Fluorescently Labeled Bacteria as a Tracer to Reveal Novel Pathways of Organic Carbon Flow in Aquatic Ecosystems

Elucidating trophic interactions, such as predation and its effects, is a frequent task for many researchers in ecology. The study of microbial ...

Biology Centre CAS

The rootless, aquatic Utricularia species belong to the largest and most cosmopolitan carnivorous plant genus. Populations of Utricularia plants are an important component of many standing, nutrient-poor, and humic waters. Carbon (C) allocation is an aspect of Utricularia's ecophysiology that has not been studied previously and there is considerable uncertainty about the functional and ecological benefit of the trap-associated microbial community and the potential role played by C exudation in enhancing plant-microbe interactions. A 13C-labelling experiment was conducted in greenhouse conditions to determine the C allocation between plant tissues of increasing age and trap fluid in two Utricularia species. Both species allocated a majority of the newly fixed C into the fast growing shoot apex (46.1+/-8.6% in U. vulgaris and 56.1% in U. australis). Carbon allocation rapidly decreased with increasing age of the shoot, constituting only 8.0+/-4.0% and 6.7% of the total newly fixed C in the oldest analysed segments in U. vulgaris and U. australis, respectively. In the trap-bearing shoot segments, the ratio of C exuded into the trap fluid to that in plant tissues increased markedly with age--in the oldest analysed segments twice as much newly fixed C was allocated into the trap fluid than the plant tissue. Overall, a significant amount of the newly fixed C, approximately 25% (U. vulgaris) and 20% (U. australis), was allocated to the trap fluid. The importance of C exudation for the development of the microbial community associated with the traps as well as for the growth and ecology of aquatic Utricularia is discussed.

Utricularia carnivory revisited: plants supply photosynthetic carbon to traps.

Rootless carnivorous plants of the genus Utricularia are important components of many standing waters worldwide, as well as suitable model organisms for studying plant-microbe interactions. In this study, an investigation was made of the importance of microbial dinitrogen (N2) fixation in the N acquisition of four aquatic Utricularia species and another aquatic carnivorous plant, Aldrovanda vesiculosa.

Dinitrogen fixation associated with shoots of aquatic carnivorous plants: is it ecologically important?

Trap fluid of aquatic carnivorous plants of the genus Utricularia hosts specific microbiomes consisting of commensal pro- and eukaryotes of largely unknown ecology. We examined the characteristics and dynamics of bacteria and the three dominant eukaryotes, i.e. the algae-bearing ciliate Tetrahymena utriculariae (Ciliophora), a green flagellate Euglena agilis (Euglenophyta), and the alga Scenedesmus alternans (Chlorophyta), associated with the traps of Utricularia reflexa. Our study focused on ecological traits and life strategies of the highly abundant ciliate whose biomass by far exceeds that of other eukaryotes and bacteria independent of the trap age. The ciliate was the only bacterivore in the traps, driving rapid turnover of bacterial standing stock. However, given the large size of the ciliate and the cell-specific uptake rates of bacteria we estimated that bacterivory alone would likely be insufficient to support its apparent rapid growth in traps. We suggest that mixotrophy based on algal symbionts contributes significantly to the diet and survival strategy of the ciliate in the extreme (anaerobic, low pH) trap-fluid environment. We propose a revised concept of major microbial interactions in the trap fluid where ciliate bacterivory plays a central role in regeneration of nutrients bound in rapidly growing bacterial biomass.

Ecological Traits of the Algae-Bearing Tetrahymena utriculariae (Ciliophora) from Traps of the Aquatic Carnivorous Plant Utricularia reflexa.

The genus Tetrahymena (Ciliophora, Oligohymenophorea) probably represents the best studied ciliate genus. At present, more than forty species have been described. All are colorless, i.e. they do not harbor symbiotic algae, and as aerobes they need at least microaerobic habitats. Here, we present the morphological and molecular description of the first green representative, Tetrahymena utriculariae n. sp., living in symbiosis with endosymbiotic algae identified as Micractinium sp. (Chlorophyta). The full life cycle of the ciliate species is documented, including trophonts and theronts, conjugating cells, resting cysts and dividers. This species has been discovered in an exotic habitat, namely in traps of the carnivorous aquatic plant Utricularia reflexa (originating from Okavango Delta, Botswana). Green ciliates live as commensals of the plant in this anoxic habitat. Ciliates are bacterivorous, however, symbiosis with algae is needed to satisfy cell metabolism but also to gain oxygen from symbionts. When ciliates are cultivated outside their natural habitat under aerobic conditions and fed with saturating bacterial food, they gradually become aposymbiotic. Based on phylogenetic analyses of 18S rRNA and mitochondrial cox1 genes T. utriculariae forms a sister group to Tetrahymena thermophila.

The Green Tetrahymena utriculariae n. sp. (Ciliophora, Oligohymenophorea) with Its Endosymbiotic Algae (Micractinium sp.), Living in Traps of a Carnivorous Aquatic Plant.

A survey of the ecological variability within 52 populations of Schoenoplectus californicus (C.A. Mey.) Soják across its distributional range revealed that it is commonly found in nitrogen (N) limited areas, but rarely in phosphorus limited soils. We explored the hypothesis that S. californicus supplements its nitrogen demand by bacterial N2-fixation processes associated with its roots and rhizomes. We estimated N2-fixation of diazotrophs associated with plant rhizomes and roots from several locations throughout the species' range and conducted an experiment growing plants in zero, low, and high N additions. Nitrogenase activity in rhizomes and roots was measured using the acetylene reduction assay. The presence of diazotrophs was verified by the detection of the nifH gene. Nitrogenase activity was restricted to rhizomes and roots and it was two orders of magnitude higher in the latter plant organs (81 and 2032 nmol C2H4 g DW-1 d-1, respectively). Correspondingly, 40x more nifH gene copies were found on roots compared to rhizomes. The proportion of the nifH gene copies in total bacterial DNA was positively correlated with the nitrogenase activity. In the experiment, the contribution of fixed N to the plant N content ranged from 13.8% to 32.5% among clones from different locations. These are relatively high values for a non-cultivated plant and justify future research on the link between N-fixing bacteria and S. californicus production.

Heterotrophic N2-fixation contributes to nitrogen economy of a common wetland sedge, Schoenoplectus californicus.

Lake Medard is an oligotrophic post-mining lake characterised by ferruginous bottom waters, with marked redox gradients resulting from iron (Fe) and nitrogen (N) speciation and accompanying depth-dependent variations in the abundance of volatile fatty acids (VFAs), pH and alkalinity. The lacustrine system is meromictic, featuring a dysoxic hypolimnion and an anoxic monimolimnion with relatively high concentrations of sulfate (SO42-, 19 ± 2 mM) and Fe(ii) (127 ± 17 μM). An increase in dissolved manganese is also observed with increasing depth, together with a general lack of sulfide, which can only be detected at the sediment-water interface at concentrations of ∼0.30 μM. In the hypolimnion, nitrate (NO3-) becomes progressively depleted and ammonium (NH4+) dominates the dissolved N inventory (up to 185 ± 13 μM). Here we describe the biogeochemical disequilibrium conditions governing critical mineralogical transformations involving Fe and phosphorus (P) co-precipitation in the dysoxic-to-anoxic bottom water column. A combination of mineral equilibrium modelling and synchrotron-based diffraction and spectroscopic techniques was applied to investigate the minerals comprising the upper anoxic sediments. The combined dataset indicates that elemental recycling on and below the hypolimnion promote the precipitation of FeOOH polymorphs that accumulate as heterogeneous mineral clusters. Changes in the relative abundance of bacterioplankton taxa with increasing water depth point to a link between the activity of certain members of Proteobacteria and the co-recycling of carbon (C), N, and Fe stocks. Such a redox recycling process seems to lead to P stabilisation into organic-rich Fe-(oxyhydr)oxides near and above the anoxic sediment-water interface (SWI).

Iron and nitrogen cycling, bacterioplankton community composition and mineral transformations involving phosphorus stabilisation in the ferruginous hypolimnion of a post-mining lake.

Utricularia are rootless aquatic carnivorous plants which have recently attracted the attention of researchers due to the peculiarities of their miniaturized genomes. Here, we focus on a novel aspect of Utricularia ecophysiology-the interactions with and within the complex communities of microorganisms colonizing their traps and external surfaces.

Hunters or farmers? Microbiome characteristics help elucidate the diet composition in an aquatic carnivorous plant.

AbstractFollowing publication of the original article [1], the author reported an error in Fig. 3.

Dagmara Sirova

Department of Aquatic Microbial Ecology,
Institute of Hydrobiology,
Department of Aquatic Microbial Ecology, Institute of Hydrobiology

Biology Centre CAS

Fluorescently Labeled Bacteria as a Tracer to Reveal Novel Pathways of Organic Carbon Flow in Aquatic Ecosystems

Dagmara Sirova

.css-o250i3{font-size:18px;font-family:Open Sans,sans-serif;line-height:21.6px;}Department of Aquatic Microbial Ecology,Institute of Hydrobiology,Department of Aquatic Microbial Ecology, Institute of Hydrobiology

Biology Centre CAS

Fluorescently Labeled Bacteria as a Tracer to Reveal Novel Pathways of Organic Carbon Flow in Aquatic Ecosystems

Department of Aquatic Microbial Ecology,
Institute of Hydrobiology,
Department of Aquatic Microbial Ecology, Institute of Hydrobiology