Macrophyte landscape modulates lake ecosystem-level nitrogen losses through tightly coupled plant-microbe interactions

Abstract

Root functional diversity of submerged vegetation exerts a major effect on nitrogen (N) cycling in lake sediments. This fact, however, is neglected in current N-balance models because the links between the engineering role of plants and in situ microbial N cycling are poorly understood. We hypothesized that macrophyte species with high root oxygen loss (ROL) capacity promote the highest denitrification because of a higher abundance of ammonia oxidizers and tighter coupling between nitrifiers and denitrifier communities. We sampled five small ultraoligotrophic shallow lakes with abundant macrophyte cover including sediments dominated either by Isoetes spp. (high ROL), mixed communities of natopotamids (low ROL), and unvegetated sandy sediments. At each site, we quantified denitrification (DNT) rates and proxies for the abundance of denitrifiers (nirS and nirK genes), and both ammonia oxidizing archaea (AOA) and ammonia oxidizing bacteria (AOB) and the diversity of nirS-harboring bacteria. Vegetated sediments showed significantly higher abundances of N-cycling genes than bare sediments. Plant communities dominated by Isoetes generated sediments with higher redox and NO 2 3 concentrations and significantly higher DNT rates than natopotamidsdominated landscapes. Accordingly, increasing DNT rates were observed along the gradient from low ROL plants-bare sediments-high ROL plants. Significantly higher abundance of the archaeal amoA gene was recorded in sediments colonized by high ROL plants unveiling a key biogeochemical role for AOA in coupling macrophyte landscape and ecosystem denitrification.The global nitrogen cycle has been strongly modified by massive industrial fixation of nitrogen gas (N 2 ) for human use and by fossil-fuel combustions (Gruber and Galloway 2008). Current concentrations of bio-available nitrogen (N) forms are higher than ever in the human era (Fowler et al. 2013). Terrestrial and aquatic denitrification (DNT) and anammox processes are of special interest because they represent the only permanent removal pathway whereby bioavailable N is returned to inert N 2 gas (Rockstr€ om et al. 2009). The presence and specific composition of rooted plants is a major factor influencing DNT rates of soils and sediments (RisgaardPetersen and Jensen 1997). Plants can alter physicochemical factors known to control denitrification rates such as pH, oxygen, carbon sources and nitrate concentrations (Griffiths et al. 1997;Gacia et al. 2009). These modifications, in turn, influence the activity, diversity and abundance of rhizosphere nitrifiers and denitrifiers populations although few studies have reported quantitative evidences of these plantmicrobial interactions in lake ecosystems (Kofoed et al. 2012). Commonly, nitrification (NT) produces NO 2 3 under oxic conditions after ammonification while DNT requires suboxic conditions and is highly dependent on both NO 2 3 transport from aerobic to anaerobic zones and changes of the in situ redox conditions (Seitzinger et al. 2006).Submersed aquatic plants (SAV)...

Nitrate availability affects denitrification in Phragmites australis sediments

“…By affecting denitrification drivers (i.e. oxygen and carbon availability) in several ways, different macrophyte species may select for specific denitrifying communities in the rhizosphere and biofilms that respond differently to variable NO 3 − availability (Vila‐Costa et al., ; Veraart et al., , Yan et al., ).…”

Towards a Microbial Conservation Perspective in High Mountain Lakes

“…Nitrification helps to remove excessive ammonium nitrogen and prevent lakes from eutrophication. Thus, increasing evidence suggests that Archaea may play a significant role in ammonia oxidation in freshwaters in general, and specifically in alpine lakes with submerged vegetation (Vila-Costa et al 2016). In fact, the interaction between microbial ecology and macrophytes ecology determines the ecosystem-level denitrification and the submerged vegetation landscape has a major role in creating heterogeneity within the lakes that promotes microbial diversity (Vila-Costa et al 2016).…”

“…Thus, increasing evidence suggests that Archaea may play a significant role in ammonia oxidation in freshwaters in general, and specifically in alpine lakes with submerged vegetation (Vila-Costa et al 2016). In fact, the interaction between microbial ecology and macrophytes ecology determines the ecosystem-level denitrification and the submerged vegetation landscape has a major role in creating heterogeneity within the lakes that promotes microbial diversity (Vila-Costa et al 2016). A symbiotic or parasitic lifestyle even with Bacteria has been suggested for Pacearchaeota and Woesearchaeota, probably related to small genomes sizes and limited metabolic capabilities (Spang et al 2015;Ortiz-Alvarez and Casamayor 2016) but the gap of knowledge is certainly large.…”

Preface: Wetlands biodiversity and processes—tools for conservation and management

“…Rooted macrophytes, via radial oxygen loss and nutrient uptake, perform similar services, by trapping phosphorous in insoluble forms and favoring the loss of excess nitrogen via nitrification-coupled denitrification (Vila-Costa et al, 2016).…”