Metatranscriptome analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species

Frontiers in Microbiology

Volumn 6, Issue MAY, 2015, Pages

  Cao, Hieu X ^a   Schmutzer, Thomas ^a   Scholz, Uwe ^a   Pecinka, Ales ^b   Schubert, Ingo ^a,c   Vu, Giang T ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c MASARYK UNIVERSITY   (Czech Republic)

Author keywords

Algae commensalism; Genlisea; Lobster pot trapping; Metatranscriptomics; Plant carnivory; Plant microbe interaction; RNA sequencing; Whole genome gene transcription analysis

Indexed keywords

TRANSCRIPTOME;

ARTICLE; CARNIVOROUS PLANT; CONTIG MAPPING; DOWN REGULATION; GENE EXPRESSION; GENE INTERACTION; GENLISEA; LAMIALES; MICROBIOME; NONHUMAN; UPREGULATION;

ALGAE; AMOEBOZOA; CHLOROPHYTA; CILIOPHORA; FUNGI; GENLISEA; GENLISEA HISPIDULA; METAZOA; PROTEOBACTERIA;

EID: 84935842989     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00526     Document Type: Article

References (77)

1. Adamec, L. (1997). Mineral nutrition of carnivorous plants: A review. Bot. Rev 63, 273-299. doi: 10.1007/BF02857953.
2. Adamec, L. (2003). Zero water flows in Genlisea traps. Carniv. Pl. Newslett. 32, 46-48.
3. Adamec, L. (2007). Oxygen concentrations inside the traps of the carnivorous plants Utricularia and Genlisea (Lentibulariaceae). Ann Bot 100, 849-856. doi: 10.1093/aob/mcm182.
4. Adlassnig, W., Peroutka, M., and Lendl, T. (2011). Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities. Ann Bot 107, 181-194. doi: 10.1093/aob/mcq238.
5. Albert, V.A., Jobson, R.W., Michael, T.P., and Taylor, D.J. (2010). The carnivorous bladderwort (Utricularia, Lentibulariaceae): a system inflates. J. Exp. Bot. 61, 5-9. doi: 10.1093/jxb/erp349.
6. Albert, V.A., Williams, S.E., and Chase, M.W. (1992). Carnivorous plants: phylogeny and structural evolution. Science 257, 1491-1495.
7. Albino, U., Saridakis, D.P., Ferreira, M.C., Hungria, M., Vinuesa, P., and 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. doi: 10.1007/s11104-006-9066-7.
8. 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, W88-95. doi: 10.1093/nar/gks497.
9. Badri, D.V., Chaparro, J.M., Zhang, R., Shen, Q., and 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. doi: 10.1074/jbc.M112.433300.
10. Bakker, P.A., Berendsen, R.L., Doornbos, R.F., Wintermans, P.C., and Pieterse, C.M. (2013). The rhizosphere revisited: root microbiomics. Front Plant Sci 4, 165. doi: 10.3389/fpls.2013.00165.
11. Barthlott, W., Porembski, S., Fischer, E., and Gemmel, B. (1998). First protozoa-trapping plant found. Nature 392, 447-447.
12. Berendsen, R.L., Pieterse, C.M., and Bakker, P.A. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478-486. doi: 10.1016/j.tplants.2012.04.001.
13. Broeckling, C.D., Broz, A.K., Bergelson, J., Manter, D.K., and Vivanco, J.M. (2008). Root exudates regulate soil fungal community composition and diversity. Appl. Environ. Microbiol. 74, 738-744. doi: 10.1128/AEM.02188-07.
14. 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 root603 inhabiting bacterial microbiota. Nature 488, 91-95. doi: 10.1038/nature11336.
15. 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. PNAS 108, 4516-4522. doi: DOI 10.1073/pnas.1000080107.
16. Caravieri, F.A., Ferreira, A.J., Ferreira, A., Clivati, D., De Miranda, V.F.O., and Araújo, W.L. (2014). Bacterial community associated with traps of the carnivorous plants Utricularia hydrocarpa and Genlisea filiformis. Aquat. Bot. 116, 8-12. doi: 10.1016/j.aquabot.2013.12.008.
17. Cardinale, M., Grube, M., Erlacher, A., Quehenberger, J., and Berg, G. (2015). Bacterial networks and co-occurrence relationships in the lettuce root microbiota. Environ Microbiol 17, 239-252. doi: 10.1111/1462-2920.12686.
18. Cohen, I., Knopf, J.A., Irihimovitch, V., and 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. doi: 10.1104/pp.104.056341.
19. Conesa, A., and Gotz, S. (2008). Blast2GO: A comprehensive suite for functional analysis in plant genomics. International journal of plant genomics 2008, 619832. doi: 10.1155/2008/619832.
20. 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. doi: 10.1111/j.1462-2920.2009.02048.x.
21. 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. doi: 10.1371/journal.pgen.1000654.
22. Edgar, R.C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461.
23. 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. PNAS. doi: 10.1073/pnas.1414592112.
24. 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. doi: 10.1371/journal.pbio.0040286.
25. Ellison, A.M., and Gotelli, N.J. (2001). Evolutionary ecology of carnivorous plants. Trends Ecol. Evol. 16, 623-629. doi: 10.1016/S0169-5347(01)02269-8.
26. Ellison, A.M., and 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. doi: 10.1093/jxb/ern179.
27. Farnsworth, E.J., and 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. doi: 10.1111/j.1365-2745.2007.01313.x.
28. Fedoroff, N.V. (2012). Presidential address. Transposable elements, epigenetics, and genome evolution. Science 338, 758-767.
29. Fleischmann, A. (2012). Monograph of the Genus Genlisea. Poole, Dorset, England: Redfern Natural History Productions.
30. Fleischmann, A., Schaferhoff, B., Heubl, G., Rivadavia, F., Barthlott, W., and Muller, K.F. (2010). Phylogenetics and character evolution in the carnivorous plant genus Genlisea A. St.-Hil. (Lentibulariaceae). Mol. Phylogenet. Evol. 56, 768-783. doi: 10.1016/j.ympev.2010.03.009.
31. Giorgi, G., Marcantonio, P., and Del Re, B. (2011). LINE-1 retrotransposition in human neuroblastoma cells is affected by oxidative stress. Cell Tissue Res. 346, 383-391. doi: 10.1007/s00441-011-1289-0.
32. 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. doi: 10.1038/ismej.2008.80.
33. Huson, D.H., Mitra, S., Ruscheweyh, H.-J., Weber, N., and Schuster, S.C. (2011). Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21, 1552-1560.
34. 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 662 plant with a minimal genome. BMC Plant Biol. 11, 101. doi: 10.1186/1471-2229-11-101.
35. Ikeda, K., Nakayashiki, H., Takagi, M., Tosa, Y., and 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.
36. Jobson, R.W., and Morris, E.C. (2001). Feeding ecology of a carnivorous bladderwort (Utricularia uliginosa, Lentibulariaceae). Austral. Ecol. 26, 680-691. doi: 10.1046/j.1442-9993.2001.01149.x.
37. Jobson, R.W., Playford, J., Cameron, K.M., and 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.
38. Ke, X., Angel, R., Lu, Y., and Conrad, R. (2013). Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environ Microbiol 15, 2275-2292. doi: 10.1111/1462-2920.12098.
39. Kierul, K., Voigt, B., Albrecht, D., Chen, X.H., Carvalhais, L.C., and Borriss, R. (2015). Influence of root exudates on the extracellular proteome of the plant growth678 promoting bacterium Bacillus amyloliquefaciens FZB42. Microbiology 161, 131-147. doi: 10.1099/mic.0.083576-0.
40. Koopman, M., and Carstens, B. (2011). The microbial phyllogeography of the carnivorous plant Sarracenia alata. Microb. Ecol. 61, 750-758. doi: 10.1007/s00248-011-9832-9.
41. Krieger, J.R., and 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. doi: 10.1111/j.1574-6941.2011.01240.x.
42. Król, E., Plachno, B.J., Adamec, L., Stolarz, M., Dziubińska, H., and Trębacz, K. (2012). Quite a few reasons for calling carnivores 'the most wonderful plants in the world'. Ann. Bot. 109, 47-64. doi: 10.1093/aob/mcr249.
43. Legendre, L. (2000). The genus Pinguicula L.(Lentibulariaceae): an overview. Acta Bot. Gall. 147, 77-95.
44. Lugtenberg, B., and Kamilova, F. (2009). Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541-556. doi: 10.1146/annurev.micro.62.081307.162918.
45. 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. doi: 10.1038/nature11237.
46. Meyers-Rice, B. (1994). Are Genlisea traps active? A crude calculation. Carniv. Pl. Newslett 23, 40-42.
47. Mhiri, C., Morel, J.B., Vernhettes, S., Casacuberta, J.M., Lucas, H., and 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. doi: 10.1023/A:1005727132202.
48. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498. doi: 10.1016/j.tplants.2004.08.009.
49. Muller, K.F., Borsch, T., Legendre, L., Porembski, S., and Barthlott, W. (2006). Recent progress in understanding the evolution of carnivorous Lentibulariaceae (Lamiales). Plant Biol. (Stuttg.) 8, 748-757. doi: 10.1055/s-2006-924706.
50. Ofek-Lalzar, M., Sela, N., Goldman-Voronov, M., Green, S.J., Hadar, Y., and Minz, D. (2014). Niche and host-associated functional signatures of the root surface microbiome. Nat Commun 5, 4950. doi: 10.1038/ncomms5950.
51. Peterson, C.N., Day, S., Wolfe, B.E., Ellison, A.M., Kolter, R., and Pringle, A. (2008). A keystone predator controls bacterial diversity in the pitcher-plant (Sarracenia purpurea) microecosystem. Environ Microbiol 10, 2257-2266. doi: 10.1111/j.1462-2920.2008.01648.x.
52. Plachno, B.J., Adamec, L., Lichtscheidl, I.K., Peroutka, M., Adlassnig, W., and Vrba, J. (2006). Fluorescence labelling of phosphatase activity in digestive glands of carnivorous plants. Plant Biol. (Stuttg.) 8, 813-820. doi: 10.1055/s-2006-924177.
53. Plachno, B.J., Adamus, K., Faber, J., and Kozlowski, J. (2005). Feeding behaviour of carnivorous Genlisea plants in the laboratory. Acta Bot. Gall. 152, 159-164.
54. Plachno, B.J., Kozieradzka-Kiszkurno, M., and Swiatek, P. (2007). Functional utrastructure of Genlisea (Lentibulariaceae) digestive hairs. Ann Bot 100, 195-203. doi: 10.1093/aob/mcm109.
55. Plachno, B.J., and Wolowski, K. (2008). Algae commensal community in Genlisea traps. Acta Soc. Bot. Pol. 77.
56. Prankevicius, A.B., and Cameron, D.M. (1991). Bacterial Dinitrogen Fixation in the Leaf of the Northern Pitcher Plant (Sarracenia-Purpurea). Can. J. Bot. 69, 2296-2298.
57. 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 web727 based tools. Nucleic Acids Res. 41, D590-596. doi: 10.1093/nar/gks1219.
58. Reinhold-Hurek, B., and Hurek, T. (2011). Living inside plants: bacterial endophytes. Curr. Opin. Plant Biol. 14, 435-443. doi: 10.1016/j.pbi.2011.04.004.
59. Richards, J. (2001). Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important? Am. J. Bot. 88, 170-176.
60. Rockwood, L.D., Felix, K., and 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-Fund Mol M 548, 117-125. doi: 10.1016/j.mrfmmm.2004.01.005.
61. Rout, M.E., and 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. doi: 10.1093/aob/mcs061.
62. Siragusa, A., Swenson, J., and 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. doi: 10.1007/s00248-006-9205-y.
63. Sirová, D., Adamec, L., and Vrba, J. (2003). Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia. New Phytol. 159, 669-675. doi: 10.1046/j.1469-8137.2003.00834.x.
64. Sirová, D., Borovec, J., Cerná, B., Rejmánková, E., Adamec, L., and Vrba, J. (2009). Microbial community development in the traps of aquatic Utricularia species. Aquat. Bot. 90, 129-136. doi: 10.1016/j.aquabot.2008.07.007.
65. 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. doi: 10.1093/Aob/Mcu067.
66. Skutch, A.F. (1928). The capture of prey by the bladderwort. New Phytol. 27, 261-297. doi: 10.1111/j.1469-8137.1928.tb06742.x.
67. Soltis, P.S., Soltis, D.E., Wolf, P.G., Nickrent, D.L., Chaw, S.M., and 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.
68. Studnicka, M. (1996). Several ecophysiological observations in Genlisea. Carniv. Pl. Newslett. 25, 14-16.
69. Studnicka, M. (2003a). Further problem in Genlisea trap untangled. Carniv. Pl. Newslett. 32, 40-45.
70. Studnicka, M. (2003b). Observations on life strategies of Genlisea, Heliamphora, and Utricularia in natural habitats. Carniv. Pl. Newslett. 32, 57-61.
71. 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. doi: 10.1371/journal.pgen.1001129.
72. 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. doi: 10.1038/ismej.2013.119.
73. Vandenkoornhuyse, P., Quaiser, A., Duhamel, M., Le Van, A., and Dufresne, A. (2015). The importance of the microbiome of the plant holobiont. New Phytol. doi: 10.1111/nph.13312.
74. 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. doi: 10.1098/rspb.2010.2292.
75. Vu, G.T.H., Schmutzer, T., Bull, F., Cao, H.X., Fuchs, J., Tran, T.D., et al. (2015). Rapid and divergent genome size evolution in carnivorous plants without obvious selection pressure. The Plant Genome submitted.
76. 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. doi: 10.1128/AEM.02294-08.
77. 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. doi: 10.1038/Nrmicro3330.