Dataset Information

Endocytosis and Digestion in Carnivorous Pitcher Plants of the Family Sarraceniaceae.

ABSTRACT: Highly evolved carnivorous plants secrete digestive enzymes for degradation of trapped animals and absorb whole macromolecules from their prey by means of endocytosis. (1) Background: In the pitcher-plant family Sarraceniaceae, the production of enzymes is dubious and no evidence for endocytosis is known so far. (2) Methods: Heliamphora nutans, Darlingtonia californica, and nine taxa of Sarracenia are tested for cuticular pores, and for protease and endocytosis of the fluorescent protein analogue FITC-BSA, after 10-48 h of stimulation. (3) Results: Cuticular pores as a prerequisite for enzyme secretion and nutrient uptake are present in all tested species. Permeable cells form clusters in the inner epidermis of the pitchers, but are only little differentiated from impermeable epidermis cells. Proteases are found in S. psittacina, S. leucophylla, S. minor, S. oreophila, S. alabamensis, H. nutans, D. californica lacking only in S. flava and in S. purpurea ssp. purpurea, S. purpurea ssp. venosa, S. rosea, where enzyme production is possibly replaced by degradation via the extraordinary diverse inquiline fauna. S. leucophylla, S. minor, S. oreophila exhibit both protease production and endocytosis; S. psittacina, S. alabamensis, H. nutans, D. californica produce proteases only; no single species shows endocytosis without protease production. (4) Conclusions: Protease secretion seems to be a prerequisite for endocytotic nutrient uptake. Transport of FITC-BSA absorbed by endocytosis towards the vascular tissue of the trap leaves suggests that endocytosis of nutrients is more than a side effect of enzyme secretion.

SUBMITTER: Koller-Peroutka M

PROVIDER: S-EPMC6843295 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Endocytosis and Digestion in Carnivorous Pitcher Plants of the Family Sarraceniaceae.

Koller-Peroutka Marianne M Krammer Stefanie S Pavlik Anselm A Edlinger Manfred M Lang Ingeborg I Adlassnig Wolfram W

Plants (Basel, Switzerland) 20190924 10

Highly evolved carnivorous plants secrete digestive enzymes for degradation of trapped animals and absorb whole macromolecules from their prey by means of endocytosis. (1) Background: In the pitcher-plant family Sarraceniaceae, the production of enzymes is dubious and no evidence for endocytosis is known so far. (2) Methods: Heliamphora nutans, Darlingtonia californica, and nine taxa of Sarracenia are tested for cuticular pores, and for protease and endocytosis of the fluore ...[more]

PMID: 31554185

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Project description:BackgroundThe leaves of carnivorous pitcher plants harbor diverse communities of inquiline species, including bacteria and larvae of the pitcher plant mosquito (Wyeomyia smithii), which aid the plant by processing captured prey. Despite the growing appreciation for this microecosystem as a tractable model in which to study food web dynamics and the moniker of W. smithii as a 'keystone predator', very little is known about microbiota acquisition and assembly in W. smithii mosquitoes or the impacts of W. smithii-microbiota interactions on mosquito and/or plant fitness.ResultsIn this study, we used high throughput sequencing of bacterial 16S rRNA gene amplicons to characterize and compare microbiota diversity in field- and laboratory-derived W. smithii larvae. We then conducted controlled experiments in the laboratory to better understand the factors shaping microbiota acquisition and persistence across the W. smithii life cycle. Methods were also developed to produce axenic (microbiota-free) W. smithii larvae that can be selectively recolonized with one or more known bacterial species in order to study microbiota function. Our results support a dominant role for the pitcher environment in shaping microbiota diversity in W. smithii larvae, while also indicating that pitcher-associated microbiota can persist in and be dispersed by adult W. smithii mosquitoes. We also demonstrate the successful generation of axenic W. smithii larvae and report variable fitness outcomes in gnotobiotic larvae monocolonized by individual bacterial isolates derived from naturally occurring pitchers in the field.ConclusionsThis study provides the first information on microbiota acquisition and assembly in W. smithii mosquitoes. This study also provides the first evidence for successful microbiota manipulation in this species. Altogether, our results highlight the value of such methods for studying host-microbiota interactions and lay the foundation for future studies to understand how W. smithii-microbiota interactions shape the structure and stability of this important model ecosystem.

Project description:BackgroundCarnivorous pitcher plants (CPPs) use cone-shaped leaves to trap animals for nutrient supply but are not able to kill all intruders of their traps. Numerous species, ranging from bacteria to vertrebrates, survive and propagate in the otherwise deadly traps. This paper reviews the literature on phytotelmata of CPPs.PitcherFluid as a Habitat The volumes of pitchers range from 0·2 mL to 1·5 L. In Nepenthes and Cephalotus, the fluid is secreted by the trap; the other genera collect rain water. The fluid is usually acidic, rich in O(2) and contains digestive enzymes. In some taxa, toxins or detergents are found, or the fluid is extremely viscous. In Heliamphora or Sarracenia, the fluid differs little from pure water.InquilineDiversity Pitcher inquilines comprise bacteria, protozoa, algae, fungi, rotifers, crustaceans, arachnids, insects and amphibia. The dominant groups are protists and Dipteran larvae. The various species of CPPs host different sets of inquilines. Sarracenia purpurea hosts up to 165 species of inquilines, followed by Nepenthes ampullaria with 59 species, compared with only three species from Brocchinia reducta. Reasons for these differences include size, the life span of the pitcher as well as its fluid. MUTUALISTIC: Activities Inquilines closely interact with their host. Some live as parasites, but the vast majority are mutualists. Beneficial activities include secretion of enzymes, feeding on the plant's prey and successive excretion of inorganic nutrients, mechanical break up of the prey, removal of excessive prey and assimilation of atmospheric N(2).ConclusionsThere is strong evidence that CPPs influence their phytotelm. Two strategies can be distinguished: (1) Nepenthes and Cephalotus produce acidic, toxic or digestive fluids and host a limited diversity of inquilines. (2) Genera without efficient enzymes such as Sarracenia or Heliamphora host diverse organisms and depend to a large extent on their symbionts for prey utilization.

Dataset Information

Endocytosis and Digestion in Carnivorous Pitcher Plants of the Family Sarraceniaceae.

Publications

Endocytosis and Digestion in Carnivorous Pitcher Plants of the Family Sarraceniaceae.

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