Most cited article - PubMed ID 24817095
Dinitrogen fixation associated with shoots of aquatic carnivorous plants: is it ecologically important?
Changes in organic matter accumulation in wetlands are critical for climate dynamics. Different nitrogen (N) inputs in Sphagnum-dominated peat bogs can lead to varying rates of carbon (C) and N accumulation, influencing greenhouse gas emissions. We investigated how contrasting N deposition shapes microbial communities in two Czech peat bogs, focusing on biological N2 fixation (BNF) as a key N input in pristine wetlands. Higher N deposition resulted in a more active microbial community with increased enzyme activity and C acquisition, potentially accelerating decomposition and reducing C storage. Enhanced denitrification, indicated by active nosZ Clade I genes, suggests that higher N inputs may increase N losses through denitrification. In contrast, the lower N site showed a less active microbial community with slower decomposition, beneficial for C sequestration, though potentially less adaptable to future N increases. Experimental BNF rates were 70 times higher at the high N site, consistent with elevated diazotroph activity indicated by active nifH gene. Phosphorus (P) availability and NH4+/NO3- ratios appeared to drive BNF differences, emphasizing the need for managed N inputs to maintain peatland ecological functions.
- Keywords
- Sphagnum, biological nitrogen fixation, denitrification, microbiome, nitrogen deposition, peat bog,
- MeSH
- Bacteria * genetics metabolism classification MeSH
- Denitrification MeSH
- Nitrogen * metabolism analysis MeSH
- Nitrogen Fixation MeSH
- Phosphorus metabolism MeSH
- Microbiota * MeSH
- Wetlands * MeSH
- Soil chemistry MeSH
- Soil Microbiology * MeSH
- Sphagnopsida microbiology MeSH
- Carbon metabolism MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Czech Republic MeSH
- Names of Substances
- Nitrogen * MeSH
- Phosphorus MeSH
- Soil MeSH
- Carbon MeSH
BACKGROUND: Carnivorous plants are an ecological group of approx. 810 vascular species which capture and digest animal prey, absorb prey-derived nutrients and utilize them to enhance their growth and development. Extant carnivorous plants have evolved in at least ten independent lineages, and their adaptive traits represent an example of structural and functional convergence. Plant carnivory is a result of complex adaptations to mostly nutrient-poor, wet and sunny habitats when the benefits of carnivory exceed the costs. With a boost in interest and extensive research in recent years, many aspects of these adaptations have been clarified (at least partly), but many remain unknown. SCOPE: We provide some of the most recent insights into substantial ecophysiological, biochemical and evolutional particulars of plant carnivory from the functional viewpoint. We focus on those processes and traits in carnivorous plants associated with their ecological characterization, mineral nutrition, cost-benefit relationships, functioning of digestive enzymes and regulation of the hunting cycle in traps. We elucidate mechanisms by which uptake of prey-derived nutrients leads to stimulation of photosynthesis and root nutrient uptake. CONCLUSIONS: Utilization of prey-derived mineral (mainly N and P) and organic nutrients is highly beneficial for plants and increases the photosynthetic rate in leaves as a prerequisite for faster plant growth. Whole-genome and tandem gene duplications brought gene material for diversification into carnivorous functions and enabled recruitment of defence-related genes. Possible mechanisms for the evolution of digestive enzymes are summarized, and a comprehensive picture on the biochemistry and regulation of prey decomposition and prey-derived nutrient uptake is provided.
- Keywords
- Dionaea, Drosera, Nepenthes, Carnivorous plant, co-option, cost–benefit relationships, digestive enzymes, evolution of carnivory, hunting cycle, mineral nutrient economy, regulation of enzyme secretion, terrestrial and aquatic species,
- MeSH
- Photosynthesis MeSH
- Plant Leaves MeSH
- Carnivory * MeSH
- Plants * genetics MeSH
- Nutrients MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: Utricularia are rootless aquatic carnivorous plants which have recently attracted the attention of researchers due to the peculiarities of their miniaturized genomes. Here, we focus on a novel aspect of Utricularia ecophysiology-the interactions with and within the complex communities of microorganisms colonizing their traps and external surfaces. RESULTS: Bacteria, fungi, algae, and protozoa inhabit the miniature ecosystem of the Utricularia trap lumen and are involved in the regeneration of nutrients from complex organic matter. By combining molecular methods, microscopy, and other approaches to assess the trap-associated microbial community structure, diversity, function, as well as the nutrient turn-over potential of bacterivory, we gained insight into the nutrient acquisition strategies of the Utricularia hosts. CONCLUSIONS: We conclude that Utricularia traps can, in terms of their ecophysiological function, be compared to microbial cultivators or farms, which center around complex microbial consortia acting synergistically to convert complex organic matter, often of algal origin, into a source of utilizable nutrients for the plants.
- Keywords
- Algae, Bacteria, Ciliate bacterivory, Digestive mutualism, Fungi, Herbivory, Nutrient turnover, Plant–microbe interactions, Protists, Utricularia traps,
- MeSH
- Bacteria classification genetics isolation & purification MeSH
- DNA, Bacterial genetics MeSH
- DNA, Fungal genetics MeSH
- DNA, Algal genetics MeSH
- Phylogeny MeSH
- Lamiales microbiology physiology MeSH
- Fungi classification genetics isolation & purification MeSH
- Metagenomics methods MeSH
- Microbial Consortia MeSH
- Gene Expression Profiling methods MeSH
- Aquatic Organisms microbiology physiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA, Bacterial MeSH
- DNA, Fungal MeSH
- DNA, Algal MeSH
In the carnivorous plant genus Genlisea a unique lobster pot trapping mechanism supplements nutrition in nutrient-poor habitats. A wide spectrum of microbes frequently occurs in Genlisea's leaf-derived traps without clear relevance for Genlisea carnivory. We sequenced the metatranscriptomes of subterrestrial traps vs. the aerial chlorophyll-containing leaves of G. nigrocaulis and of G. hispidula. Ribosomal RNA assignment revealed soil-borne microbial diversity in Genlisea traps, with 92 genera of 19 phyla present in more than one sample. Microbes from 16 of these phyla including proteobacteria, green algae, amoebozoa, fungi, ciliates and metazoans, contributed additionally short-lived mRNA to the metatranscriptome. Furthermore, transcripts of 438 members of hydrolases (e.g., proteases, phosphatases, lipases), mainly resembling those of metazoans, ciliates and green algae, were found. Compared to aerial leaves, Genlisea traps displayed a transcriptional up-regulation of endogenous NADH oxidases generating reactive oxygen species as well as of acid phosphatases for prey digestion. A leaf-vs.-trap transcriptome comparison reflects that carnivory provides inorganic P- and different forms of N-compounds (ammonium, nitrate, amino acid, oligopeptides) and implies the need to protect trap cells against oxidative stress. The analysis elucidates a complex food web inside the Genlisea traps, and suggests ecological relationships between this plant genus and its entrapped microbiome.
