Ecological implications of organic carbon dynamics in the traps of aquatic carnivorous Utricularia plants
Dagmara Sirová A B E , Jakub Borovec A B , Tomáš Picek A , Lubomír Adamec C , Linda Nedbalová C D and Jaroslav Vrba A B
+ Author Affiliations
- Author Affiliations
A Faculty of Science, University of South Bohemia, Department of Ecosystem Biology, Branišovská 31, CZ–37005 České Budějovice, Czech Republic.
B Institute of Hydrobiology, Biology Centre AS CR, Na Sádkách 7, CZ–37005 České Budějovice, Czech Republic.
C Institute of Botany AS CR, Dukelská 135, CZ–37982 Třeboň, Czech Republic.
D Faculty of Science, Charles University, Viničná 7, CZ–12844 Praha, Czech Republic.
E Corresponding author. Email: dagmara_sirova@hotmail.com
Functional Plant Biology 38(7) 583-593 https://doi.org/10.1071/FP11023
Submitted: 22 January 2011 Accepted: 23 May 2011 Published: 12 July 2011
Abstract
Rootless aquatic carnivorous Utricularia exude up to 25% of their photosynthates into the trap lumen, which also harbours a complex microbial community thought to play a role in enhancing Utricularia nutrient acquisition. We investigated the composition of organic carbon in the trap fluid, its availability for microbial uptake, the influence of plant nutrient status and trap age on its biodegradability, and the composition of prokaryotic assemblages within the traps of three aquatic Utricularia species. Using ion chromatography and basal respiration rate measurements we confirmed that up to 30% of total dissolved organic carbon in Utricularia trap fluid in oligotrophic conditions was easily biodegradable compounds commonly found in plant root exudates (mainly glucose, fructose and lactate). The proportion of these compounds and their microbial utilisation decreased with increasing mineral nutrient supply and trap age. Fluorescence in situ hybridisation analyses showed that microbial trap assemblages are dominated by alpha and beta Proteobacteria, and that the assemblage composition is affected by changes in the ambient mineral nutrient supply. We suggest that organic carbon dynamics within the traps, involving both the plant and associated microbial assemblages, underlies the acquisition of key nutrients by Utricularia and may help explain the evolutionary success of the genus.
Aditional keywords: amino acids, biodegradability, exudate composition, nutrient availability, organic acids, plant–microbe interactions, sugars.
References
Adamec L (1997) Photosynthetic characteristics of the aquatic carnivorous plant Aldrovanda vesiculosa. Aquatic Botany 59, 297–306.| Photosynthetic characteristics of the aquatic carnivorous plant Aldrovanda vesiculosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhsFCgsQ%3D%3D&md5=6ed25cadaf33cddbb1f54e79d716cb28CAS |
Adamec L (2007) Oxygen concentrations inside the traps of the carnivorous plants Utricularia and Genlisea (Lentibulariaceae). Annals of Botany 100, 849–856.
| Oxygen concentrations inside the traps of the carnivorous plants Utricularia and Genlisea (Lentibulariaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlyhs7jF&md5=77704fbc5dd7347eecc8dea879534685CAS | 17720681PubMed |
Adamec L (2008a) The influence of prey capture on photosynthetic rate in two aquatic carnivorous plant species. Aquatic Botany 89, 66–70.
| The influence of prey capture on photosynthetic rate in two aquatic carnivorous plant species.Crossref | GoogleScholarGoogle Scholar |
Adamec L (2008b) Mineral nutrient relations in the aquatic carnivorous plant Utricularia australis and its investment in carnivory. Fundamental and Applied Limnology 171, 175–183.
| Mineral nutrient relations in the aquatic carnivorous plant Utricularia australis and its investment in carnivory.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlCqtbg%3D&md5=1ec07ec006085f406036213652bd10bdCAS |
Adamec L (2010a) Field growth analysis of Utricularia stygia and U. intermedia – two aquatic carnivorous plants with dimorphic shoots. Phyton 49, 241–251.
Adamec L (2010b) Tissue mineral nutrient content in turions of aquatic plants: does it represent a storage function? Fundamental and Applied Limnology 176, 145–151.
| Tissue mineral nutrient content in turions of aquatic plants: does it represent a storage function?Crossref | GoogleScholarGoogle Scholar |
Adamec L, Kovářová M (2006) Field growth characteristics of two aquatic carnivorous plants, Aldrovanda vesiculosa and Utricularia australis. Folia Geobotanica 41, 395–406.
| Field growth characteristics of two aquatic carnivorous plants, Aldrovanda vesiculosa and Utricularia australis.Crossref | GoogleScholarGoogle Scholar |
Adamec L, Sirová D, Vrba J (2010) Contrasting growth effects of prey capture in two carnivorous plant species. Fundamental and Applied Limnology 176, 153–160.
| Contrasting growth effects of prey capture in two carnivorous plant species.Crossref | GoogleScholarGoogle Scholar |
Brimecombe MJ, De Leij F, Lynch JM (2007) Rhizodeposition and microbial populations. In ‘The rhizosphere – biochemistry and organic substances at the soil–plant interface’. (Eds R Pinton, Z Varanini, P Nannipieri) pp. 73–109. (CRC Press: Boca Raton, FL, USA)
Bruun T, Elberling B, Christensen BT (2010) Lability of soil organic carbon in tropical soils with different clay minerals. Soil Biology and Biochemistry 42, 888–895.
| Lability of soil organic carbon in tropical soils with different clay minerals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFCmu7g%3D&md5=94e1978d1597af99173b2aa07dbdb10aCAS |
Cadillo-Quiroz H, Yavitt JB, Zinder SH, Thies JE (2010) Diversity and community structure of Archaea inhabiting the rhizoplane of two contrasting plants from an acidic bog. Microbial Ecology 59, 757–767.
| Diversity and community structure of Archaea inhabiting the rhizoplane of two contrasting plants from an acidic bog.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntVCrsr0%3D&md5=632cf422eca4b760d682376feee243f8CAS | 20024684PubMed |
Caputo C, Barneix AJ (1997) Export of amino acids to the phloem in relation to N supply in wheat. Physiologia Plantarum 101, 853–860.
| Export of amino acids to the phloem in relation to N supply in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFOmtA%3D%3D&md5=9ca17f9266dabf0e693690eb6ca91b94CAS |
Chiang C, Knight SG (1960) Metabolism of D-Xylose by moulds. Nature 188, 79–81.
Cochran-Stafira DL, von Ende CN (1998) Integrating bacteria into food webs: studies with Sarracenia purpurea inquilines. Ecology 79, 880–898.
Dahija JS (1991) Xylitol production by Petromyces albertensis grown on medium containing D-xylose. Canadian Journal of Microbiology 37, 14–18.
Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Systematic and Applied Microbiology 22, 434–444.
Darwent MJ, Paterson E, McDonald AJS, Tomos AD (2003) Biosensor reporting of root exudation from Hordeum vulgare in relation to shoot nitrate concentration. Journal of Experimental Botany 54, 325–334.
| Biosensor reporting of root exudation from Hordeum vulgare in relation to shoot nitrate concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlOiu7g%3D&md5=5905b6a3f8050f03dcf2657d4b672383CAS | 12493860PubMed |
Darwin C (1875) ‘Insectivorous plants.’ (D Appleton & Company: New York)
Englund G, Harms S (2003) Effects of light and microcrustacean prey on growth and investment in carnivory in Utricularia vulgaris. Freshwater Biology 48, 786–794.
| Effects of light and microcrustacean prey on growth and investment in carnivory in Utricularia vulgaris.Crossref | GoogleScholarGoogle Scholar |
Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiology Reviews 33, 855–869.
| Environmental factors shaping the ecological niches of ammonia-oxidizing archaea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVWksbnE&md5=f2a1ef9ad0f83b2236770dfde6392e8eCAS | 19453522PubMed |
Fineran BA, Lee MSL (1980) Organization of mature external glands on the trap and other organs of the bladderwort Utricularia monanthos. Protoplasma 103, 17–34.
| Organization of mature external glands on the trap and other organs of the bladderwort Utricularia monanthos.Crossref | GoogleScholarGoogle Scholar |
Friday LE, Quarmby C (1994) Uptake and translocation of prey-derived 15N and 32P in Utricularia vulgaris L. New Phytologist 126, 273–281.
| Uptake and translocation of prey-derived 15N and 32P in Utricularia vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVyitr4%3D&md5=be5ee6286ede654a1c1e12df31211f4fCAS |
Harms S (1999) Prey selection in three species of the carnivorous aquatic plant Utricularia (bladderwort). Archiv für Hydrobiologie 146, 449–470.
Herfort L, Schouten S, Abbas B, Veldhuis MJW, Coolen MJL, Wuchter C, Boon JP, Herndl GJ, Damste JSS (2007) Variations in spatial and temporal distribution of Archaea in the North Sea in relation to environmental variables. FEMS Microbiology Ecology 62, 242–257.
| Variations in spatial and temporal distribution of Archaea in the North Sea in relation to environmental variables.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsValtr7P&md5=b98004360909d6dca359cb05438e1016CAS | 17991018PubMed |
Herrmann M, Saunders AM, Schramm A (2008) Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Applied and Environmental Microbiology 74, 3279–3283.
| Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVOku7c%3D&md5=16136943f94c95f8032b00f565023765CAS | 18344332PubMed |
Herrmann M, Saunders AM, Schramm A (2009) Effect of lake trophic status and rooted macrophytes on community on composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments. Applied and Environmental Microbiology 75, 3127–3136.
| Effect of lake trophic status and rooted macrophytes on community on composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsFWisLs%3D&md5=fcc8bb5abfb94b25466d5174451077a9CAS | 19304820PubMed |
Jezbera J, Horňák K, Šimek K (2006) Prey selectivity of bacterivorous protists in different size fractions of reservoir water amended with nutrients. Environmental Microbiology 8, 1330–1339.
| Prey selectivity of bacterivorous protists in different size fractions of reservoir water amended with nutrients.Crossref | GoogleScholarGoogle Scholar | 16872397PubMed |
Joergensen RG, Emmerling C (2006) Methods for evaluating human impact on soil microorganisms based on their activity, biomass, and diversity in agricultural soils. Journal of Plant Nutrition and Soil Science – Zeitschrift für Pflanzenernährung und Bodenkunde 169, 295–309.
Juniper BE, Robins RJ, Joel DM (1989) ‘The carnivorous plants.’ (Academic Press: London)
Kibriya S, Jones JI (2007) Nutrient availability and the carnivorous habit in Utricularia vulgaris. Freshwater Biology 52, 500–509.
| Nutrient availability and the carnivorous habit in Utricularia vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFSit7k%3D&md5=dcf070ef201456afae0178833df8be90CAS |
Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant–rhizosphere mutualisms. Annual Review of Ecology Evolution and Systematics 39, 215–236.
| Sanctions, cooperation, and the stability of plant–rhizosphere mutualisms.Crossref | GoogleScholarGoogle Scholar |
Kopáček J, Hejzlar J (1993) Semi-micro determination of total phosphorus in fresh waters with perchloric acid digestion. International Journal of Environmental Analytical Chemistry 53, 173–183.
| Semi-micro determination of total phosphorus in fresh waters with perchloric acid digestion.Crossref | GoogleScholarGoogle Scholar |
Kosiba P (1992) Studies on the ecology of Utricularia vulgaris L. I. Ecological differentiation of Utricularia vulgaris L. population affected by chemical factors of the habitat. Ekologia Polska 40, 147–192.
Macdonald CA, Thomas N, Robinson L, Tate KR, Ross DJ, Dando J, Singh BK (2009) Physiological, biochemical and molecular responses of the soil microbial community after afforestation of pastures with Pinus radiata. Soil Biology & Biochemistry 41, 1642–1651.
| Physiological, biochemical and molecular responses of the soil microbial community after afforestation of pastures with Pinus radiata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXoslGjsLs%3D&md5=4c8c6e3e1097da278b81c9aef875ce05CAS |
Manz W, Amann R, Ludwig E (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria – problems and solutions. Systematic and Applied Microbiology 15, 593–600.
Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga–Flavobacter–Bacteroides in the natural environment. Microbiology – UK 142, 1097–1106.
Mette N, Wilbert N, Barthlott W (2000) Food composition of aquatic bladderworts (Utricularia, Lentibulariaceae) in various habitats. Beiträge zur Biologie der Pflanzen 72, 1–13.
Mouquet N, Daufresne T, Gray SM, Miller TE (2008) Modelling the relationship between a pitcher plant (Sarracenia purpurea) and its phytotelma community: mutualism or parasitism? Functional Ecology 22, 728–737.
| Modelling the relationship between a pitcher plant (Sarracenia purpurea) and its phytotelma community: mutualism or parasitism?Crossref | GoogleScholarGoogle Scholar |
Muller B, Touraine B (1992) Inhibition of NO3 – uptake by various phloem-translocated amino acids in soybean seedlings. Journal of Experimental Botany 43, 617–623.
| Inhibition of NO3 – uptake by various phloem-translocated amino acids in soybean seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XksVOnsLg%3D&md5=39d1f4981c811a99ed8c44395a28bdcdCAS |
Neef A (1997) ‘Anwendung der in situ-Einzelzell-Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen.’ (PhD thesis, Technische Universität München: München, Germany)
Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In ‘Methods of soil analysis. Part 3: Chemical methods’. (Ed. DL Sparks) pp. 961–1010. (SSSA: Madison, WI, USA)
Neumann G, Römheld V (2007) The release of root exudates as affected by the plant physiological status. In ‘The rhizosphere – biochemistry and organic substances at the soil–plant interface’. (Eds R Pinton, Z Varanini, P Nannipieri) pp. 23–72. (CRC Press: Boca Raton, FL, USA)
Owen AG, Jones DL (2001) Competition for amino acids between wheat roots and rhizosphere micro-organisms and the role of amino acids in plant N acquisition. Soil Biology & Biochemistry 33, 651–657.
| Competition for amino acids between wheat roots and rhizosphere micro-organisms and the role of amino acids in plant N acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1aksLo%3D&md5=206d9e10932f92fd11ccbc1cb17ec26cCAS |
Paungfoo-Lonhienne C, Rentsch D, Robatzek S, Webb RI, Sagulenko E, Näsholm T, Schmidt S, Lonhienne T (2010) Turning the table: plants consume microbes as a source of nutrients. PLoS ONE 5, e11915
| Turning the table: plants consume microbes as a source of nutrients.Crossref | GoogleScholarGoogle Scholar | 20689833PubMed |
Peroutka M, Adlassnig W, Volgger M, Lendl T, Url WG, Lichtscheidl IK (2008) Utricularia: a vegetarian carnivorous plant? Plant Ecology 199, 153–162.
| Utricularia: a vegetarian carnivorous plant?Crossref | GoogleScholarGoogle Scholar |
Richards JH (2001) Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important? American Journal of Botany 88, 170–176.
| Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important?Crossref | GoogleScholarGoogle Scholar | 11159137PubMed |
Roller C, Wagner M, Amann RI, Ludwig W, Schleifer KH (1994) In situ probing of gram-positive bacteria with high DNA G+C content using 23S rRNA-targeted oligonucleotides. Microbiology 140, 2849–2858.
| In situ probing of gram-positive bacteria with high DNA G+C content using 23S rRNA-targeted oligonucleotides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhslGlu7Y%3D&md5=a6df4a6c53ccc9fbaf64996a33bb1b65CAS | 8000548PubMed |
Sasago A, Sibaoka T (1985a) Water extrusion in the trap bladders of Utricularia vulgaris. I. Possible pathway of water across the bladder wall. Botanical Magazine 98, 55–66.
| Water extrusion in the trap bladders of Utricularia vulgaris. I. Possible pathway of water across the bladder wall.Crossref | GoogleScholarGoogle Scholar |
Sasago A, Sibaoka T (1985b) Water extrusion in the trap bladders of Utricularia vulgaris. II. Possible mechanism of water outflow. Botanical Magazine 98, 113–124.
| Water extrusion in the trap bladders of Utricularia vulgaris. II. Possible mechanism of water outflow.Crossref | GoogleScholarGoogle Scholar |
Sekar R, Pernthaler A, Pernthaler J, Warnecke F, Posch T, Amann R (2003) An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization. Applied and Environmental Microbiology 69, 2928–2935.
| An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjslOlt7s%3D&md5=d539f4a96c9df9fa08e2f3b0cbbeb720CAS | 12732568PubMed |
Siragusa AJ (2007) Culturable bacteria present in the fluid of the hooded-pitcher plant Sarracenia minor based on 16S rDNA gene sequence data. Microbial Ecology 54, 324–331.
| Culturable bacteria present in the fluid of the hooded-pitcher plant Sarracenia minor based on 16S rDNA gene sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosVSls7w%3D&md5=7431b06c5efe218a0dcc82492c997d74CAS | 17380356PubMed |
Sirová D, Adamec L, Vrba J (2003) Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia. New Phytologist 159, 669–675.
| Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia.Crossref | GoogleScholarGoogle Scholar |
Sirová D, Borovec J, Černá B, Rejmánková E, Adamec L, Vrba J (2009) Microbial community development in the traps of aquatic Utricularia species. Aquatic Botany 90, 129–136.
| Microbial community development in the traps of aquatic Utricularia species.Crossref | GoogleScholarGoogle Scholar |
Sirová D, Borovec J, Šantrůčková H, Šantrůček J, Vrba J, Adamec L (2010) Utricularia carnivory revisited: plants supply photosynthetic carbon to traps. Journal of Experimental Botany 61, 99–103.
| Utricularia carnivory revisited: plants supply photosynthetic carbon to traps.Crossref | GoogleScholarGoogle Scholar | 19755570PubMed |
Söderling EM, Hietala-Lenkkeri AM (2010) Xylitol and erythritol decrease adherence of polysaccharide-producing oral streptococci. Current Microbiology 60, 25–29.
| Xylitol and erythritol decrease adherence of polysaccharide-producing oral streptococci.Crossref | GoogleScholarGoogle Scholar | 19777305PubMed |
Sorenson DR, Jackson WT (1968) The utilization of Paramecia by the carnivorous plant Utricularia gibba. Planta 83, 166–170.
| The utilization of Paramecia by the carnivorous plant Utricularia gibba.Crossref | GoogleScholarGoogle Scholar |
Sota T, Mogi M, Kato K (1998) Local and regional-scale food web structure in Nepenthes alata pitchers. Biotropica 30, 82–91.
| Local and regional-scale food web structure in Nepenthes alata pitchers.Crossref | GoogleScholarGoogle Scholar |
Stahl DA, Amann R (1991) Development and application of nucleic acid probes. In ‘Nucleic acid techniques in bacterial systematics’. (Eds E Stackebrandt, M Goodfellow) (John Wiley & Sons: London)
Sydenham PH, Findlay GP (1973) The rapid movements of the bladder of Utricularia sp. Australian Journal of Biological Sciences 26, 1115–1126.
Sydenham PH, Findlay GP (1975) Transport of solutes and water by resetting bladders of Utricularia. Australian Journal of Plant Physiology 2, 335–351.
Tapiainen T, Sormunen R, Kaijalainen T, Kontiokari T, Ikaheimo I, Uhari M (2004) Ultrastructure of Streptococcus pneumoniae after exposure to xylitol. Journal of Antimicrobial Chemotherapy 54, 225–228.
| Ultrastructure of Streptococcus pneumoniae after exposure to xylitol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlyjtbk%3D&md5=6114f1d3d55d79fa341fc84ffb78778aCAS | 15190027PubMed |
Taylor P (1989) ‘The genus Utricularia: a taxonomic monograph.’ (Kew Bulletin Additional Series, XIV, HMSO: London)
Uren NC (2007) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In ‘The rhizosphere – biochemistry and organic substances at the soil–plant interface’. (Eds R Pinton, Z Varanini, P Nannipieri) pp. 1–23. (CRC Press: Boca Raton, FL, USA)
