An official website of the United States government
Abstract Leaves of the carnivorous sundew plants (Droseraspp.) secrete mucilage that hosts microorganisms, but whether this microbiota contributes to prey digestion is unclear. We identified the acidophilic fungusAcrodontium crateriformeas the dominant species in the mucilage microbial communities, thriving in multiple sundew species across the global range. The fungus grows and sporulates on sundew glands as its preferred acidic environment, and its presence in traps increased the prey digestion process.A. crateriformehas a reduced genome similar to other symbiotic fungi. DuringA. crateriforme–Drosera spatulatacoexistence and digestion of prey insects, transcriptomes revealed significant gene co-option in both partners. Holobiont expression patterns during prey digestion further revealed synergistic effects in several gene families including fungal aspartic and sedolisin peptidases, facilitating prey digestion in leaves, as well as nutrient assimilation and jasmonate signalling pathway expression. This study establishes that botanical carnivory is defined by adaptations involving microbial partners and interspecies interactions.
more »
« less
Leaf NPK stoichiometry, δ15N , and apparent nutrient limitation of co‐occurring carnivorous and noncarnivorous plants
Abstract 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 δ15N, and no difference from noncarnivores in leaf N, P, K, and δ13C. Sedges had significantly lower leaf percentage P, percentage C, and N:K ratio, and higher K:P ratio than nonsedges restricted to theSphagnummat, 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 δ15N 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, δ15N, 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 δ15N values for carnivores, noncarnivores, and insects produced an estimate of 50% of leaf N derived from prey forUtricularia, 42% forSarracenia, and 41% forDrosera.
more »
« less
- Award ID(s):
- 1929296
- PAR ID:
- 10383282
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology
- Volume:
- 103
- Issue:
- 12
- ISSN:
- 0012-9658
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Carnivorous plants are a paradigm of convergent evolution, but their genomes reveal even deeper layers of complexity. Recent work uncovers widespread polyploidy, including the decaploid East Asian pitcher plant (Nepenthes gracilis) genome and hybrid origins for the tetraploid Venus flytrap (Dionaea muscipula) and queen (hexaploid) and Cape (dodecaploid) sundews (Drosera regia and D. capensis, respectively). The bladderwort (Utricularia gibba) experienced extreme genome compaction while retaining otherwise typical gene number, challenging assumptions about genome size. Molecular convergence is conspicuous, from digestive enzyme recruitment to repeated amino acid substitutions under functional constraints. Drosera species further illustrate how centromere type (monocentric versus holocentric) shapes genome architecture. These discoveries position carnivorous plants as models for studying the plasticity and adaptive landscapes of plant genomes, including tradeoffs between local and global gene duplication and intergenic DNA deletion.more » « less
-
Abstract Background and AimsFreshwater nitrogen inputs are increasing globally, altering the structure and function of wetland ecosystems adapted to low nutrient conditions. Carnivorous wetland plants of the genus Utricularia are hypothesized to reduce their reliance on carnivory and increase their assimilation of environmental nutrients when the supply of ambient nutrients increases. Despite success in using stable isotope approaches to quantify carnivory of terrestrial carnivorous plants, quantifying carnivory of aquatic Utricularia requires improvement. MethodsWe developed stable isotope mixing models to quantify aquatic plant carnivory and used these models to measure dietary changes of three Utricularia species, Utricularia australis, U. gibba and U. uliginosa, in 11 wetlands across a 794-km gradient in eastern Australia. Diet was assessed using multiple models that compared variations in the natural-abundance nitrogen isotope composition (δ15N) of Utricularia spp. with that of non-carnivorous plants, and environmental and carnivorous nitrogen sources. Key ResultsCarnivory supplied 40–100 % of plant nitrogen. The lowest carnivory rates coincided with the highest availability of ammonium and dissolved organic carbon. ConclusionsOur findings suggest that Utricularia populations may adapt to high nutrient environments by shifting away from energetically costly carnivory. This has implications for species conservation as anthropogenic impacts continue to affect global wetland ecosystems.more » « less
-
Glass, Jennifer B (Ed.)ABSTRACT 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. IMPORTANCEMicrobial 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.more » « less
-
Abstract Interactions between plants and soil microbes influence plant nutrient transformations, including nitrogen (N) fixation, nutrient mineralization, and resource exchanges through fungal networks. Physical disturbances to soils can disrupt soil microbes and associated processes that support plant and microbial productivity. In low resource drylands, biological soil crusts (“biocrusts”) occupy surface soils and house key autotrophic and diazotrophic bacteria, non‐vascular plants, or lichens. Interactions among biocrusts, plants, and fungal networks between them are hypothesized to drive carbon and nutrient dynamics; however, comparisons across ecosystems are needed to generalize how soil disturbances alter microbial communities and their contributions to N pools and transformations. To evaluate linkages among plants, fungi, and biocrusts, we disturbed all unvegetated surfaces with human foot trampling twice yearly from 2013–2019 in dry conditions in cyanobacteria‐dominated biocrusts in the Chihuahuan Desert grassland and shrubland ecosystems. After 5 years, disturbance decreased the abundances of cyanobacteria (especiallyMicrocoleus steenstrupiiclade) and N‐fixers (Scytonemasp., andSchizothrixsp.) by >77% and chlorophyllaby up to 55% but, conversely, increased soil fungal abundance by 50% compared with controls. Responses of root‐associated fungi differed between the two dominant plant species and ecosystem types, with a maximum of 80% more aseptate hyphae in disturbed than in control plots. Although disturbance did not affect15N tracer transfer from biocrusts to the dominant grass,Bouteloua eriopoda, disturbance increased available soil N by 65% in the shrubland, and decreased leaf N ofB. eriopodaby up to 16%, suggesting that, although rapid N transfer during peak production was not affected by disturbance, over the long‐term plant nutrient content was disrupted. Altogether, the shrubland may be more resilient to detrimental changes due to disturbance than grassland, and these results demonstrated that disturbances to soil microbial communities have the potential to cause substantial changes in N pools by reducing and reordering biocrust taxa.more » « less
