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

Sirová, Dagmara; Šantrůček, Jiří; Adamec, Lubomír; Bárta, Jiří; Borovec, Jakub; Pech, Jiří; Owens, Sarah M.; Šantrůčková, Hana; Schäufele, Rudi; Štorchová, Helena; Vrba, Jaroslav

doi:10.1093/aob/mcu067

Cited by 18 publications

(17 citation statements)

References 53 publications

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“…Plant-associated N 2 fixation has been considered as a potential source of N for carnivorous plants with pitcher or snapping traps (Prankevicius and Cameron, 1991 ; Albino et al, 2006 ). Although N 2 fixing bacteria represent up to 16% of the bacterial community in Utricularia traps, N 2 fixation contributed less than 1% of daily N gain of Utricularia (Sirova et al, 2014 ). This limited N 2 fixation is likely due to the high concentration of NH 4− N in the Utricularia trap fluid, resulting from fast turnover of organic matter.…”

Section: Resultsmentioning

confidence: 99%

Metatranscriptome analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species

et al. 2015

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In the carnivorous plant genus Genlisea a unique lobster pot trapping mechanism supplements nutrition in nutrient-poor habitats. A wide spectrum of microbes frequently occurs in Genlisea's leaf-derived traps without clear relevance for Genlisea carnivory. We sequenced the metatranscriptomes of subterrestrial traps vs. the aerial chlorophyll-containing leaves of G. nigrocaulis and of G. hispidula. Ribosomal RNA assignment revealed soil-borne microbial diversity in Genlisea traps, with 92 genera of 19 phyla present in more than one sample. Microbes from 16 of these phyla including proteobacteria, green algae, amoebozoa, fungi, ciliates and metazoans, contributed additionally short-lived mRNA to the metatranscriptome. Furthermore, transcripts of 438 members of hydrolases (e.g., proteases, phosphatases, lipases), mainly resembling those of metazoans, ciliates and green algae, were found. Compared to aerial leaves, Genlisea traps displayed a transcriptional up-regulation of endogenous NADH oxidases generating reactive oxygen species as well as of acid phosphatases for prey digestion. A leaf-vs.-trap transcriptome comparison reflects that carnivory provides inorganic P- and different forms of N-compounds (ammonium, nitrate, amino acid, oligopeptides) and implies the need to protect trap cells against oxidative stress. The analysis elucidates a complex food web inside the Genlisea traps, and suggests ecological relationships between this plant genus and its entrapped microbiome.

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Section: Resultsmentioning

confidence: 99%

Metatranscriptome analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species

et al. 2015

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“…These species are generally more abundant in organic‐rich waters (John et al., ) and organisms with this trophic character can be most competitive under non‐limiting nutrient concentrations (Burkholder, Glibert, & Skelton, ; Sommer, ; Willen, ). Due to the degradation of trapped prey and detritus, the nutrient concentrations in traps of Utricularia can be 2–3 orders of magnitude higher than those in the ambient water (Sirová et al., , ), this would place these algae well in the traps of Utricularia . Moreover, Chilomonas has demonstrated good growth in media containing organic detritus and bacteria (Scherwass, Fischer, & Arndt, ), across a range of CO 2 and O 2 concentrations, but best at low O 2 and high CO 2 (Pace & Ireland, ) and also tolerating acid conditions (Nixdorf, Fyson, & Krumbeck, ), so it is highly adapted to the trap lumen environment.…”

Section: Discussionmentioning

confidence: 99%

The role of phytoplankton in the diet of the bladderwort Utricularia australis R.Br. (Lentibulariaceae)

2018

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It is becoming more apparent that the aquatic carnivorous plants Utricularia (Lentibulariaceae) can capture and utilise a wide range of small aquatic organisms. Although they can take up nutrients directly from the water by rootless shoots, much of their overall nutrition comes from prey caught in their traps. Most of the early literature was focused mainly on animal prey, hence the term carnivorous to describe Utricularia spp., but more recently the contribution of other microorganisms and detritus to their diet is being realised. Specifically, the importance of the phytoplankton in traps as prey is proving interesting. However, most investigations have focused on the trap communities with few comparisons to phytoplankton as potential prey, which could reveal the occurrence of feeding selectivity. The eurytopic species Utricularia australis was surveyed across 12 sites in central Italy in lentic waterbodies ranging from oligotrophic to eutrophic. Phytoplankton communities outside the traps were composed of 135 taxa from 21 orders belonging to eight phyla and the algal community in the traps comprised 124 taxa from 17 orders belonging to eight phyla, recorded from all sampling sites. Among the 12 sites phytoplankton communities were highly diverse; however, communities inside and outside the traps at each site were very similar. This similarity indicated that feeding was not selective. Algal movements are not able to elicit a trap response, yet around 70% of the traps contained phytoplankton only (no animal prey). Therefore, regular spontaneous trap firing, known to occur in U. australis, is thought to be responsible for the similarities in trap and plankton algal communities. At two sites, a Euglenophyte (Lepocinclis sp.) and a Cryptophyte (Chilomonas sp.) proliferated, which were otherwise very rare in the phytoplankton community. This is indicative of favourable growth conditions in the traps and possibly of commensal relationships. It seems that the diet requirements of U. australis are met by having a highly varied prey spectrum.

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“…; Sirová et al. , ). While the protistan biomass in traps is known to be largely dominated by the ciliate, its ecology has not been studied.…”

Section: Physico‐chemical Properties Of the Environment Inside Utricumentioning

confidence: 96%

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

Šimek

Pitsch

Salcher

et al. 2016

J Eukaryotic Microbiology

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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.

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

Cited by 18 publications

References 53 publications

Metatranscriptome analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species

Metatranscriptome analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species

The role of phytoplankton in the diet of the bladderwort Utricularia australis R.Br. (Lentibulariaceae)

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

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