Ecological implications of organic carbon dynamics in the traps of aquatic carnivorous Utricularia plants

Abstract

Rootless aquatic carnivorous Utricularia exude up to 25% of their photosynthates into the trap lumen, which also harbours a complex microbial community thought to play a role in enhancing Utricularia nutrient acquisition. We investigated the composition of organic carbon in the trap fluid, its availability for microbial uptake, the influence of plant nutrient status and trap age on its biodegradability, and the composition of prokaryotic assemblages within the traps of three aquatic Utricularia species. Using ion chromatography and basal respiration rate measurements we confirmed that up to 30% of total dissolved organic carbon in Utricularia trap fluid in oligotrophic conditions was easily biodegradable compounds commonly found in plant root exudates (mainly glucose, fructose and lactate). The proportion of these compounds and their microbial utilisation decreased with increasing mineral nutrient supply and trap age. Fluorescence in situ hybridisation analyses showed that microbial trap assemblages are dominated by alpha and beta Proteobacteria, and that the assemblage composition is affected by changes in the ambient mineral nutrient supply. We suggest that organic carbon dynamics within the traps, involving both the plant and associated microbial assemblages, underlies the acquisition of key nutrients by Utricularia and may help explain the evolutionary success of the genus.

Ecological Traits of the Algae‐BearingTetrahymena utriculariae(Ciliophora) from Traps of the Aquatic Carnivorous PlantUtricularia reflexa

“…; Sirová et al. ). However, very little is known about their specific interactions and their roles in plant life cycle and nutrition.…”

“…; Sirová et al. , ), several authors reported the occurrence of highly abundant populations of mixotrophic ciliates (e.g. Płachno et al.…”

“…Besides their role in the acquisition of nutrients, the traps appear to represent a highly specific environment with distinct microbial communities (microbiomes) that colonize the trap lumen (Sirová et al. , ).…”

“…On one hand, the trap‐associated microorganisms live under extremely nutrient‐rich conditions with regard to organic carbon, phosphorus, and nitrogen (Sirová et al. , , ). Table characterizes the physico‐chemical properties in Utricularia trap lumen, detailing the highly specific aquatic environment with conditions of low pH, frequent anoxia or very low concentrations of dissolved oxygen, extremely high concentrations of total and dissolved organic carbon with high proportions of simple organic carbon compounds, and relatively high concentrations of different chemical species of total and dissolved nitrogen and phosphorus.…”

The mixotrophic nature of photosynthetic plants

“…2; Raven et al 2009). We do not consider carnivorous angiosperms in detail here, but note that they are photosynthetic (Juniper et al 1989;Raven et al 2009;Król et al 2012), can take up organic C in amino acids and peptides via transporters (Schulze et al 1999) and via endocytosis (Adlassnig et al 2012), but have a significant C cost in trap construction and maintenance and in enzyme secretion (Ellison and Adamec 2011;Sirová et al 2011).…”