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.

Department of Breeding Research Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben Germany

Department of Breeding Research Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben Germany ; Faculty of Science and Central European Institute of Technology Masaryk University Brno Czech Republic

Department of Plant Breeding and Genetics Max Planck Institute for Plant Breeding Research Köln Germany

Zobrazit více v PubMed

Adamec L. (1997). Mineral nutrition of carnivorous plants: a review. Bot. Rev. 63, 273–299. 10.1007/BF02857953 DOI

Adamec L. (2003). Zero water flows in Genlisea traps. Carniv. Pl. Newslett. 32, 46–48.

Adamec L. (2007). Oxygen concentrations inside the traps of the carnivorous plants Utricularia and Genlisea (Lentibulariaceae). Ann. Bot. 100, 849–856. 10.1093/aob/mcm182 PubMed DOI PMC

Adlassnig W., Peroutka M., Lendl T. (2011). Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities. Ann. Bot. 107, 181–194. 10.1093/aob/mcq238 PubMed DOI PMC

Albert V. A., Jobson R. W., Michael T. P., Taylor D. J. (2010). The carnivorous bladderwort (Utricularia, Lentibulariaceae): a system inflates. J. Exp. Bot. 61, 5–9. 10.1093/jxb/erp349 PubMed DOI

Albert V. A., Williams S. E., Chase M. W. (1992). Carnivorous plants: phylogeny and structural evolution. Science 257, 1491–1495. 10.1126/science.1523408 PubMed DOI

Albino U., Saridakis D. P., Ferreira M. C., Hungria M., Vinuesa P., Andrade G. (2006). High diversity of diazotrophic bacteria associated with the carnivorous plant Drosera villosa var. villosa growing in oligotrophic habitats in Brazil. Plant Soil 287, 199–207. 10.1007/s11104-006-9066-7 DOI

Arndt D., Xia J., Liu Y., Zhou Y., Guo A. C., Cruz J. A., et al. . (2012). METAGENassist: a comprehensive web server for comparative metagenomics. Nucleic Acids Res. 40, W88–W95. 10.1093/nar/gks497 PubMed DOI PMC

Badri D. V., Chaparro J. M., Zhang R., Shen Q., Vivanco J. M. (2013). Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J. Biol. Chem. 288, 4502–4512. 10.1074/jbc.M112.433300 PubMed DOI PMC

Bakker P. A., Berendsen R. L., Doornbos R. F., Wintermans P. C., Pieterse C. M. (2013). The rhizosphere revisited: root microbiomics. Front. Plant Sci. 4:165. 10.3389/fpls.2013.00165 PubMed DOI PMC

Barthlott W., Porembski S., Fischer E., Gemmel B. (1998). First protozoa-trapping plant found. Nature 392, 447–447. 10.1038/33037 PubMed DOI

Berendsen R. L., Pieterse C. M., Bakker P. A. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486. 10.1016/j.tplants.2012.04.001 PubMed DOI

Broeckling C. D., Broz A. K., Bergelson J., Manter D. K., Vivanco J. M. (2008). Root exudates regulate soil fungal community composition and diversity. Appl. Environ. Microbiol. 74, 738–744. 10.1128/AEM.02188-07 PubMed DOI PMC

Bulgarelli D., Rott M., Schlaeppi K., Ver Loren Van Themaat E., Ahmadinejad N., Assenza F., et al. . (2012). Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95. 10.1038/nature11336 PubMed DOI

Caporaso J. G., Lauber C. L., Walters W. A., Berg-Lyons D., Lozupone C. A., Turnbaugh P. J., et al. . (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. U.S.A. 108, 4516–4522. 10.1073/pnas.1000080107 PubMed DOI PMC

Caravieri F. A., Ferreira A. J., Ferreira A., Clivati D., De Miranda V. F. O., Araújo W. L. (2014). Bacterial community associated with traps of the carnivorous plants Utricularia hydrocarpa and Genlisea filiformis. Aquat. Bot. 116, 8–12. 10.1016/j.aquabot.2013.12.008 DOI

Cardinale M., Grube M., Erlacher A., Quehenberger J., Berg G. (2015). Bacterial networks and co-occurrence relationships in the lettuce root microbiota. Environ. Microbiol. 17, 239–252. 10.1111/1462-2920.12686 PubMed DOI

Cohen I., Knopf J. A., Irihimovitch V., Shapira M. (2005). A proposed mechanism for the inhibitory effects of oxidative stress on Rubisco assembly and its subunit expression. Plant Physiol. 137, 738–746. 10.1104/pp.104.056341 PubMed DOI PMC

Conesa A., Gotz S. (2008). Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int. J. Plant Genomics 2008, 619832. 10.1155/2008/619832 PubMed DOI PMC

Crotti E., Damiani C., Pajoro M., Gonella E., Rizzi A., Ricci I., et al. . (2009). Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ. Microbiol. 11, 3252–3264. 10.1111/j.1462-2920.2009.02048.x PubMed DOI

De Muyt A., Pereira L., Vezon D., Chelysheva L., Gendrot G., Chambon A., et al. . (2009). A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet. 5:e1000654. 10.1371/journal.pgen.1000654 PubMed DOI PMC

Edgar R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461. 10.1093/bioinformatics/btq461 PubMed DOI

Edwards J., Johnson C., Santos-Medellin C., Lurie E., Podishetty N. K., Bhatnagar S., et al. . (2015). Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. U.S.A. 112, E911–E920. 10.1073/pnas.1414592112 PubMed DOI PMC

Eisen J. A., Coyne R. S., Wu M., Wu D., Thiagarajan M., Wortman J. R., et al. . (2006). Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4:e286. 10.1371/journal.pbio.0040286 PubMed DOI PMC

Ellison A. M., Gotelli N. J. (2001). Evolutionary ecology of carnivorous plants. Trends Ecol. Evol. 16, 623–629. 10.1016/S0169-5347(01)02269-8 DOI

Ellison A. M., Gotelli N. J. (2009). Energetics and the evolution of carnivorous plants–Darwin's ‘most wonderful plants in the world’. J. Exp. Bot. 60, 19–42. 10.1093/jxb/ern179 PubMed DOI

Farnsworth E. J., Ellison A. M. (2008). Prey availability directly affects physiology, growth, nutrient allocation and scaling relationships among leaf traits in 10 carnivorous plant species. J. Ecol. 96, 213–221. 10.1111/j.1365-2745.2007.01313.x. DOI

Fedoroff N. V. (2012). Presidential address. Transposable elements, epigenetics, and genome evolution. Science 338, 758–767. 10.1126/science.338.6108.758 PubMed DOI

Fleischmann A. (2012). Monograph of the Genus Genlisea. Poole; Dorset; England: Redfern Natural History Productions.

Fleischmann A., Schaferhoff B., Heubl G., Rivadavia F., Barthlott W., Muller K. F. (2010). Phylogenetics and character evolution in the carnivorous plant genus Genlisea A. St.-Hil. (Lentibulariaceae). Mol. Phylogenet. Evol. 56, 768–783. 10.1016/j.ympev.2010.03.009 PubMed DOI

Giorgi G., Marcantonio P., Del Re B. (2011). LINE-1 retrotransposition in human neuroblastoma cells is affected by oxidative stress. Cell Tissue Res. 346, 383–391. 10.1007/s00441-011-1289-0 PubMed DOI

Haichar F. Z., Marol C., Berge O., Rangel-Castro J. I., Prosser J. I., Balesdent J., et al. . (2008). Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2, 1221–1230. 10.1038/ismej.2008.80 PubMed DOI

Huson D. H., Mitra S., Ruscheweyh H.-J., Weber N., Schuster S. C. (2011). Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21, 1552–1560. 10.1101/gr.120618.111 PubMed DOI PMC

Ibarra-Laclette E., Albert V. A., Perez-Torres C. A., Zamudio-Hernandez F., Ortega-Estrada Mde J., Herrera-Estrella A., et al. . (2011). Transcriptomics and molecular evolutionary rate analysis of the bladderwort (Utricularia), a carnivorous plant with a minimal genome. BMC Plant Biol. 11:101. 10.1186/1471-2229-11-101 PubMed DOI PMC

Ikeda K., Nakayashiki H., Takagi M., Tosa Y., Mayama S. (2001). Heat shock, copper sulfate and oxidative stress activate the retrotransposon MAGGY resident in the plant pathogenic fungus Magnaporthe grisea. Mol. Genet. Genomics 266, 318–325. 10.1007/s004380100560 PubMed DOI

Jobson R. W., Morris E. C. (2001). Feeding ecology of a carnivorous bladderwort (Utricularia uliginosa, Lentibulariaceae). Austral. Ecol. 26, 680–691. 10.1046/j.1442-9993.2001.01149.x DOI

Jobson R. W., Playford J., Cameron K. M., Albert V. A. (2003). Molecular phylogenetics of Lentibulariaceae inferred from plastid rps 16 intron and trn LF DNA sequences: implications for character evolution and biogeography. Syst. Bot. 28, 157–171.

Ke X., Angel R., Lu Y., Conrad R. (2013). Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environ. Microbiol. 15, 2275–2292. 10.1111/1462-2920.12098 PubMed DOI

Kierul K., Voigt B., Albrecht D., Chen X. H., Carvalhais L. C., Borriss R. (2015). Influence of root exudates on the extracellular proteome of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Microbiology 161, 131–147. 10.1099/mic.0.083576-0 PubMed DOI

Koopman M., Carstens B. (2011). The microbial phyllogeography of the carnivorous plant Sarracenia alata. Microb. Ecol. 61, 750–758. 10.1007/s00248-011-9832-9 PubMed DOI

Krieger J. R., Kourtev P. S. (2012). Bacterial diversity in three distinct sub-habitats within the pitchers of the northern pitcher plant, Sarracenia purpurea. FEMS Microbiol. Ecol. 79, 555–567. 10.1111/j.1574-6941.2011.01240.x PubMed DOI

Król E., Płachno B. J., Adamec L., Stolarz M., Dziubiñska H., Trẽbacz K. (2012). Quite a few reasons for calling carnivores ‘the most wonderful plants in the world’. Ann. Bot. 109, 47–64. 10.1093/aob/mcr249 PubMed DOI PMC

Legendre L. (2000). The genus Pinguicula L. (Lentibulariaceae): an overview. Acta Bot. Gall. 147, 77–95. 10.1080/12538078.2000.10515837 DOI

Lugtenberg B., Kamilova F. (2009). Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556. 10.1146/annurev.micro.62.081307.162918 PubMed DOI

Lundberg D. S., Lebeis S. L., Paredes S. H., Yourstone S., Gehring J., Malfatti S., et al. . (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90. 10.1038/nature11237 PubMed DOI PMC

Meyers-Rice B. (1994). Are Genlisea traps active? A crude calculation. Carniv. Pl. Newslett 23, 40–42.

Mhiri C., Morel J. B., Vernhettes S., Casacuberta J. M., Lucas H., Grandbastien M. A. (1997). The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol. Biol. 33, 257–266. 10.1023/A:1005727132202 PubMed DOI

Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. (2004). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–498. 10.1016/j.tplants.2004.08.009 PubMed DOI

Muller K. F., Borsch T., Legendre L., Porembski S., Barthlott W. (2006). Recent progress in understanding the evolution of carnivorous Lentibulariaceae (Lamiales). Plant Biol. (Stuttg.) 8, 748–757. 10.1055/s-2006-924706 PubMed DOI

Ofek-Lalzar M., Sela N., Goldman-Voronov M., Green S. J., Hadar Y., Minz D. (2014). Niche and host-associated functional signatures of the root surface microbiome. Nat. Commun. 5, 4950. 10.1038/ncomms5950 PubMed DOI

Peterson C. N., Day S., Wolfe B. E., Ellison A. M., Kolter R., Pringle A. (2008). A keystone predator controls bacterial diversity in the pitcher-plant (Sarracenia purpurea) microecosystem. Environ. Microbiol. 10, 2257–2266. 10.1111/j.1462-2920.2008.01648.x PubMed DOI

Plachno B. J., Adamec L., Lichtscheidl I. K., Peroutka M., Adlassnig W., Vrba J. (2006). Fluorescence labelling of phosphatase activity in digestive glands of carnivorous plants. Plant Biol. (Stuttg.) 8, 813–820. 10.1055/s-2006-924177 PubMed DOI

Płachno B. J., Adamus K., Faber J., Kozłowski J. (2005). Feeding behaviour of carnivorous Genlisea plants in the laboratory. Acta Bot. Gall. 152, 159–164. 10.1080/12538078.2005.10515466 DOI

Plachno B. J., Kozieradzka-Kiszkurno M., Swiatek P. (2007). Functional utrastructure of Genlisea (Lentibulariaceae) digestive hairs. Ann. Bot. 100, 195–203. 10.1093/aob/mcm109 PubMed DOI PMC

Plachno B. J., Wolowski K. (2008). Algae commensal community in Genlisea traps. Acta Soc. Bot. Pol. 77, 77–86. 10.5586/asbp.2008.011 DOI

Prankevicius A. B., Cameron D. M. (1991). Bacterial Dinitrogen Fixation in the Leaf of the Northern Pitcher Plant (Sarracenia-Purpurea). Can. J. Bot. 69, 2296–2298. 10.1139/b91-289 DOI

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., et al. . (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596. 10.1093/nar/gks1219 PubMed DOI PMC

Reinhold-Hurek B., Hurek T. (2011). Living inside plants: bacterial endophytes. Curr. Opin. Plant Biol. 14, 435–443. 10.1016/j.pbi.2011.04.004 PubMed DOI

Richards J. (2001). Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important? Am. J. Bot. 88, 170–176. 10.2307/2657137 PubMed DOI

Rockwood L. D., Felix K., Janz S. (2004). Elevated presence of retrotransposons at sites of DNA double strand break repair in mouse models of metabolic oxidative stress and MYC-induced lymphoma. Mutat Res. 548, 117–125. 10.1016/j.mrfmmm.2004.01.005 PubMed DOI

Rout M. E., Callaway R. M. (2012). Interactions between exotic invasive plants and soil microbes in the rhizosphere suggest that ‘everything is not everywhere’. Ann. Bot. 110, 213–222. 10.1093/aob/mcs061 PubMed DOI PMC

Siragusa A., Swenson J., Casamatta D. (2007). Culturable bacteria present in the fluid of the hooded-pitcher plant Sarracenia minor based on 16S rDNA gene sequence data. Microb. Ecol. 54, 324–331. 10.1007/s00248-006-9205-y PubMed DOI

Sirová D., Adamec L., Vrba J. (2003). Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia. New Phytol. 159, 669–675. 10.1046/j.1469-8137.2003.00834.x PubMed DOI

Sirová D., Borovec J., Èerná B., Rejmánková E., Adamec L., Vrba J. (2009). Microbial community development in the traps of aquatic Utricularia species. Aquat. Bot. 90, 129–136. 10.1016/j.aquabot.2008.07.007 DOI

Sirova D., Santrucek J., Adamec L., Barta J., Borovec J., Pech J., et al. . (2014). Dinitrogen fixation associated with shoots of aquatic carnivorous plants: is it ecologically important? Ann. Bot. 114, 125–133. 10.1093/aob/mcu067 PubMed DOI PMC

Skutch A. F. (1928). The capture of prey by the bladderwort. New Phytol. 27, 261–297. 10.1111/j.1469-8137.1928.tb06742.x DOI

Soltis P. S., Soltis D. E., Wolf P. G., Nickrent D. L., Chaw S. M., Chapman R. L. (1999). The phylogeny of land plants inferred from 18S rDNA sequences: pushing the limits of rDNA signal? Mol. Biol. Evol. 16, 1774–1784. 10.1093/oxfordjournals.molbev.a026089 PubMed DOI

Studnicka M. (1996). Several ecophysiological observations in Genlisea. Carniv. Pl. Newslett. 25, 14–16.

Studnicka M. (2003a). Further problem in Genlisea trap untangled. Carniv. Pl. Newslett. 32, 40–45.

Studnicka M. (2003b). Genlisea traps - A new piece of knowledge. Carniv. Pl. Newslett. 32, 36–39.

Studnicka M. (2003c). Observations on life strategies of Genlisea, Heliamphora, and Utricularia in natural habitats. Carniv. Pl. Newslett. 32, 57–61.

Suen G., Scott J. J., Aylward F. O., Adams S. M., Tringe S. G., Pinto-Tomas A. A., et al. . (2010). An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genet. 6:e1001129. 10.1371/journal.pgen.1001129 PubMed DOI PMC

Turner T. R., Ramakrishnan K., Walshaw J., Heavens D., Alston M., Swarbreck D., et al. . (2013). Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J. 7, 2248–2258. 10.1038/ismej.2013.119 PubMed DOI PMC

Vandenkoornhuyse P., Quaiser A., Duhamel M., Le Van A., Dufresne A. (2015). The importance of the microbiome of the plant holobiont. New Phytol. 206, 1196–1206. 10.1111/nph.13312 PubMed DOI

Vincent O., Weisskopf C., Poppinga S., Masselter T., Speck T., Joyeux M., et al. . (2011). Ultra-fast underwater suction traps. Proc. Biol. Sci. 278, 2909–2914. 10.1098/rspb.2010.2292 PubMed DOI PMC

Ward N. L., Challacombe J. F., Janssen P. H., Henrissat B., Coutinho P. M., Wu M., et al. . (2009). Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl. Environ. Microbiol. 75, 2046–2056. 10.1128/AEM.02294-08 PubMed DOI PMC

Yarza P., Yilmaz P., Pruesse E., Glockner F. O., Ludwig W., Schleifer K. H., et al. . (2014). Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat. Rev. Microbiol. 12, 635–645. 10.1038/nrmicro3330 PubMed DOI

Chromosome identification for the carnivorous plant Genlisea margaretae

Chromatin organization and cytological features of carnivorous Genlisea species with large genome size differences