Radial oxygen loss from roots of Vallisneria spiralis L.: biogeochemical implications in eutrophic aquatic ecosystems

Eutrophication and the accumulation of organic matter have been addressed as the major factors determining the decline of benthic vegetation in impacted water bodies and the consequent loss of key ecosystemic functions. In freshwater environments the literature reports submersed macrophyte die-back events and the switch to free-floating and floating-leaved plants dominated states. Species-specific differences in macrophyte response along organic gradients are evident. Some species have developed adaptations that allow not only their survival along pronounced gradients of sedimentary organic content but also their fast response to short-term variations of pore water chemistry, as those occurring seasonally in freshwater temperate ecosystems. Vallisneria spiralis L. (Hydrocharitaceae family), a perennial stoloniferous species, is tolerant to eutrophication and colonizes both lentic and lotic environments. It performs photosynthesis in low light conditions, grows in nutrient-rich waters and on a wide range of substrates, from gravel bottoms to organic-rich muddy sediments. The aim of this thesis is to investigate the role of a tolerant rooted macrophyte in the regulation of biogeochemical dynamics and the interactions with microbial communities (with a particular focus on nitrogen cycle) in freshwater ecosystems undergoing eutrophication processes. Different methodological approaches are adopted (i.e. hydroponic incubations of plant tissues and intact plants, microcosm incubations, characterization of pore water and measurements of benthic fluxes) and the following aspects are evaluated: I) direct (uptake) and indirect (oxygen release) effects of V. spiralis presence on pore water features and redox-dependent processes; II) V. spiralis plasticity to colonize substrates with increasing organic content and changes of its influence on sediment chemistry and microbial activity along the gradient; III) relation between assimilative (mediated by vegetation) and dissimilative nitrogen processes (mediated by bacteria) when nitrogen is not limiting. The key point is the evaluation of the effect of radial oxygen loss by V. spiralis on benthic biogeochemical dynamics. Oxygen released by roots has the potential to alter the chemical environment within sediments, with cascade effects on nutrient and gas exchanges at the water-sediment interface. Relevant consequences have been demonstrated for plants growing in oligotrophic systems, while the effects in organic-rich substrates are scantily explored. The outcomes of the present work show that V. spiralis releases a great amount of the photosynthetically produced oxygen to the rhizosphere, affecting significantly the redox-dependent processes. Multiple evidences support the hypothesis that this plant varies seasonally the oxygen quota transported to the below-ground tissues to counteract the changing interstitial chemical conditions. Even if radial oxygen loss represents a small fraction in the plant oxygen economy, it can significantly affect the sediment biogeochemistry of eutrophic sites, representing a relevant amount of the daily benthic oxygen demand. V. spiralis acts as an engineer species controlling actively interstitial features (NH4+, NOx-, PO43-, Fe2+ and CH4) over a wide range of trophic conditions and along its whole vegetative cycle. In sediments with a moderate organic enrichment, radial oxygen loss promotes denitrification coupled to nitrification, thus enhancing nitrogen loss and the ecosystem capacity to control nitrogen contamination. Furthermore, the high nitrogen availability in both pore water and water column weakens the competition between macrophytes and nitrifying and denitrifying bacteria, favoring nitrogen removal through a combination of plant uptake and dissimilative microbial processes. However, at extremely elevated organic enrichment, vegetated sediment lose their role as nitrogen traps due to nitrification inhibition and plant stress induced by very reduced conditions. In summary, V. spiralis has the potential to withstand large perturbations of sedimentary features, being able to colonize organic matter impacted substrates. Even pore water conditions potentially hostile to roots do not affect its function as a benthic metabolism regulator. This macrophyte plays a crucial role in driving water-sediment exchanges of gases and nutrients, partially buffering the negative effects of organic enrichment connected to eutrophication. Moreover, it modifies sedimentary features, with positive feedbacks for water bodies restoration (i.e. regeneration of ferric iron buffer and phosphorus retention in sediment, stimulation of coupled nitrification-denitrification, reduction of internal organic load) which makes this plant an interesting option in programs for improving sediment conditions and favoring ecosystem recovery.