Dataset Information

Nepenthes pitchers are CO₂-enriched cavities, emit CO₂ to attract preys.

ABSTRACT: Carnivorous plants of the genus Nepenthes supplement their nutrient deficiency by capturing arthropods or by mutualistic interactions, through their leaf-evolved biological traps (pitchers). Though there are numerous studies on these traps, mostly on their prey capture mechanisms, the gas composition inside them remains unknown. Here we show that, Nepenthes unopened pitchers are CO₂-enriched 'cavities', when open they emit CO₂, and the CO₂ gradient around open pitchers acts as a cue attracting preys towards them. CO₂ contents in near mature, unopened Nepenthes pitchers were in the range 2500-5000 ppm. Gas collected from inside open N. khasiana pitchers showed CO₂ at 476.75 ± 59.83 ppm. CO₂-enriched air-streaming through N. khasiana pitchers (at 619.83 ± 4.53 ppm) attracted (captured) substantially higher number of aerial preys compared to air-streamed pitchers (CO₂ at 412.76 ± 4.51 ppm). High levels of CO₂ dissolved in acidic Nepenthes pitcher fluids were also detected. We demonstrate respiration as the source of elevated CO₂ within Nepenthes pitchers. Most unique features of Nepenthes pitchers, viz., high growth rate, enhanced carbohydrate levels, declined protein levels, low photosynthetic capacity, high respiration rate and evolved stomata, are influenced by the CO₂-enriched environment within them.

SUBMITTER: Baby S

PROVIDER: S-EPMC5595901 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Nepenthes pitchers are CO2-enriched cavities, emit CO2 to attract preys.

Baby Sabulal S Johnson Anil John AJ Zachariah Elavinamannil Jacob EJ Hussain Abdul Azeez AA

Scientific reports 20170912 1

Carnivorous plants of the genus Nepenthes supplement their nutrient deficiency by capturing arthropods or by mutualistic interactions, through their leaf-evolved biological traps (pitchers). Though there are numerous studies on these traps, mostly on their prey capture mechanisms, the gas composition inside them remains unknown. Here we show that, Nepenthes unopened pitchers are CO2-enriched 'cavities', when open they emit CO2, and the CO2 gradient around open pi ...[more]

PMID: 28900277

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Project description:Carnivorous pitcher plants are uniquely adapted to nitrogen limitation, using pitfall traps to acquire nutrients from insect prey. Pitcher plants in the genus Sarracenia may also use nitrogen fixed by bacteria inhabiting the aquatic microcosms of their pitchers. Here, we investigated whether species of a convergently evolved pitcher plant genus, Nepenthes, might also use bacterial nitrogen fixation as an alternative strategy for nitrogen capture. First, we constructed predicted metagenomes of pitcher organisms from three species of Singaporean Nepenthes using 16S rRNA sequence data and correlated predicted nifH abundances with metadata. Second, we used gene-specific primers to amplify and quantify the presence or absence of nifH directly from 102 environmental samples and identified potential diazotrophs with significant differential abundance in samples that also had positive nifH PCR tests. Third, we analyzed nifH in eight shotgun metagenomes from four additional Bornean Nepenthes species. Finally, we conducted an acetylene reduction assay using greenhouse-grown Nepenthes pitcher fluids to confirm nitrogen fixation is indeed possible within the pitcher habitat. Results show active acetylene reduction can occur in Nepenthes pitcher fluid. Variation in nifH from wild samples correlates with Nepenthes host species identity and pitcher fluid acidity. Nitrogen-fixing bacteria are associated with more neutral fluid pH, while endogenous Nepenthes digestive enzymes are most active at low fluid pH. We hypothesize Nepenthes species experience a trade-off in nitrogen acquisition; when fluids are acidic, nitrogen is primarily acquired via plant enzymatic degradation of insects, but when fluids are neutral, Nepenthes plants take up more nitrogen via bacterial nitrogen fixation. IMPORTANCE Plants use different strategies to obtain the nutrients that they need to grow. Some plants access their nitrogen directly from the soil, while others rely on microbes to access the nitrogen for them. Carnivorous pitcher plants generally trap and digest insect prey, using plant-derived enzymes to break down insect proteins and generate a large portion of the nitrogen that they subsequently absorb. In this study, we present results suggesting that bacteria living in the fluids formed by Nepenthes pitcher plants can fix nitrogen directly from the atmosphere, providing an alternative pathway for plants to access nitrogen. These nitrogen-fixing bacteria are only likely to be present when pitcher plant fluids are not strongly acidic. Interestingly, the plant's enzymes are known to be more active under strongly acidic conditions. We propose a potential trade-off where pitcher plants sometimes access nitrogen using their own enzymes to digest prey and at other times take advantage of bacterial nitrogen fixation.

Project description:Nepenthes is a genus comprising carnivorous tropical pitcher plants that have evolved trapping organs at the tip of their leaves for nutrient acquisition from insect trapping. Recent studies have applied proteomics approaches to identify proteins in the pitcher fluids for better understanding the carnivory mechanism, but protein identification is hindered by limited species-specific transcriptomes for Nepenthes. In this study, the proteomics informed by transcriptomics (PIT) approach was utilized to identify and compare proteins in the pitcher fluids of Nepenthes ampullaria, Nepenthes rafflesiana, and their hybrid Nepenthes × hookeriana through PacBio isoform sequencing (Iso-Seq) and liquid chromatography-mass spectrometry (LC-MS) proteomic profiling. We generated full-length transcriptomes from all three species of 80,791 consensus isoforms with an average length of 1,692 bp as a reference for protein identification. The comparative analysis found that transcripts and proteins identified in the hybrid N. × hookeriana were more resembling N. rafflesiana, both of which are insectivorous compared with omnivorous N. ampullaria that can derive nutrients from leaf litters. Previously reported hydrolytic proteins were detected, including proteases, glucanases, chitinases, phosphatases, nucleases, peroxidases, lipid transfer protein, thaumatin-like protein, pathogenesis-related protein, and disease resistance proteins. Many new proteins with diverse predicted functions were also identified, such as amylase, invertase, catalase, kinases, ligases, synthases, esterases, transferases, transporters, and transcription factors. Despite the discovery of a few unique enzymes in N. ampullaria, we found no strong evidence of adaptive evolution to produce endogenous enzymes for the breakdown of leaf litter. A more complete picture of digestive fluid protein composition in this study provides important insights on the molecular physiology of pitchers and carnivory mechanism of Nepenthes species with distinct dietary habits.

Project description:Hybridization is key to the evolution and diversity of plants in nature. Nepenthaceae comprises a family of diverse tropical carnivorous pitcher plant species with extensive hybridization. However, there is no study to date on the metabolite expression of hybrids in this family. We performed a non-targeted metabolomics analysis of the pitchers of two Nepenthes species with different dietary habits, namely, the semi-detritivorous N. ampullaria and carnivorous N. rafflesiana with their hybrid (N. × hookeriana) for a comparative study. The whole-pitcher samples were extracted in methanol:chloroform:water (3:1:1) via sonication-assisted extraction and analyzed using ultra-performance liquid chromatography time-of-flight mass spectrometry (UPLC-TOF-MS) followed by data analysis to profile chemical compositions. A total of 1,441 metabolite features were profiled from the three species in which 43.3% of features in the hybrid samples were not found in either of its parents. The partial least squares discriminant analysis (PLS-DA) found 324 metabolite features with variable in projection (VIP) values greater than one in which 55 features were statistically significant. This showed that the hybrid is closer to N. rafflesiana, which is consistent to the previous study on gene and protein expressions. A total of 105 metabolites were putatively identified with manual searches using public metabolite databases. Phenols were detected to be the most abundant secondary metabolites due to a high flavonoid content, especially in N. rafflesiana. The most abundant feature 476.3s:449.102 was found to be the most significant VIP for distinguishing between the three species as a chemical marker. This is the first study comparing metabolites in the carnivory organs of different Nepenthes species with comprehensive profiling and putative identification. The differential metabolite compositions in the pitchers of different species might have ecological implications with the hybrid showing intermediate phenotype between the parents as well as manifesting unique metabolites. However, there is no clear evidence of metabolites related to the differences in dietary habits between the hybrid and the two parent species.

Dataset Information

Nepenthes pitchers are CO₂-enriched cavities, emit CO₂ to attract preys.

Publications

Nepenthes pitchers are CO<sub>2</sub>-enriched cavities, emit CO<sub>2</sub> to attract preys.

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