The Metagenome of Utricularia gibba's Traps: Into the Microbial Input to a Carnivorous Plant

Alcaraz, Luis David; Martínez-Sánchez, Shamayim; Torres, Ignacio; Ibarra-Laclette, Enrique; Herrera-Estrella, Luis

doi:10.1371/journal.pone.0148979

Cited by 23 publications

(16 citation statements)

References 78 publications

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“…The larger microbial diversity observed in ruderal plants shows the commitment of wild plants to their microbes, fostering plant-microbe relationships which are not observed in domesticated cultivars (Wissuwa et al, 2009). We have previously tested other non-domesticated plants, such as the aquatic carnivorous bladderwort Utricularia gibba (Alcaraz et al 2016) and the bryophyte species…”

Section: Discussionmentioning

confidence: 99%

Testing the two-step model of plant root microbiome acquisition under multiple plant species and soil sources

Barajas

Martínez-Sánchez

Romero

et al. 2020

Preprint

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The two-step model for plant root microbiomes considers soil as the primary microbial source. Active selection of the plant's bacterial inhabitants results in a biodiversity decrease towards roots. We collected in situ ruderal plant roots and their soils and used these soils as the main microbial input for single genotype tomatoes grown in a greenhouse. We massively sequenced the 16S rRNA and shotgun metagenomes of the soils, in situ plants, and tomato roots. Tomato roots did follow the two-step model, while ruderal plants did not. Ruderal plants and their soils are closer than tomato and its soil, based on protein comparisons. We calculated a metagenomic tomato root core of 51 bacterial genera and 2,762 proteins, which could be the basis for microbiome-oriented plant breeding programs. The tomato and ruderal metagenomic differences are probably due to plant domestication trade-offs, impacting plantmicrobe interactions.

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Section: Discussionmentioning

confidence: 99%

Testing the two-step model of plant root microbiome acquisition under multiple plant species and soil sources

Barajas

Martínez-Sánchez

Romero

et al. 2020

Preprint

Self Cite

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“…In accordance with the latter possibility, there is increasing evidence that some specialized prokaryotes and protists form a peculiar trap microbiome (Alcaraz et al. ; Alkhalaf et al. ; Płachno et al.…”

Section: Physico‐chemical Properties Of the Environment Inside Utricumentioning

confidence: 82%

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

Section: Physico‐chemical Properties Of the Environment Inside Utricumentioning

confidence: 99%

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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“…It is interesting that a ribonuclease expressed in Arabidopsis and tomato roots is expressed in the trap of the rootless U. gibba, perhaps suggesting that many of the nutrient uptake functions of root systems were re-deployed in the traps of these carnivorous plants. Moreover, analysis of the microbiome of the U. gibba traps showed that many bacterial species normally present in the plant rhizosphere are present in U. gibba traps [25]. It has been reported that secretory ribonucleases play an important role in phosphate and nitrogen scavenging in the gut of humans and zebrafish [44].…”

Section: Discussionmentioning

confidence: 99%

“…In Utricularia, quadrifid glands play an important role in phosphatase secretion for hydrolysis of organic phosphorus compounds [20,23,24]. It has also been suggested that zooplankton communities and microorganisms inside the trap could also play an important role in the process of prey digestion [24,25].…”

Section: Introductionmentioning

confidence: 99%

Agrobacterium tumefaciens mediated transformation of the aquatic carnivorous plant Utricularia gibba

2020

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Background: The genus Utricularia belongs to Lentibulariaceae, the largest family of carnivorous plants, which includes terrestrial, epiphytic and aquatic species. The development of specialized structures that evolved for carnivory is a feature of this genus that has been of great interest to biologists since Darwin's early studies. Utricularia gibba is itself an aquatic plant with sophisticated bladder traps having one of the most complex suction mechanisms for trapping prey. However, the molecular characterization of the mechanisms that regulate trap development and the biophysical processes involved in prey trapping are still largely unknown due to the lack of a simple and reproducible gene transfer system. Results:Here, we report the establishment of a simple, fast and reproducible protocol for genetic transformation of U. gibba based on the T-DNA of Agrobacterium tumefaciens. An in vitro selection system using Phosphinotricin as a selective agent was established for U. gibba. Plant transformation was confirmed by histochemical GUS assays and PCR and qRT-PCR analyses. We report on the expression pattern of the 35S promoter and of the promoter of a trapspecific ribonuclease gene in transgenic U. gibba plants. Conclusions:The genetic transformation protocol reported here is an effective method for studying developmental biology and functional genomics of this genus of carnivorous plants and advances the utility of U. gibba as a model system to study developmental processes involved in trap formation.

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The Metagenome of Utricularia gibba's Traps: Into the Microbial Input to a Carnivorous Plant

Cited by 23 publications

References 78 publications

Testing the two-step model of plant root microbiome acquisition under multiple plant species and soil sources

Testing the two-step model of plant root microbiome acquisition under multiple plant species and soil sources

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

Agrobacterium tumefaciens mediated transformation of the aquatic carnivorous plant Utricularia gibba

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