RESUMO
Microbial communities perform various functions, many of which contribute to ecosystem-level nutrient cycling via decomposition. Factors influencing leaf detrital decomposition are well understood in terrestrial and aquatic ecosystems, but much less is known about arthropod detrital inputs. Here, we sought to infer how differences in arthropod detritus affect microbial-driven decomposition and community function in a carnivorous pitcher plant, Sarracenia purpurea. Using sterile mesh bags filled with different types of sterile arthropod prey, we assessed if prey type influenced the rate of decomposition in pitcher plants over 7 weeks. Additionally, we measured microbial community composition and function, including hydrolytic enzyme activity and carbon substrate use. When comparing decomposition rates, we found that ant and beetle prey with higher exoskeleton content lost less mass compared with fly prey. We observed the highest protease activity in the fly treatment, which had the lowest exoskeleton content. Additionally, we saw differences in the pH of the pitcher fluid, driven by the ant treatment which had the lowest pH. According to our results from 16S rRNA gene metabarcoding, prey treatments with the highest bacterial amplicon sequence variant (ASV) richness (ant and beetle) were associated with prey that lost a lower proportion of mass over the 7 weeks. Overall, arthropod detritus provides unique nutrient sources to decomposer communities, with different prey influencing microbial hydrolytic enzyme activity and composition. IMPORTANCE: Microbial communities play pivotal roles in nutrient cycling via decomposition and nutrient transformation; however, it is often unclear how different substrates influence microbial activity and community composition. Our study highlights how different types of insects influence decomposition and, in turn, microbial composition and function. We use the aquatic pools found in a carnivorous pitcher plant as small, discrete ecosystems that we can manipulate and study independently. We find that some insect prey (flies) breaks down faster than others (beetles or ants) likely because flies contain more things that are easy for microbes to eat and derive essential nutrients from. This is also reflected in higher enzyme activity in the microbes decomposing the flies. Our work bridges a knowledge gap about how different substrates affect microbial decomposition, contributing to the broader understanding of ecosystem function in a nutrient cycling context.
Assuntos
Formigas , Microbiota , Sarraceniaceae , Animais , Sarraceniaceae/microbiologia , Sarraceniaceae/metabolismo , Formigas/microbiologia , Artrópodes , Bactérias/classificação , Bactérias/genética , Bactérias/metabolismo , Bactérias/isolamento & purificação , Besouros/microbiologia , RNA Ribossômico 16S/genética , Ecossistema , Cadeia AlimentarRESUMO
BACKGROUND AND AIMS: The carnivorous pitcher plants of the genus Nepenthes have evolved modified leaves that act as pitcher traps. The traps are specialized for prey attraction, capture, digestion and nutrient uptake but not for photosynthetic assimilation. METHODS: In this study, we used antibodies against different photosynthetic (D1, Lhcb2, Lhcb4, RbcL) and respiratory-related (AOX, COXII) proteins for semi-quantification of these proteins in the assimilation part of the leaves and the pitcher traps of different Nepenthes species and hybrids. Different functional zones of the trap and the traps from different ontogenetic stages were investigated. The pitcher traps of the distantly related species Sarracenia purpurea ssp. venosa were used as an outgroup. In addition, chlorophyll fluorescence and infrared gas analysis were used for measurements of the net rate of photosynthesis (AN) and respiration in the dark (RD). KEY RESULTS: The pitcher traps contained the same or lower abundance of photosynthesis-related proteins in accordance with their low AN in comparison to the assimilation part of the leaves. Surprisingly, all traps contained a high amount of alternative oxidase (AOX) and low amount of cytochrome c oxidase subunit II (COX II) than in the assimilation part of the leaves. Thermal imaging did not confirm the role of AOX in pitcher thermogenesis. CONCLUSIONS: The pitcher traps contain a high amount of AOX enzyme. The possible role of AOX in specialized pitcher tissue is discussed based on knowledge of the role and function of AOX in non-carnivorous plants. The roles of AOX in prey attraction, balance between light and dark reactions of photosynthesis, homeostasis of reactive oxygen species, digestive physiology and nutrient assimilation are discussed.
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Planta Carnívora , Sarraceniaceae , Proteínas Mitocondriais , Compostos Orgânicos , Oxirredutases , Proteínas de Plantas/metabolismo , Sarraceniaceae/metabolismoRESUMO
Incremental increases in a driver variable, such as nutrients or detritus, can trigger abrupt shifts in aquatic ecosystems that may exhibit hysteretic dynamics and a slow return to the initial state. A model system for understanding these dynamics is the microbial assemblage that inhabits the cup-shaped leaves of the pitcher plant Sarracenia purpurea. With enrichment of organic matter, this system flips within three days from an oxygen-rich state to an oxygen-poor state. In a replicated greenhouse experiment, we enriched pitcher-plant leaves at different rates with bovine serum albumin (BSA), a molecular substitute for detritus. Changes in dissolved oxygen (DO) and undigested BSA concentration were monitored during enrichment and recovery phases. With increasing enrichment rates, the dynamics ranged from clockwise hysteresis (low), to environmental tracking (medium), to novel counter-clockwise hysteresis (high). These experiments demonstrate that detrital enrichment rate can modulate a diversity of hysteretic responses within a single aquatic ecosystem, and suggest different management strategies may be needed to mitigate the effects of high vs. low rates of detrital enrichment.
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Ecossistema , Sarraceniaceae , Modelos Biológicos , Folhas de PlantaRESUMO
Resource variation along abiotic gradients influences subsequent trophic interactions and these effects can be transmitted through entire food webs. Interactions along abiotic gradients can provide clues as to how organisms will face changing environmental conditions, such as future range shifts. However, it is challenging to find replicated systems to study these effects. Phytotelmata, such as those found in carnivorous plants, are isolated aquatic communities and thus form a good model for the study of replicated food webs. Due to the degraded nature of the prey, molecular techniques provide a useful tool to study these communities. We studied the pitcher plant Sarracenia purpurea L. in allochthonous populations along an elevational gradient in the Alps and Jura. We predicted that invertebrate richness in the contents of the pitcher plants would decrease with increasing elevation, reflecting harsher environmental conditions. Using metabarcoding of the COI gene, we sequenced the invertebrate contents of these pitcher plants. We assigned Molecular Operational Taxonomic Units at ordinal level as well as recovering species-level data. We found small but significant changes in community composition with elevation. These recovered sequences could belong to invertebrate prey, rotifer inquilines, pollinators and other animals possibly living inside the pitchers. However, we found no directional trend or site-based differences in MOTU richness with elevational gradient. Use of molecular techniques for dietary or contents analysis is a powerful way to examine numerous degraded samples, although factors such as DNA persistence and the relationship with species presence still have to be completely determined.
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Carnívoros/genética , Código de Barras de DNA Taxonômico , Fenômenos Fisiológicos Vegetais/genética , Sarraceniaceae/fisiologia , Altitude , Animais , Biodiversidade , Carnívoros/fisiologia , DNA/genética , DNA/isolamento & purificação , Ecossistema , Cadeia Alimentar , Plantas/genética , Sarraceniaceae/genéticaRESUMO
The importance of predators in influencing community structure is a well-studied area of ecology. However, few studies test ecological hypotheses of predation in multi-predator microbial communities. The phytotelmic community found within the water-filled leaves of the pitcher plant, Sarracenia purpurea, exhibits a simple trophic structure that includes multiple protozoan predators and microbial prey. Using this system, we sought to determine whether different predators target distinct microorganisms, how interactions among protozoans affect resource (microorganism) use, and how predator diversity affects prey community diversity. In particular, we endeavored to determine if protozoa followed known ecological patterns such as keystone predation or generalist predation. For these experiments, replicate inquiline microbial communities were maintained for seven days with five protozoan species. Microbial community structure was determined by 16S rRNA gene amplicon sequencing (iTag) and analysis. Compared to the control (no protozoa), two ciliates followed patterns of keystone predation by increasing microbial evenness. In pairwise competition treatments with a generalist flagellate, prey communities resembled the microbial communities of the respective keystone predator in monoculture. The relative abundance of the most common bacterial Operational Taxonomic Unit (OTU) in our system decreased compared to the control in the presence of these ciliates. This OTU was 98% similar to a known chitin degrader and nitrate reducer, important functions for the microbial community and the plant host. Collectively, the data demonstrated that predator identity had a greater effect on prey diversity and composition than overall predator diversity.
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Sarraceniaceae , Animais , Ecologia , Cadeia Alimentar , Folhas de Planta/microbiologia , Comportamento Predatório , RNA Ribossômico 16S/genéticaRESUMO
Carnivorous pitcher plants Sarracenia purpurea host diverse eukaryotic and bacterial communities which aid in insect prey digestion, but little is known about the functional processes mediated by the microbial communities. This study aimed to connect pitcher community diversity with functional nutrient transformation processes, identifying bacterial taxa, and measuring regulation of hydrolytic enzyme activity in response to prey and alternative nutrient sources. Genetic analysis identified diverse bacterial taxa known to produce hydrolytic enzyme activities. Chitinase, protease, and phosphatase activities were measured using fluorometric assays. Enzyme activity in field pitchers was positively correlated with bacterial abundance, and activity was suppressed by antibiotics suggesting predominantly bacterial sources of chitinase and protease activity. Fungi, algae, and rotifers observed could also contribute enzyme activity, but fresh insect prey released minimal chitinase activity. Activity of chitinase and proteases was upregulated in response to insect additions, and phosphatase activity was suppressed by phosphate additions. Particulate organic P in prey was broken down, appearing as increasing dissolved organic and inorganic P pools within 14 days. Chitinase and protease were not significantly suppressed by availability of dissolved organic substrates, though organic C and N stimulated bacterial growth, resulting in elevated enzyme activity. This comprehensive field and experimental study show that pitcher plant microbial communities dynamically regulate hydrolytic enzyme activity, to digest prey nutrients to simpler forms, mediating biogeochemical nutrient transformations and release of nutrients for microbial and host plant uptake.
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Bactérias/enzimologia , Proteínas de Bactérias/metabolismo , Cadeia Alimentar , Insetos/fisiologia , Sarraceniaceae/microbiologia , Animais , WisconsinRESUMO
Biogeographic barriers have long been implicated as drivers of biological diversification, but how these barriers influence co-occurring taxa can vary depending on factors intrinsic to the organism and in their relationships with other species. Due to the interdependence among taxa, ecological communities present a compelling opportunity to explore how interactions among species may lead to a shared response to historical events. Here we collect single nucleotide polymorphism data from five commensal arthropods associated with the Sarracenia alata carnivorous pitcher plant, and test for codiversification across the Mississippi River, a major biogeographic barrier in the southeastern United States. Population genetic structure in three of the ecologically dependent arthropods mirrors that of the host pitcher plant, with divergence time estimates suggesting two of the species (the pitcher plant moth Exyra semicrocea and a flesh fly Sarcophaga sarraceniae) dispersed synchronously across this barrier along with the pitcher plant. Patterns in population size and genetic diversity suggest the plant and ecologically dependent arthropods dispersed from east to west across the Mississippi River. In contrast, species less dependent on the plant ecologically show discordant phylogeographic patterns. This study demonstrates that ecological relationships may be an important predictor of codiversification, and supports recent suggestions that organismal trait data should be prominently featured in comparative phylogeographic investigations.
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Artrópodes/classificação , Biota , Sarraceniaceae , Distribuição Animal , Animais , Variação Genética , Filogenia , Filogeografia , Polimorfismo de Nucleotídeo Único , Densidade Demográfica , Rios , Sudeste dos Estados UnidosRESUMO
Climate change research has demonstrated that changing temperatures will have an effect on community-level dynamics by altering species survival rates, shifting species distributions, and ultimately, creating mismatches in community interactions. However, most of this work has focused on increasing temperature, and still little is known about how the variation in temperature extremes will affect community dynamics. We used the model aquatic community held within the leaves of the carnivorous plant, Sarracenia purpurea, to test how food web dynamics will be affected by high temperature variation. We tested the community response of the first (bacterial density), second (protist diversity and composition), and third trophic level (predator mortality), and measured community respiration. We collected early and late successional stage inquiline communities from S. purpurea from two North American and two European sites with similar average July temperature. We then created a common garden experiment in which replicates of these communities underwent either high or normal daily temperature variation, with the average temperature equal among treatments. We found an impact of temperature variation on the first two, but not on the third trophic level. For bacteria in the high-variation treatment, density experienced an initial boost in growth but then decreased quickly through time. For protists in the high-variation treatment, alpha-diversity decreased faster than in the normal-variation treatment, beta-diversity increased only in the European sites, and protist community composition tended to diverge more in the late successional stage. The mortality of the predatory mosquito larvae was unaffected by temperature variation. Community respiration was lower in the high-variation treatment, indicating a lower ecosystem functioning. Our results highlight clear impacts of temperature variation. A more mechanistic understanding of the effects that temperature, and especially temperature variation, will have on community dynamics is still greatly needed.
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Mudança Climática , Cadeia Alimentar , Animais , Ecossistema , Sarraceniaceae , TemperaturaRESUMO
Coniine, a polyketide-derived alkaloid, is poisonous to humans and animals. It is a nicotinic acetylcholine receptor antagonist, which leads to inhibition of the nervous system, eventually causing death by suffocation in mammals. Coniine's most famous victim is Socrates who was sentenced to death by poison chalice containing poison hemlock in 399 BC. In chemistry, coniine holds two historical records: It is the first alkaloid the chemical structure of which was established (in 1881), and that was chemically synthesized (in 1886). In plants, coniine and twelve closely related alkaloids are known from poison hemlock (Conium maculatum L.), and several Sarracenia and Aloe species. Recent work confirmed its biosynthetic polyketide origin. Biosynthesis commences by carbon backbone formation from butyryl-CoA and two malonyl-CoA building blocks catalyzed by polyketide synthase. A transamination reaction incorporates nitrogen from l-alanine and non-enzymatic cyclization leads to γ-coniceine, the first hemlock alkaloid in the pathway. Ultimately, reduction of γ-coniceine to coniine is facilitated by NADPH-dependent γ-coniceine reductase. Although coniine is notorious for its toxicity, there is no consensus on its ecological roles, especially in the carnivorous pitcher plants where it occurs. Lately there has been renewed interest in coniine's medical uses particularly for pain relief without an addictive side effect.
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Alcaloides/química , Alcaloides/toxicidade , Piperidinas/química , Piperidinas/toxicidade , Alcaloides/metabolismo , Alcaloides/farmacocinética , Alcaloides/farmacologia , Animais , Vias Biossintéticas , Humanos , Piperidinas/metabolismo , Piperidinas/farmacocinética , Plantas/química , Plantas/metabolismo , Relação Estrutura-AtividadeRESUMO
Sarracenia purpurea is a carnivorous plant historically used to treat smallpox infections. Our previous data found S. purpurea had broad spectrum antiviral activity in vitro. S. purpurea is one of several hundred identified carnivorous species of plants. Carnivorous plants have evolved through convergent evolution in at least ten independent events, usually in response to harsh environments where nutrition from prey is required for growth. These prey are known vectors of plant viruses that might introduce novel biotic stressors and defense pathways in carnivorous plants. This study evaluated the antiviral activity of several non-carnivorous and carnivorous plants from four evolutionarily distinct clades. Results demonstrated that carnivorous plants have evolved antiviral activity, a trait that is not present in related species of non-carnivorous plants. The antiviral trait may be due to the plant-prey relationship with insect vectors and an evolutionary need for carnivorous plants to have more robust antiviral defense systems.
Assuntos
Sarraceniaceae , Sarraceniaceae/virologia , Planta Carnívora/virologia , Planta Carnívora/fisiologia , Vírus de Plantas/fisiologia , Antivirais/farmacologia , AnimaisRESUMO
PREMISE OF THE STUDY: The role of hybridization in plant evolution remains a source of intense debate. Potential consequences range from genetic dead-ends to species fusion or hybrid speciation. While much has been learned from model systems such as Populus, Iris, and Helianthus, many questions remain. Consisting of 11 species that are all capable of hybridizing, Sarracenia presents an excellent system in which to study hybridization. ⢠METHODS: Using microsatellites, we examined a single field site consisting of three species: S. leucophylla, S. alata, and S. rubra subsp. wherryi. We determined the level of genetic admixture and compared it with allopatric sites of the same taxa. ⢠KEY RESULTS: In contrast to the well-defined clusters formed when we examined the allopatric sites, the sympatric field site exhibited a wide range of admixture. Additionally, when the relative genetic makeup of "pure" species at the site was compared with the makeup of hybrids, we found that Sarracenia alata contributed disproportionately to the hybrid genomes. ⢠CONCLUSIONS: Our study provides further evidence that hybridization is contributing to interspecific gene flow in the genus and that all species do not contribute equally to hybridization. Implications for conservation are discussed.
Assuntos
Fluxo Gênico , Hibridização Genética , Sarraceniaceae/genética , Alelos , Genética Populacional , Genótipo , Especificidade da EspécieRESUMO
PREMISE OF THE STUDY: Narrow-ranging, rare species often exhibit levels of genetic diversity lower than more common or widespread congeners. These taxa are at increased risk of extinction due to threats associated with natural as well as anthropogenic events. We assessed genetic variation in three federally endangered Sarracenia species. We discuss maintenance of genetic diversity and evolutionary implications of rarity. ⢠METHODS: We analyzed three noncoding chloroplast regions and nine microsatellite loci in populations spanning the geographic ranges of S. oreophila, S. alabamensis, and S. jonesii. The same microsatellite loci were used to examine a single field site of three more widespread species (S. alata, S. leucophylla, and S. rubra subsp. wherryi). ⢠KEY RESULTS: All three endangered species have experienced reductions in population size and numbers. All show considerably less variation than more widespread members of the genus. Sarracenia alabamensis maintains the greatest microsatellite variation but has the fewest remaining populations and may be under the greatest threat. More widespread S. oreophila maintains surprising chloroplast diversity, yet exhibits little microsatellite diversity. Sarracenia jonesii lacks chloroplast diversity, yet maintains greater microsatellite diversity than S. oreophila. ⢠CONCLUSIONS: The three endangered species differ in levels and structure of diversity, yet not in predictable ways, emphasizing that unique demographic and ecological histories, rather than current distribution and population size, best explain present patterns of genetic variation. Maintenance of remaining genetic variation is important, but preventing further habitat loss and degradation is critical.
Assuntos
Espécies em Perigo de Extinção , Variação Genética , Sarraceniaceae/genética , Alabama , DNA de Cloroplastos/genética , DNA Intergênico/genética , Loci Gênicos/genética , Haplótipos/genética , Repetições de Microssatélites/genética , Filogenia , Especificidade da EspécieRESUMO
Introgression can produce novel genetic variation in organisms that hybridize. Sympatric species pairs in the carnivorous plant genus Sarracenia L. frequently hybridize, and all known hybrids are fertile. Despite being a desirable system for studying the evolutionary consequences of hybridization, the extent to which introgression occurs in the genus is limited to a few species in only two field sites. Previous phylogenomic analysis of Sarracenia estimated a highly resolved species tree from 199 nuclear genes, but revealed a plastid genome that is highly discordant with the species tree. Such cytonuclear discordance could be caused by chloroplast introgression (i.e. chloroplast capture) or incomplete lineage sorting (ILS). To better understand the extent to which introgression is occurring in Sarracenia, the chloroplast capture and ILS hypotheses were formally evaluated. Plastomes were assembled de-novo from sequencing reads generated from 17 individuals in addition to reads obtained from the previous study. Assemblies of 14 whole plastomes were generated and annotated, and the remaining fragmented assemblies were scaffolded to these whole-plastome assemblies. Coding sequence from 79 homologous genes were aligned and concatenated for maximum-likelihood phylogeny estimation. The plastome tree is extremely discordant with the published species tree. Plastome trees were simulated under the coalescent and tree distance from the species tree was calculated to generate a null distribution of discordance that is expected under ILS alone. A t-test rejected the null hypothesis that ILS could cause the level of discordance seen in the plastome tree, suggesting that chloroplast capture must be invoked to explain the discordance. Due to the extreme level of discordance in the plastome tree, it is likely that chloroplast capture has been common in the evolutionary history of Sarracenia.
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The use of ever-advancing sequencing technologies has revealed incredible biodiversity at the microbial scale, and yet we know little about the ecological interactions in these communities. For example, in the phytotelmic community found in the purple pitcher plant, Sarracenia purpurea, ecologists typically consider the bacteria as a functionally homogenous group. In this food web, bacteria decompose detritus and are consumed by protozoa that are considered generalist consumers. Here, we tested whether a generalist consumer benefits from all bacteria equally. We isolated and identified 22 strains of bacteria, belonging to six genera, from S. purpurea plants. We grew the protozoa, Tetrahymena sp. with single isolates and strain mixtures of bacteria and measured Tetrahymena fitness. We found that different bacterial strains had different effects on protozoan fitness, both in isolation and in mixture. Our results demonstrate that not accounting for the composition of prey communities may affect the predicted outcome of predator-prey interactions.
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Processes influencing recruitment of diverse bacteria to plant microbiomes remain poorly understood. In the carnivorous pitcher plant Sarracenia purpurea model system, individual pitchers open to collect rainwater, invertebrates and a diverse microbial community, and this detrital food web is sustained by captured insect prey. This study examined how potential sources of bacteria affect the development of the bacterial community within pitchers, how the host plant tissue affects community development and how established vs. assembling communities differ. In a controlled greenhouse experiment, seven replicate pitchers were allocated to five treatments to exclude specific bacterial sources or host tissue: milliQ water only, milliQ + insect prey, rainwater + prey, established communities + prey, artificial pitchers with milliQ + prey. Community composition and functions were examined over 8-40 weeks using bacterial gene sequencing and functional predictions, measurements of cell abundance, hydrolytic enzyme activity and nutrient transformations. Distinct community composition and functional differences between artificial and real pitchers confirm an important influence of host plant tissue on community development, but also suggest this could be partially related to host nutrient uptake. Significant recruitment of bacteria to pitchers from air was evident from many taxa common to all treatments, overlap in composition between milliQ, milliQ + prey, and rainwater + prey treatments, and few taxa unique to milliQ only pitchers. Community functions measured as hydrolytic enzyme (chitinase, protease) activity suggested a strong influence of insect prey additions and were linked to rapid transformation of insect nutrients into dissolved and inorganic sources. Bacterial taxa found in 6 of 7 replicate pitchers within treatments, the "core microbiome" showed tighter successional trajectories over 8 weeks than all taxa. Established pitcher community composition was more stable over 8 weeks, suggesting a diversity-stability relationship and effect of microinvertebrates on bacteria. This study broadly demonstrates that bacterial composition in host pitcher plants is related to both stochastic and specific bacterial recruitment and host plants influence microbial selection and support microbiomes through capture of insect prey.
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The Staphylococcus aureus SsbA protein (SaSsbA) is a single-stranded DNA-binding protein (SSB) that is categorically required for DNA replication and cell survival, and it is thus an attractive target for potential antipathogen chemotherapy. In this study, we prepared the stem extract of Sarracenia purpurea obtained from 100% acetone to investigate its inhibitory effect against SaSsbA. In addition, the cytotoxic effects of this extract on the survival, apoptosis, proliferation, and migration of B16F10 melanoma cells were also examined. Initially, myricetin, quercetin, kaempferol, dihydroquercetin, dihydrokaempferol, rutin, catechin, ß-amyrin, oridonin, thioflavin T, primuline, and thioflavin S were used as possible inhibitors against SaSsbA. Of these compounds, dihydrokaempferol and oridonin were capable of inhibiting the ssDNA-binding activity of SaSsbA with respective IC50 values of 750 ± 62 and 2607 ± 242 µM. Given the poor inhibition abilities of dihydrokaempferol and oridonin, we screened the extracts of S. purpurea, Nepenthes miranda, and Plinia cauliflora for SaSsbA inhibitors. The stem extract of S. purpurea exhibited high anti-SaSsbA activity, with an IC50 value of 4.0 ± 0.3 µg/mL. The most abundant compounds in the stem extract of S. purpurea were identified using gas chromatography−mass spectrometry. The top five most abundant contents in this extract were driman-8,11-diol, deoxysericealactone, stigmast-5-en-3-ol, apocynin, and α-amyrin. Using the MOE-Dock tool, the binding modes of these compounds, as well as dihydrokaempferol and oridonin, to SaSsbA were elucidated, and their binding energies were also calculated. Based on the S scores, the binding capacity of these compounds was in the following order: deoxysericealactone > dihydrokaempferol > apocynin > driman-8,11-diol > stigmast-5-en-3-ol > oridonin > α-amyrin. Incubation of B16F10 cells with the stem extract of S. purpurea at a concentration of 100 µg/mL caused deaths at the rate of 76%, reduced migration by 95%, suppressed proliferation and colony formation by 99%, and induced apoptosis, which was observed in 96% of the B16F10 cells. Overall, the collective data in this study indicate the pharmacological potential of the stem extract of S. purpurea for further medical applications.
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The carnivorous pitcher plant Sarracenia purpurea is native to North America, but has been introduced into Europe, where it is now widespread. Understanding of how this species functions in its non-native range is limited. We measured pitcher morphology and prey capture by S. purpurea in its non-native range in Britain and Ireland. Pitchers were removed from different plants at each of six bogs covering the species range in Britain and Ireland (n = 10 pitchers per site). For each pitcher we counted and identified every prey item and took measurements of morphology. We also compiled prey capture data for existing studies in Europe and North America. Prey capture characteristics varied between sites in Britain and Ireland. The amount of prey captured varied 20-fold between sites and was partially explained by differences in pitcher size; larger pitchers caught more prey. The primary prey was Formicidae, Diptera and Coleoptera. At the rank of order, prey composition varied between bogs, some contained mainly Formicidae, some mainly Diptera and some a mix. Prey capture was less evenly distributed at some bogs compared to others, suggesting more specialization. There was no overall difference in prey capture (composition or evenness) at the rank of order between plants in Europe compared to those in North America. At the rank of species, prey capture varied between populations even within the same order. This study demonstrates a large amount of variability between sites in prey capture characteristics. This may reflect different site characteristics and/or plant strategies, which will likely impact plant function, and may impact the inquiline community. In terms of prey capture at the rank of order, S. purpurea functions identically in its non-native range. This supports its use as a model system in a natural experiment for understanding food webs.
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Previous meta-analyses suggested that carnivorous plants-despite access to N, P, and K from prey-have significantly lower leaf concentrations of these nutrients than noncarnivores. Those studies, however, largely compared carnivores in nutrient-poor habitats with noncarnivores in more nutrient-rich sites, so that the differences reported might reflect habitat differences as much as differences in nutrient-capture strategy. Here we examine three carnivorous and 12 noncarnivorous plants in the same nutrient-poor bog to compare their foliar nutrient concentrations, assess their patterns of nutrient limitation using leaf NPK stoichiometry, and estimate percentage N derived from prey by carnivores using a mixing model for stable N isotopes. We hypothesized that (1) carnivore leaf nutrient concentrations approach or exceed those of noncarnivores in the same nutrient-poor habitat; (2) species in different functional groups show different patterns of stoichiometry and apparent nutrient limitation; and (3) noncarnivores might show evidence of using other means of nutrient acquisition or conservation to reduce nutrient limitation. At Fallison Bog in northern Wisconsin, carnivorous plants (Drosera rotundifolia, Sarracenia purpurea, Utricularia macrorhiza) showed significantly lower leaf percentage C and N:P ratio, higher δ15 N, and no difference from noncarnivores in leaf N, P, K, and δ13 C. Sedges had significantly lower leaf percentage P, percentage C, and N:K ratio, and higher K:P ratio than nonsedges restricted to the Sphagnum mat, and may tap peat N via aerenchyma-facilitated peat oxidation (oxipeditrophy). Evergreen ericaceous shrubs exhibited significantly higher levels of percentage C and lower values of δ15 N than mat nonericads. Calla palustris-growing in the nutrient-rich moat at the bog's upland edge-had very high values of leaf N, K, δ15 N, and N:P ratio, suggesting that it may obtain nutrients from minerotrophic flows from the adjacent uplands and/or rapidly decaying peat. Stoichiometric analyses indicated that most species are N limited. A mixing model applied to δ15 N values for carnivores, noncarnivores, and insects produced an estimate of 50% of leaf N derived from prey for Utricularia, 42% for Sarracenia, and 41% for Drosera.
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Carnivoridade , Drosera , Folhas de Planta , Plantas , Solo , NutrientesRESUMO
The carnivorous pitcher plant Sarracenia purpurea exhibits many ethnobotanical uses, including the treatments of type 2 diabetes and tuberculosis-like symptoms. In this study, we prepared different extracts from the leaves (pitchers), stems, and roots of S. purpurea and investigated their antioxidant and anticancer properties. To evaluate the extraction efficiency, we individually used different solvents, namely methanol, ethanol, acetone, and distilled water, for S. purpurea extract preparations. The root extract of S. purpurea, obtained by 100% acetone (S. purpurea-root-acetone), had the highest anticancer activities, antioxidation capacity (the DPPH activity with IC50 of 89.3 ± 2.2 µg/mL), antibacterial activities, total phenolic content (33.4 ± 0.7 mg GAE/g), and total flavonoid content (107.9 ± 2.2 mg QUE/g). The most abundant compounds in S. purpurea-root-acetone were identified using gas chromatography-mass spectrometry; 7,8-Dihydro-α-ionone was the major compound present in S. purpurea-root-acetone. In addition, the co-cytotoxicity of S. purpurea-root-acetone (combined with the clinical anticancer drug 5-fluorouracil (5-FU) on the survival, apoptosis, proliferation, and migration of the 4T1 mammary carcinoma) was examined. The combination of 5-FU with S. purpurea-root-acetone could be highly efficient for anti-4T1 cells. We also found that S. purpurea-root-acetone could inhibit the enzymatic activity of human dihydroorotase (huDHOase), an attractive target for potential anticancer chemotherapy. The sic most abundant compounds in S. purpurea-root-acetone were tested using an in silico analysis via MOE-Dock software for their binding affinities. The top-ranked docking conformations were observed for 7,8-dihydro-α-ionone and stigmast-5-en-3-ol, suggesting the inhibition potential against huDHOase. Overall, the collective data in this study may indicate the pharmacological potentials of S. purpurea-root-acetone for possible medical applications.
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Plant carnivory is often manifested as dramatic changes in the structure and morphology of the leaf. These changes appear to begin early in leaf development. For example, the development of the Sarracenia purpurea leaf primordium is associated with the formation of an adaxial ridge, whose growth along with that of the leaf margin resulted in a hollow structure that later developed into a pitcher. In Nepenthes khasiana, pitcher formation occurs during the initial stages of leaf development, although this has not been shown at the primordial stage. The formation of the Utricularia gibba trap resulted from the growth of the dome-shaped primordium in both the longitudinal and transverse directions. Recent research has begun to unfold the genetic basis of the development of the carnivorous leaf. We review these findings and discuss them in relation to the flat-shaped leaves of the model plant Arabidopsis.