Most cited article - PubMed ID 19755570
Utricularia carnivory revisited: plants supply photosynthetic carbon to traps
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
BACKGROUND: The cost-benefit model for the evolution of botanical carnivory provides a conceptual framework for interpreting a wide range of comparative and experimental studies on carnivorous plants. This model assumes that the modified leaves called traps represent a significant cost for the plant, and this cost is outweighed by the benefits from increased nutrient uptake from prey, in terms of enhancing the rate of photosynthesis per unit leaf mass or area (AN) in the microsites inhabited by carnivorous plants. SCOPE: This review summarizes results from the classical interpretation of the cost-benefit model for evolution of botanical carnivory and highlights the costs and benefits of active trapping mechanisms, including water pumping, electrical signalling and accumulation of jasmonates. Novel alternative sequestration strategies (utilization of leaf litter and faeces) in carnivorous plants are also discussed in the context of the cost-benefit model. CONCLUSIONS: Traps of carnivorous plants have lower AN than leaves, and the leaves have higher AN after feeding. Prey digestion, water pumping and electrical signalling represent a significant carbon cost (as an increased rate of respiration, RD) for carnivorous plants. On the other hand, jasmonate accumulation during the digestive period and reprogramming of gene expression from growth and photosynthesis to prey digestion optimizes enzyme production in comparison with constitutive secretion. This inducibility may have evolved as a cost-saving strategy beneficial for carnivorous plants. The similarities between plant defence mechanisms and botanical carnivory are highlighted.
- Keywords
- Action potential, Dionaea, Drosera, Nepenthes, Venus flytrap, botanical carnivory, carnivorous plant, cost–benefit, electrical signalling, jasmonates,
- MeSH
- Biological Evolution * MeSH
- Models, Biological * MeSH
- Droseraceae physiology MeSH
- Plant Physiological Phenomena * MeSH
- Signal Transduction MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
BACKGROUND AND AIMS: Rootless carnivorous plants of the genus Utricularia are important components of many standing waters worldwide, as well as suitable model organisms for studying plant-microbe interactions. In this study, an investigation was made of the importance of microbial dinitrogen (N2) fixation in the N acquisition of four aquatic Utricularia species and another aquatic carnivorous plant, Aldrovanda vesiculosa. METHODS: 16S rRNA amplicon sequencing was used to assess the presence of micro-organisms with known ability to fix N2. Next-generation sequencing provided information on the expression of N2 fixation-associated genes. N2 fixation rates were measured following (15)N2-labelling and were used to calculate the plant assimilation rate of microbially fixed N2. KEY RESULTS: Utricularia traps were confirmed as primary sites of N2 fixation, with up to 16 % of the plant-associated microbial community consisting of bacteria capable of fixing N2. Of these, rhizobia were the most abundant group. Nitrogen fixation rates increased with increasing shoot age, but never exceeded 1·3 μmol N g(-1) d. mass d(-1). Plant assimilation rates of fixed N2 were detectable and significant, but this fraction formed less than 1 % of daily plant N gain. Although trap fluid provides conditions favourable for microbial N2 fixation, levels of nif gene transcription comprised <0·01 % of the total prokaryotic transcripts. CONCLUSIONS: It is hypothesized that the reason for limited N2 fixation in aquatic Utricularia, despite the large potential capacity, is the high concentration of NH4-N (2·0-4·3 mg L(-1)) in the trap fluid. Resulting from fast turnover of organic detritus, it probably inhibits N2 fixation in most of the microorganisms present. Nitrogen fixation is not expected to contribute significantly to N nutrition of aquatic carnivorous plants under their typical growth conditions; however, on an annual basis the plant-microbe system can supply nitrogen in the order of hundreds of mg m(-2) into the nutrient-limited littoral zone, where it may thus represent an important N source.
- Keywords
- 15N2 labelling, Aldrovanda vesiculosa, N nutrition, U. australis, U. intermedia, U. reflexa, Utricularia vulgaris, aquatic carnivorous plants, daily nitrogen gain, nitrogen fixation, periphyton, traps,
- MeSH
- Ammonium Compounds analysis MeSH
- Bacteria genetics isolation & purification metabolism MeSH
- RNA, Bacterial chemistry genetics MeSH
- Droseraceae metabolism microbiology MeSH
- Nitrogen metabolism MeSH
- Ecology MeSH
- Ecosystem MeSH
- Nitrogen Fixation * MeSH
- Nitrogen Isotopes MeSH
- Magnoliopsida metabolism microbiology MeSH
- Molecular Sequence Data MeSH
- RNA, Ribosomal, 16S chemistry genetics MeSH
- Base Sequence MeSH
- Sequence Analysis, RNA MeSH
- Water metabolism MeSH
- Plant Shoots metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Comparative Study MeSH
- Names of Substances
- Ammonium Compounds MeSH
- RNA, Bacterial MeSH
- Nitrogen MeSH
- Nitrogen Isotopes MeSH
- RNA, Ribosomal, 16S MeSH
- Water MeSH
Aquatic Utricularia species usually grow in standing, nutrient-poor humic waters. They take up all necessary nutrients either directly from the water by rootless shoots or from animal prey by traps. The traps are hollow bladders, 1-6 mm long with elastic walls and have a mobile trap door. The inner part of the trap is densely lined with quadrifid and bifid glands and these are involved in the secretion of digestive enzymes, resorption of nutrients and pumping out the water. The traps capture small aquatic animals but they also host a community of microorganisms considered as commensals. How do these perfect traps function, kill and digest their prey? How do they provide ATP energy for their demanding physiological functions? What are the nature of the interactions between the traps and the mutualistic microorganisms living inside as commensals? In this mini review, all of these questions are considered from an ecophysiologist's point of view, based on the most recent literature data and unpublished results. A new concept on the role of the commensal community for the plants is presented.
- MeSH
- Ecosystem * MeSH
- Oxygen metabolism MeSH
- Magnoliopsida enzymology physiology MeSH
- Food Chain MeSH
- Water physiology MeSH
- Aquatic Organisms physiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- Oxygen MeSH
- Water MeSH