Dataset Information

Inquiline predator increases nutrient-cycling efficiency of Nepenthes rafflesiana pitchers.

ABSTRACT: The modified-leaf pitchers of Nepenthes rafflesiana pitcher plants are aquatic, allochthonous ecosystems that are inhabited by specialist inquilines and sustained by the input of invertebrate prey. Detritivorous inquilines are known to increase the nutrient-cycling efficiency (NCE) of pitchers but it is unclear whether predatory inquilines that prey on these detritivores decrease the NCE of pitchers by reducing detritivore populations or increase the NCE of pitchers by processing nutrients that may otherwise be locked up in detritivore biomass. Nepenthosyrphus is a small and poorly studied genus of hoverflies and the larvae of one such species is a facultatively detritivorous predator that inhabits the pitchers of N. rafflesiana. We fitted a consumer-resource model to experimental data collected from this system. Simulations showed that systems containing the predator at equilibrium almost always had higher NCEs than those containing only prey (detritivore) species. We showed using a combination of simulated predator/prey exclusions that the processing of the resource through multiple pathways and trophic levels in this system is more efficient than that accomplished through fewer pathways and trophic levels. Our results thus support the vertical diversity hypothesis, which predicts that greater diversity across trophic levels results in greater ecosystem functioning.

SUBMITTER: Lam WN

PROVIDER: S-EPMC6936022 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Inquiline predator increases nutrient-cycling efficiency of <i>Nepenthes rafflesiana</i> pitchers.

Lam Weng Ngai WN Chou Ying Yi YY Leong Felicia Wei Shan FWS Tan Hugh Tiang Wah HTW

Biology letters 20191204 12

The modified-leaf pitchers of <i>Nepenthes rafflesiana</i> pitcher plants are aquatic, allochthonous ecosystems that are inhabited by specialist inquilines and sustained by the input of invertebrate prey. Detritivorous inquilines are known to increase the nutrient-cycling efficiency (NCE) of pitchers but it is unclear whether predatory inquilines that prey on these detritivores decrease the NCE of pitchers by reducing detritivore populations or increase the NCE of pitchers by processing nutrient ...[more]

PMID: 31795851

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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

Inquiline predator increases nutrient-cycling efficiency of Nepenthes rafflesiana pitchers.

Publications

Inquiline predator increases nutrient-cycling efficiency of <i>Nepenthes rafflesiana</i> pitchers.

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