes collected from 2 species of kelp (Laminaria setchellii and Nereocystis luetkeana) and 3 marine angiosperms (Phyllospadix scouleri, P. serrulatus, and Zostera marina), including the rhizomes of two surfgrass species (Phyllospadix spp.), the seagrass Zostera marina, and the sediments surrounding P. scouleri and Z. marina. Using metagenomic sequencing, we describe 63 metagenome-assembled genomes (MAGs) that potentially benefit from being associated with macrophytes and may contribute to macrophyte fitness through their metabolic activity. Host-associated metagenomes contained genes for the use of dissolved organic matter from hosts and vitamin (B1, B2, B7, B12) biosynthesis in addition to a range of nitrogen and sulfur metabolisms that recycle dissolved inorganic nutrients into forms more available to the host. The rhizosphere of surfgrass and seagrass contained genes for anaerobic microbial metabolisms, including nifH genes associated with nitrogen fixation, despite residing in a well-mixed and oxygenated environment. The range of oxygen environments engineered by macrophytes likely explains the diversity of both oxidizing and reducing microbial metabolisms and contributes to the functional capabilities of microbes and their influences on carbon and nitrogen cycling in nearshore ecosystems. IMPORTANCE Kelps, seagrasses, and surfgrasses are ecosystem engineers on rocky shorelines, where they show remarkably high levels of primary production. Through analysis of their associated microbial communities, we found a variety of microbial metabolisms that may benefit the host, including nitrogen metabolisms, sulfur oxidation, and the production of B vitamins. In turn, these microbes have the genetic capabilities to assimilate the dissolved organic compounds released by their macrophyte hosts. We describe a range of oxygen environments associated with surfgrass, including low-oxygen microhabitats in their rhizomes that host genes for nitrogen fixation. The tremendous productivity of coastal seaweeds and seagrasses is likely due in part to the activities of associated microbes, and an increased understanding of these associations is needed.
