Wetland plant root exudates and their effects on the carbon cycle

Krüger, Namid

Zusammenfassung

Plants are the primary pathway for carbon transport from the atmosphere to the pedosphere, since they provide dead litter-carbon to the soil and release hundreds of different soluble organic compounds from their living roots, known as root exudates, into the rhizosphere. The stability of soil organic matter is determined not only by environmental conditions and soil properties, but also by the vegetation cover, which can induce changes in decomposition rates, so-called priming effects. While priming effects are increasingly well understood in terrestrial upland soils, critical knowledge gaps remain for wetland soils, where soils typically exhibit reducing conditions, and vascular plants supply oxygen along with root exudates. Besides that, the exudation rates and compositions of exudate profiles in different wetland plant species have been poorly investigated. The stability of soil organic matter is becoming more uncertain under climate change, which induces soil warming and alters wetland plant traits and community composition, thereby modifying root exudate dynamics. However, it remains unclear whether priming effects are temperature-sensitive and whether the quantity and quality of exudate compounds (e.g., their nutrient contents) have the potential to influence the magnitude or direction of priming effects in anoxic wetland soils. Given the disproportionately large contribution of wetlands to the global soil organic carbon (SOC) storage, the limited understanding of recent and future plant-induced priming effects represents a critical knowledge gap in global carbon budgets. The aim of this dissertation was to provide an overview of wetland plant root exudation, to investigate exudate-induced effects on organic carbon stability in anoxic wetland soils at the mechanistic level, and to apply these insights to elucidate rhizosphere priming effects in a plant-soil system. The dissertation is structured into six chapters, four of which (Chapter II - Chapter V) consist of research manuscripts that have been published in peer-reviewed journals, are currently under review, or are in preparation for submission. Chapter I provides a general introduction, and Chapter VI presents an integrative discussion of the research findings. Chapter II presents a literature synthesis that compiles available data on root exudation rates and exudate diversity across wetland plant species, thereby providing an overview of exudate dynamics in wetlands. Additionally, the synthesis reports environmental, biological, and analytical factors influencing both the rate and composition of root exudates. The analysis found that organic acids contributed the most to the compounds identified in wetland plant root exudates and were the most frequently analyzed compound class, accounting for 75 % of observations. By contrast, exudation rates of sugars, amino acids, and secondary metabolites were rarely reported, and their ecological roles in wetlands remain poorly understood. The literature synthesis identified a mismatch between studies on priming effects, which typically investigate the effects of sugars on SOC decomposition, and exudate studies, which commonly report organic acids as the dominant compounds. Analysis of data distribution across species functional types revealed that most available data came from graminoids and mangroves, while information on exudation rates of other herbaceous and woody plants remained limited. Within these groups, mangroves exhibited higher exudation rates for most organic acids compared to graminoids. Overall, the analysis highlighted that comparing exudation rates across studies remains challenging due to differences in collection methods and environmental conditions. Chapter III presents incubation experiments investigating whether priming effects in anoxic peat soils are driven by labile carbon exudate inputs (glucose), oxygen inputs, or their interaction. The experiments also assessed whether the exudate-to-microbial biomass ratio influences the direction of priming under anoxic conditions. Using a carbon stable isotope approach, respiration was distinguished as originating from peat SOC or from exudate-surrogates. The incubation experiments showed that glucose inputs alone induced a cumulative negative priming effect of -70 %. Priming effects were less negative under lower glucose inputs; however, even glucose-carbon inputs below the estimated microbial biomass carbon resulted in negative or zero priming. Oxygen inputs, by contrast, stimulated SOC mineralization, leading to strong positive priming effect of +376 %. When glucose was supplied in combination with oxygen, the magnitude of positive priming effect was reduced to +229 %. Both positive and negative priming effects persisted for several weeks during a legacy phase without further inputs and increased in magnitude. The data suggest that negative priming effects are driven by preferential substrate usage and are amplified in anoxic soils due to the exhaustion of terminal electron acceptors (TEA-depletion hypothesis) through exudate-fuelled respiration. Oxygen inputs overcome the limitation of electron acceptors by replenishing them and acting as electron acceptors themselves, thereby provoking positive priming effects. Chapter IV reports an incubation experiment comparing priming effects of different primary exudate compound classes by adding alanine (amino acid), glucose (sugar), or oxalic acid (organic acid) to anoxic peat. The temperature sensitivity of the priming effect was tested by conducting the incubation at two temperatures. It was further investigated whether the presence of nitrogen in exudates can influence the priming effect by applying an exudate mixture containing glucose and alanine. The incubation experiment found more negative cumulative priming effects in the exudate mixture (glucose and alanine) and in the glucose treatment (all < -76 %) than in the alanine (-36 % at 20 °C and -33 % at 10 °C) and the oxalic acid treatments (-29 % at 20°C and -43 % at 10 °C). Relative priming effects on anoxic peat SOC were observed to be mostly temperature-insensitive and negative regardless of the compound type or the presence of nitrogen in exudate inputs. The data suggest that changes in the composition of primary compounds in wetland root exudates are unlikely to alter the direction of priming effects on SOC, as long as soils remain anoxic. Chapter V presents a greenhouse microcosm experiment quantifying rhizosphere priming effects of two sedge species (Eriophorum spp.) with contrasting root morphologies (rhizomatous vs. bunch-forming) on litter buried beneath the plants in waterlogged peat. Using 13C-labeled litter, litter-derived respiration was quantified applying a two-end-member mixing model. Additionally, the role of plant traits in driving rhizosphere priming effects was investigated by analyzing enzyme activities through zymography and examining O₂ and CO₂ dynamics in the rhizosphere using a planar optode imaging system. Besides that, root oxygen loss was assessed in a hydroponic setup. The microcosm experiment revealed that litter decomposition was enhanced in the initial decomposition phase under both sedge species. Positive priming declined from +224 ± 57 % to -28 ± 17 % under Eriophorum angustifolium and from +214 ± 67 % to -24 ± 8 % under E. vaginatum within three months. Cumulative CO2 respiration from litter was approximately 85 % higher under rhizomatous E. angustifolium and 100 % higher under bunch-forming E. vaginatum compared to the unplanted control, although E. vaginatum exhibited a lower root oxygen loss rate than E. angustifolium. Oxygen loss was primarily observed at the tips of young roots. The β-glucosidase activity was mainly elevated around mature roots, likely more enhanced by dead root tissues than by exudate releases. Conversely, acid phosphatase activity was elevated around all roots and therefore likely driven by exudate and oxygen release. Overall, the cumulative positive rhizosphere priming effects of sedges on their litter were probably driven by a net plant-induced recharge of the electron acceptor capacity in the rhizosphere due to root oxygen loss, coupled with enhanced activities of carbon- and phosphorus-acquiring enzymes. In conclusion, the results of the thesis suggest that vegetation changes, such as the expansion of vascular plants into moss-dominated peatlands, could stimulate SOC and litter decomposition through root oxygen release, while exudate release acts to stabilize anoxic SOC. The findings imply that alterations in priming effects in wetlands under climate and vegetation changes are likely driven more by species-specific variation in root oxygen loss than by soil warming or by variation in the composition of primary root exudates. However, the role of secondary root exudates in wetland ecosystems, including their exudation rates and functions, remains to be clarified.