Rhizosphere Processes in Wetlands

Abstract

Wetlands are diverse and important ecosystems in global nutrient and carbon cycles but are declining due to anthropogenic and climatic threats to their areal extent and quality. Wetlands are profoundly shaped by their hydrology that gives rise to unique soil characteristics and well-adapted plant communities. Water level fluctuations are a common feature in many wetlands such as estuarine tidal marshes and freshwater lakes, where increased variability in abiotic factors can have a strong influence on plant productivity and the distribution of plant traits. Vegetation is a key element in carbon sequestration because of carbon fixation and deposition into the soil as various forms of organic matter, including belowground biomass and root exudates. Plant inputs are subsequently transformed by soil microbiota that drive organic matter degradation and contribute to the formation of soil organic matter (i.e. long-term soil carbon storage). The imbalance between input and output of carbon is remarkably large in many wetland types, making them significant carbon sinks. Most information we have on wetland plants and their role in nutrient and carbon cycling stems from investigations of certain aboveground plant traits (e.g. aboveground biomass, plant height, specific leaf area). These aboveground plant traits have been related to nutrient acquisition and depicted along gradients that reflect a variety of plant functional strategies (i.e. plant economic spectrum). Comparatively, belowground plant traits are more challenging to access and study, revealing a research gap in how these traits also relate to overall plant function. Functional plant traits at the individual or species level have been shown to correlate with observations of plants at the community- and ecosystem scales. Therefore, examining root traits, particularly those that influence microbial degradation of organic matter, has great potential to make predictions about ecosystems functioning with respect to carbon sequestration and storage. As root-microbiota interactions are most intense in the rhizosphere, i.e. the immediate soil around the roots, a trait-based approach was used to evaluate of physiological root traits (O2 release, CO2 uptake, exudation) on biogeochemical properties of soil or sediments and microbial communities in wetlands.

Plant effects on soil redox conditions were quantified along a hydrological gradient in a salt marsh at the Wadden Sea and in a mesocosm experiment (Chapter 2) to determine the impact of plants on soil reduction using IRIS (Indicator of Reduction in Soils) sticks. The study revealed the ability of wetland plants to act as both net oxidizers and reducers of tidally-influenced soil in a manner inversely related to background redox conditions. Plants generally reduced soil with relatively high redox potential and oxidized the soil when redox potentials were low. Intraspecific variation in radial oxygen loss was more deeply investigated using planar optodes; these observations gave further support for plastic root responses of O2 release along a gradient of oxygen demand in the rhizosphere. These findings identify substrate characteristics as an important abiotic filter of plant-mediated shifts of soil redox conditions.

Physiological root traits related to gas exchange between the sediment and plant roots (O2 release, CO2 uptake) were measured in two life forms of the amphibious plant Littorella uniflora (Chapter 3) to evaluate trait performance in each life form under two hydrological treatments and alternating light cycles. The findings of this study indicate that these physiological traits may not be maintained between the aquatic and terrestrial life forms as the terrestrial form demonstrated limited abilities of both sediment CO2 uptake and O2 release compared to the aquatic counterpart, especially upon reintroduction to aquatic conditions (i.e. under submergence). Limitations in either root trait could mean significant consequences for individuals to meet metabolic demands for photosynthesis or respiration. This study underscores the role of phenotypic plasticity as a possible mechanism for adaptation in highly variable environments. Furthermore, the implications of this study could be significant for occurrence of these isoetids and their ecological role in maintaining the oligotrophic status of lakes.

Plants provide electron donors to the soil or sediment via root exudation and thereby indirectly influence the degradation of organic matter by stimulating of soil decomposers. Transcriptional and community composition analysis of prokaryotic soil microbiota (i.e. bacteria and archaea) was conducted on bulk and rhizosphere soil of a common salt marsh plant, Spartina anglica (Chapter 4). By performing pulse-labeling of the aboveground tissues of Spartina anglica with the carbon isotope 13C, photosynthetically-fixed carbon by the plant could be traced into the soil and used to detect the presence of root exudates. In this way, samples could be distinguished by their 13C signature following enrichment analysis and operationally defined as either rhizosphere samples (13C-enriched) or bulk soil samples (13C signatures that did not diverge from control samples). Key gene analysis of both rhizosphere and bulk soils revealed the prominence of two main energy-conserving metabolic pathways, Wood-Ljungdahl and dissimilatory sulfate reduction. Transcriptional activity of the prokaryotes in the rhizosphere showed upregulation of genes involved in motility, stress response and infection, suggesting that roots stimulate bacterial mobility and organismal interactions. Analysis of community composition demonstrated enhanced relative abundances of certain prokaryotic groups in rhizosphere soil compared to the bulk soil, implying that roots may create favorable conditions for certain taxa who might gain a competitive advantage over other constituents of the community.

Altogether investigating root trait variability at the individual or species level provided mechanistic insight into how plants influence soil biogeochemistry (e.g. soil redox potential) and soil microbiota through physiological root traits. Root traits such as radial oxygen loss and root exudation are both influenced by abiotic factors such as sediment properties and biological drivers of intraspecific variability (e.g. phenotypic plasticity). These insights further the concept of root trait economics by addressing the role of previously neglected functional traits. Future of more physiological root trait measurements will likely enrich the growing knowledge of functional root traits and help to identify further common strategies in the root economic space. As this framework exists to help us predict plant functional responses to a range of environmental gradients, measurements in variable ecosystems like wetlands are particularly needed to make these predictions for wetland-specific plant adaptations. Considering the importance of wetlands not only for carbon sequestration but carbon storage, future research might use a more robust trait-based approach to elucidate the role of functional root traits in carbon stabilization processes as well.