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Titel:Colonization of the rice rhizosphere by microbial communities involved in the syntrophic degradation of rhizodeposits to methane
Autor:Vogel, Dirk
Weitere Beteiligte: Conrad, Ralf (Prof. Dr.)
Veröffentlicht:2017
URI:https://archiv.ub.uni-marburg.de/diss/z2017/0241
DOI: https://doi.org/10.17192/z2017.0241
URN: urn:nbn:de:hebis:04-z2017-02419
DDC: Naturwissenschaften
Titel (trans.):Besiedlung der Reis-Rhizosphäre durch am syntrophen Abbau von Rhizodepositen zu Methan beteiligte mikrobielle Lebensgemeinschaften
Publikationsdatum:2017-12-14
Lizenz:https://creativecommons.org/licenses/by-nc-sa/4.0

Dokument

Schlagwörter:
rhizosphere, Methanogenese, Abbau von organischen Substanzen, Rhizodeposition, Rhizosphäre, organic matter degradation, Methanogenese, methanogenesis, rhizodeposition, Rhizosphäre

Summary:
Roots represent the primary site of direct interaction between rice plants and soil microorganisms. The influence of the plant on the soil microbial community includes the translocation of photosynthetically fixed carbon into the rhizosphere as rhizodeposition. This extends to the rhizosphere of rice plants, which is colonized by a syntrophic microbial community, which in turn is able to degrade root derived carbon to methane. Each plant species is thought to select a specific microbial community composition as root microbiome. A general understanding of microbial colonization of the rice rhizosphere and the consequential impact on the emission of methane originating from rhizodeposits is still uncertain, since the majority of the studies have so far focused exclusively on rice roots planted in rice paddy soils. Therefore, we used different initial soil microbial communities available for colonization of the rice roots. In order to do this, an inert sand-vermiculite matrix was inoculated with rice paddy soil and digested sludge, respectively, and was afterwards planted with rice. The microbial activity essential for the formation of methane from those soil-systems was tested in pre-experiments and the colonization of the rice rhizosphere was determined afterwards in plant-soil microcosms. Each of the microcosms possessed an individually structured microbial community, which served as a seed bank for the colonization of the rice roots. We analyzed the impact of the community composition on the emission of methane by combining 13CO2 pulse-labeling with illumina sequencing and quantitative PCR, targeting the 16S rRNA as phylogenetic-, as well as mcrA and pmoA as functional marker genes for methanogenic archaea and methane-oxidizing bacteria. The degradation of rhizodeposits to methane in the different microcosms was dependent on the bacterial and methanogenic community structure, but not on their absolute abundance in the rhizosphere. Like the colonization of the rhizosphere by bacteria and methanogenic archaea, the translocation of photosynthetically fixed carbon depended upon the initial microbial communities. Nevertheless, the rice rhizosphere was found to be a distinct habitat for bacteria and methanogenic archaea. We were able to identify a methanogenic community which was linked to the degradation of rhizodeposits to methane across the rhizosphere of all microcosms. Besides hydrogenotrophic Methanocella and Methanobacteriaceae, acetoclastic Methanosaeta could also be assigned to this community. Nevertheless, most methanogens which contribute to the emission of methane originating from root derived carbon were found to belong to those with a hydrogenotrophic pathway. Within the methanogenic community linked to the formation of methane from rhizodeposits, the root surface was mainly colonized by hydrogenotrophic methanogens, while those able to perform acetoclastic methanogenesis were highly abundant in the rhizospheric soil. This was true of the colonization of the rice rhizosphere by methanogenic archaea in general. Furthermore, we were able to identify methanogens which were ubiquitous in the rhizosphere of all microcosms. Those were considered as methanogenic community selected by the rice plant on its roots. Representatives of Methanobacteriaceae, Methanosaeta and Methanosarcina colonized the overall rhizosphere, while Methanocella were found to be present in the rhizospheric soil of all microcosms. In addition to this, all methanogenic archaea which were linked to the degradation of root derived carbon to methane also belonged to this root associated community. Hence, the methanogenic community selected on the rice root also contributed to the formation of methane from rhizodeposits. Besides methanogens, we were also able to identify certain bacterial groups, which are linked to the degradation of root derived carbon to methane. These includes representatives of Kineosporiaceae, Anaeromyxobacter, Bradyrhizobium, and Bacteroidales. A higher abundance of Kineosporiaceae also resulted in an increased conversion of root derived carbon compounds to acetate, CO2, and propionate. Therefore, at least the family of Kineosporiaceae was thought to be actively involved in the degradation of rhizodeposition to precursors for methanogenesis. Nevertheless, we were not able to determine bacteria which contributed to the emission of methane originating from root derived carbon and which were ubiquitous in the rhizosphere of all soil-systems. This resulted from the fact that the microbial community structure of the rhizosphere also depended on the initial pool of microorganisms available for root colonization.

Bibliographie / References

  1. El-Khawas, H., and Adachi, K. (1999). Identification and quantification of auxins in culture media of Azospirillum and Klebsiella and their effect on rice roots. Biology and Fertility of Soils, 28(4), 377-381. doi:10.1007/s003740050507
  2. Sundberg, C., Al-Soud, W. A., Larsson, M., Alm, E., Yekta, S. S., Svensson, B. H., Karlsson, A. (2013). 454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters. FEMS Microbiology Ecology, 85: 612-626.
  3. Wardle, D. A. (1992). A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biological Reviews, 67: 321-358.
  4. Ho, A., Lüke, C., Cao, Z., and Frenzel, P. (2011). Ageing well: methane oxidation and methane oxidizing bacteria along a chronosequence of 2000 years. Environmental Microbiology Reports, 3: 738-743.
  5. Van Bodegom, P., Goudriaan, J., and Leffelaar, P. (2001). A mechanistic model on methane oxidation in a rice rhizosphere. Biogeochemistry, 55: 145-177.
  6. Raghoebarsing, A. A., Pol, A., van de Pas-Schoonen, K. T., Smolders, A. J. P., Ettwig, K. F., Rijpstra, W. I. C., Strous, M. (2006). A microbial consortium couples anaerobic methane oxidation to denitrification. Nature, 440: 918-921.
  7. Minamisawa, K., Nishioka, K., Miyaki, T., Ye, B., Miyamoto, T., You, M., Sato, T. (2004). Anaerobic Nitrogen-Fixing Consortia Consisting of Clostridia Isolated from Gramineous Plants. Applied and Environmental Microbiology, 70: 3096-3102.
  8. Haroon, M. F., Hu, S., Shi, Y., Imelfort, M., Keller, J., Hugenholtz, P., Tyson, G. W. (2013). Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature, 500: 567-570.
  9. Shapiro, S. S., and Wilk, M. B. (1965). An Analysis of Variance Test for Normality. Biometrika, 52: 591-611.
  10. Krummen, M., Hilkert, A. W., Juchelka, D., Duhr, A., Schlüter, H.-J., and Pesch, R. (2004). A new concept for isotope ratio monitoring liquid chromatography/mass spectrometry. Rapid Communications in Mass Spectrometry, 18: 2260-2266.
  11. Royston, J. P. (1982). An Extension of Shapiro and Wilk's W Test for Normality to Large Samples. Journal of the Royal Statistical Society. Series C (Applied Statistics), 31: 115-124.
  12. McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., Hugenholtz, P. (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J, 6: 610-618.
  13. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Schleifer, K. (2004). ARB: a software environment for sequence data. Nucleic Acids Research, 32: 1363-1371.
  14. Dennis, P. G., Miller, A. J., and Hirsch, P. R. (2010). Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiology Ecology, 72: 313-327.
  15. Khammas, K. M., Ageron, E., Grimont, P. A. D., and Kaiser, P. (1989). Azospirillum irakense sp. nov., a nitrogen-fixing bacterium associated with rice roots and. Research in Microbiology, 140: 679-693.
  16. Xie, C.-H., and Yokota, A. (2005a). Azospirillum oryzae sp. nov., a nitrogen-fixing bacterium isolated from the roots of the rice plant Oryza sativa. International Journal of Systematic and Evolutionary Microbiology, 55: 1435-1438.
  17. Ikenaga, M., Asakawa, S., Muraoka, Y., and Kimura, M. (2003). Bacterial communities associated with nodal roots of rice plants along with the growth stages: estimation by PCR-DGGE and sequence analyses. Soil Science and Plant Nutrition, 49: 591-602.
  18. Hiltner, L. (1904). Über neuere Erfahrungen und Probleme auf dem Gebiet der Bodenbakteriologie unter besonderer Berücksichtigung der Gründüngung und Brache. Deutsches Landwirtschaftliches Gesetz, 98: 59-78.
  19. Thauer, R. K. (1998). Biochemistry of methanogenesis: a tribute to Marjory Stephenson: 1998 Marjory Stephenson Prize Lecture. Microbiology, 144: 2377-2406.
  20. Ge, T., Yuan, H., Zhu, H., Wu, X., Nie, S., Liu, C., Brookes, P. (2012). Biological carbon assimilation and dynamics in a flooded rice - Soil system. Soil Biology and Biochemistry, 48: 39-46.
  21. Kimura, M., Murase, J., and Lu, Y. (2004). Carbon cycling in rice field ecosystems in the context of input, decomposition and translocation of organic materials and the fates of their end products (CO2 and CH4). Soil Biology and Biochemistry, 36: 1399-1416.
  22. Pump, J. (2012). Carbon translocation and methane emission in flooded rice microcosms with a manipulated root microbiome. Dissertationsschrift. Philipps-Universität Marburg.
  23. Dumont, M. G., Lüke, C., Deng, Y., and Frenzel, P. (2014). Classification of pmoA amplicon pyrosequences using BLAST and the lowest common ancestor method in MEGAN. Frontiers in Microbiology, 5.
  24. IPCC. (2014). Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva: IPCC secretariat.
  25. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22: 4673-4680.
  26. Kemnitz, D., Chin, K. J., Bodelier, P., and Conrad, R. (2004). Community analysis of methanogenic archaea within a riparian flooding gradient. Environmental Microbiology, 6: 449-461.
  27. Tringe, S. G., von Mering, C., Kobayashi, A., Salamov, A. A., Chen, K., Chang, H. W., Rubin, E. M. (2005). Comparative Metagenomics of Microbial Communities. Science, 308: 554-557.
  28. Verhagen, F. J. M., Laanbroek, H. J., and Woldendrop, J. W. (1995). Competition for ammonium between plant roots and nitrifying and heterotrophic bacteria and the effects of protozoan grazing. Plant and Soil, 170: 241-250.
  29. Lü, Z., and Lu, Y. (2012). Complete Genome Sequence of a Thermophilic Methanogen, Methanocella conradii HZ254, Isolated from Chinese Rice Field Soil. Journal of Bacteriology, 194: 2398-2399.
  30. Kaneko, T., Nakamura, Y., Sato, S., Minamisawa, K., Uchiumi, T., Sasamoto, S., Tabata, S. (2002). Complete Genomic Sequence of Nitrogen-fixing Symbiotic Bacterium Bradyrhizobium japonicum USDA110. DNA Research, 9: 189-197.
  31. Jones, D. A., Ryder, M. H., Clare, B. G., Farrand, S. K., and Kerr, A. (1988). Construction of a Tradeletion mutant of pAgK84 to safeguard the biological control of crown gall. Molecular and General Genetics MGG, 212: 207-214.
  32. Minoda, T., and Kimura, M. (1994). Contribution of photosynthesized carbon to the methane emitted from paddy fields. Geophysical Research Letters, 21: 2007-2010.
  33. Lu, Y., Watanabe, A., and Kimura, M. (2002). Contribution of plant-derived carbon to soil microbial biomass dynamics in a paddy rice microcosm. Biol Fertil Soils Biology and Fertility of Soils. 36: 136-142.
  34. Murayama, S. (1984a). Decomposition kinetics of straw saccharides and synthesis of microbial saccharides under field conditions. Journal of Soil Science, 35: 231-242.
  35. Lu, Y., Lüders, T., Friedrich, M. W., and Conrad, R. (2005). Detecting active methanogenic populations on rice roots using stable isotope probing. Environmental Microbiology, 7: 326- 336.
  36. Hernández, M., Dumont, M. G., Yuan, Q., and Conrad, R. (2015). Different bacterial populations associated with the roots and rhizosphere of rice incorporate plant-derived carbon. Applied and Environmental Microbiology, 81: 2244-2253.
  37. van Bodegom, P. M., Scholten, J. C. M., and Stams, A. J. M. (2004). Direct inhibition of methanogenesis by ferric iron. FEMS Microbiology Ecology, 49: 261-268.
  38. Hogslund, N., Radutoiu, S., Krusell, L., Voroshilova, V., Hannah, M. A., Goffard, N., Stougaard, J. (2009). Dissection of Symbiosis and Organ Development by Integrated Transcriptome Analysis of Lotus japonicus Mutant and Wild-Type Plants. PLoS ONE, 4: e6556.
  39. Lovley, D. R., Holmes, D. E., and Nevin, K. P. (2004). Dissimilatory Fe(III) and Mn(IV) Reduction. Advances in microbial physiology. 49: 219-286.
  40. Roden, E. E. (2003). Diversion of Electron Flow from Methanogenesis to Crystalline Fe(III) Oxide Reduction in Carbon-Limited Cultures of Wetland Sediment Microorganisms. Applied and Environmental Microbiology, 69: 5702-5706.
  41. Großkopf, R., Janssen, P. H., and Liesack, W. (1998a). Diversity and Structure of the Methanogenic Community in Anoxic Rice Paddy Soil Microcosms as Examined by Cultivation and Direct 16S rRNA Gene Sequence Retrieval. Applied and Environmental Microbiology, 64: 960-969.
  42. Watanabe, T., Kimura, M., and Asakawa, S. (2010). Diversity of methanogenic archaeal communities in Japanese paddy field ecosystem, estimated by denaturing gradient gel electrophoresis. Biology and Fertility of Soils, 46: 343-353.
  43. Tourlousse, D. M., Honda, T., Matsuura, N., Ohashi, A., Tonouchi, A., and Sekiguchi, Y. (2015). Draft Genome Sequence of Bacteroidales Strain 6E, Isolated from a Rice Paddy Field in Japan. Genome Announcements, 3: e01167-15.
  44. Tourlousse, D. M., Matsuura, N., Sun, L., Toyonaga, M., Kuroda, K., Ohashi, A., Sekiguchi, Y. (2015). Draft Genome Sequence of Bacteroidales Strain TBC1, a Novel Isolate from a Methanogenic Wastewater Treatment System. Genome Announcements, 3: e01168-15.
  45. Lu, Y. H., Wassmann, R., Neue, H. U., and Huang, C. Y. (2000). Dynamics of dissolved organic carbon and methane emissions in a flooded rice soil. Soil Science Society of America Journal, 64: 2011-2017.
  46. Hardoim, P. R., Hardoim, C. C. P., van Overbeek, L. S., and van Elsas, J. D. (2012). Dynamics of Seed-Borne Rice Endophytes on Early Plant Growth Stages. PLoS ONE, 7: e30438.
  47. Peng, J., Lü, Z., Rui, J., and Lu, Y. (2008). Dynamics of the Methanogenic Archaeal Community during Plant Residue Decomposition in an Anoxic Rice Field Soil. Applied and Environmental Microbiology, 74: 2894-2901.
  48. Conrad, R., and Klose, M. (2006). Dynamics of the methanogenic archaeal community in anoxic rice soil upon addition of straw. European Journal of Soil Science, 57: 476-484.
  49. Inubushi, K., Wada, H., and Takai, Y. (1984). Easily decomposable organic matter in paddy soil. Soil Science and Plant Nutrition, 30: 189-198.
  50. Wang, Q., Quensen, J. F., Fish, J. A., Kwon Lee, T., Sun, Y., Tiedje, J. M., and Cole, J. R. (2013). Ecological Patterns of nifH Genes in Four Terrestrial Climatic Zones Explored with Targeted Metagenomics Using FrameBot, a New Informatics Tool. mBio, 4: e00592-13.
  51. Watanabe, I., and Furusaka, C. (1980). Ecology of flooded rice fields. Advances in Microbial Ecology, 4: 125-168.
  52. Fetzer, S., and Conrad, R. (1993). Effect of redox potential on methanogenesis by Methanosarcina barkeri. Archives of Microbiology, 160: 108-113.
  53. Dannenberg, S., and Conrad, R. (1999). Effect of rice plants on methane production and rhizospheric metabolism in paddy soil. Bio-Geochem., 45: 53-71.
  54. Watanabe, A., Katoh, K., and Kimura, M. (1993). Effect of rice straw application on CH4 emission from paddy fields. Soil Science and Plant Nutrition, 39: 707-712.
  55. Yao, H., Conrad, R., Wassmann, R., and Neue, H. U. (1999). Effect of soil characteristics on sequential reduction and methane production in sixteen rice paddy soils from China, the Philippines, and Italy. Biogeochemistry, 47: 269-295.
  56. Kowalchuk, G., Buma, D. S., de Boer, W., Klinkhamer, P. G., and van Veen, J. A. (2002). Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek. Kluwer Academic Publishers, 81: 509-520.
  57. Scheid, D., Stubner, S., and Conrad, R. (2003). Effects of nitrate- and sulfate-amendment on the methanogenic populations in rice root incubations. FEMS Microbiology Ecology, 43: 309-315.
  58. Sun, L., Qiu, F., Zhang, X., Dai, X., Dong, X., and Song, W. (2008). Endophytic Bacterial Diversity in Rice (Oryza sativa L.) Roots Estimated by 16S rDNA Sequence Analysis. Microbial Ecology, 55: 415-424.
  59. Hu, B., Shen, L., Lian, X., Zhu, Q., Liu, S., Huang, Q., He, Y. (2014). Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. Proceedings of the National Academy of Sciences, 111: 4495-4500.
  60. Holmes, A. J., Costello, A., Lidstrom, M. E., and Murrell, J. C. (1995). Evidence that participate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiology Letters, 132: 203-208.
  61. Hale, M. G., and Moore, L. D. (1980). Factors affecting root exudation II: 1970-1978. Advances in Agronomy, 31: 93-124.
  62. Hoehler, T. M., Alperin, M. J., Albert, D. B., and Martens, C. S. (1994). Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen-sulfate reducer consortium. Global Biogeochemical Cycles, 8: 451-463.
  63. Conrad, R., and Frenzel, P. (2002). Flooded soils. In Encylopedia of Environmental Microbiology (pp. 1316-1333). Britton, G. (ed.). John Wiley & Sons, New York.
  64. Sessitsch, A., Hardoim, P. R., Döring, J., Weilharter, A., Krause, A., Woyke, T., Reinhold-Hurek, B. (2011). Functional Characteristics of an Endophyte Community Colonizing Rice Roots as Revealed by Metagenomic Analysis. Molecular Plant-Microbe Interactions, 25: 28-36.
  65. Erkel, C., Kube, M., Reinhardt, R., and Liesack, W. (2006). Genome of Rice Cluster I Archaea - the Key Methane Producers in the Rice Rhizosphere. Science, 313: 370-372.
  66. Roden, E. E. (2006). Geochemical and microbiological controls on dissimilatory iron reduction. Comptes Rendus Geoscience, 338: 456-467.
  67. Köhler, T., Dietrich, C., Scheffrahn, R. H., and Brune, A. (2012). High-Resolution Analysis of Gut Environment and Bacterial Microbiota Reveals Functional Compartmentation of the Gut in Wood-Feeding Higher Termites (Nasutitermes spp.). Appl. Environ. Microbiol., 78: 4691-4701.
  68. Madhaiyan, M., Peng, N., Te, N. S., Hsin I, C., Lin, C., Lin, F., Ji, L. (2013). Improvement of plant growth and seed yield in Jatropha curcas by a novel nitrogen-fixing root associated Enterobacter species. Biotechnology for Biofuels, 6: 140.
  69. Murty, M. G., and Ladha, J. K. (1988). Influence of Azospirillum inoculation on the mineral uptake and growth of rice under hydroponic conditions. Plant and Soil, 108: 281-285.
  70. Gilbert, B., Aßmus, B., Hartmann, A., and Frenzel, P. (1998). In situ localization of two methanotrophic strains in the rhizosphere of rice plants. FEMS Microbiology Ecology, 25: 117-128.
  71. Lu, Y., and Conrad, R. (2005). In Situ Stable Isotope Probing of Methanogenic Archaea in the Rice Rhizosphere. Science, 309: 1088-1090.
  72. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Weber, C. F. (2009). Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Applied and Environmental Microbiology, 75: 7537-7541.
  73. Nunan, N., Daniell, T. J., Singh, B. K., Papert, A., McNicol, J. W., and Prosser, J. I. (2005). Links between Plant and Rhizoplane Bacterial Communities in Grassland Soils, Characterized Using Molecular Techniques. Applied and Environmental Microbiology, 71: 6784-6792.
  74. Ratering, S., and Schnell, S. (2000). Localization of iron-reducing activity in paddy soilby profile studies. Biogeochemistry, 48: 341-365.
  75. Nouchi, I., Mariko, S., and Aoki, K. (1990). Mechanism of Methane Transport from the Rhizosphere to the Atmosphere through Rice Plants. Plant Physiol., 94: 59-66.
  76. Trotsenko, Y. A., and Murrell, J. C. (2008). Metabolic Aspects of Aerobic Obligate Methanotrophy. Advances in Applied Microbiology, 63: 183-229.
  77. Liu, Y., and Whitman, W. B. (2008). Metabolic, Phylogenetic, and Ecological Diversity of the Methanogenic Archaea. Annals of the New York Academy of Sciences, 1125: 171-189.
  78. Schellenberger, S., Kolb, S., and Drake, H. L. (2010). Metabolic responses of novel cellulolytic and saccharolytic agricultural soil Bacteria to oxygen. Environmental Microbiology, 12: 845-861.
  79. Handelsman, J. (2004). Metagenomics: Application of Genomics to Uncultured Microorganisms. Microbiology and Molecular Biology Reviews, 68: 669-685.
  80. Megonigal, J. P., and Guenther, A. B. (2008). Methane emissions from upland forest soils and vegetation. Tree Physiology, 28: 491-498.
  81. Joabsson, A., and Christensen, T. R. (2001). Methane emissions from wetlands and their relationship with vascular plants: an Arctic example. Global Change Biology, 7: 919-932.
  82. Kammann, C., Grünhage, L., Jäger, H. J., and Wachinger, G. (2001). Methane fluxes from differentially managed grassland study plots: the important role of CH4 oxidation in grassland with a high potential for CH4 production. Environmental Pollution, 115: 261-273.
  83. Jetten, M. S. M., Stams, A. J. M., and Zehnder, A. J. B. (1992). Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiology Reviews, 8: 181-197.
  84. Ikenaga, M., Asakawa, S., Muraoka, Y., and Kimura, M. (2004). Methanogenic archaeal communities in rice roots grown in flooded soil pots: estimation by PCR-DGGE and sequence analyses. Soil Science and Plant Nutrition, 50: 701-711.
  85. Hanson, R. S., and Hanson, T. E. (1996). Methanotrophic bacteria. Microbiological Reviews, 60: 439-471.
  86. Friedrich, M. W. (2005). Methyl-Coenzyme M Reductase Genes: Unique Functional Markers for Methanogenic and Anaerobic Methane-Oxidizing Archaea. Environmental Microbiology 397: 428-442).
  87. Kimura, M., Murakami, H., and Wada, H. (1988). Microbial colonization and decomposition processes in the rhizoplane. Soil Science and Plant Nutrition, 35: 63.
  88. Krüger, M., Frenzel, P., and Conrad, R. (2001). Microbial processes influencing methane emission from rice fields. Global Change Biology, 7:, 49-63.
  89. Roger, P. A., Zimmermann, W. J., and Lumpkin, T. A. (1993). Microbiological management of wetland rice fields. In Soil Microbial Ecology (pp. 417-455). Metting, B. (ed.). M. Dekker, New York.
  90. Liesack, W., Schnell, S., and Revsbech, N. P. (2000). Microbiology of flooded rice paddies. FEMS Microbiology Reviews, 24: 625-645.
  91. Costello, A. M., and Lidstrom, M. E. (1999). Molecular Characterization of Functional and Phylogenetic Genes from Natural Populations of Methanotrophs in Lake Sediments. Applied and Environmental Microbiology, 65: 5066-5074.
  92. McDonald, I. R., Bodrossy, L., Chen, Y., and Murrell, J. C. (2008). Molecular Ecology Techniques for the Study of Aerobic Methanotrophs. Applied and Environmental Microbiology, 74: 1305- 1315.
  93. Murtagh, F. (1985). Multidimensional clustering algorithms. Compstat Lectures, Vienna: Physika Verlag, 1985.
  94. McGarigal, K., Cushman, S. A., and Stafford, S. (2013). Multivariate statistics for wildlife and ecology research. Springer New York.
  95. Reddy, K. R., Patrick, W. H., and Lindau, C. W. (1989). Nitrification-denitrification at the plant rootsediment interface in wetlands. Limnology and Oceanography, 34: 1004-1013.
  96. Miller Jr, R. G. (1981). Nonparametric Techniques. In Simultaneous Statistical Inference (pp. 129- 188). Springer New York.
  97. Großkopf, R., Stubner, S., and Liesack, W. (1998b). Novel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Applied and Environmental Microbiology, 64: 4983-4989.
  98. Gray, N. D., Miskin, I. P., Kornilova, O., Curtis, T. P., and Head, I. M. (2002). Occurrence and activity of Archaea in aerated activated sludge wastewater treatment plants. Environmental Microbiology, 4: 158-168.
  99. Narihiro, T., and Sekiguchi, Y. (2011). Oligonucleotide primers, probes and molecular methods for the environmental monitoring of methanogenic archaea. Microbial Biotechnology, 4: 585-602.
  100. Hinsinger, P., Plassard, C., Tang, C., and Jaillard, B. (2003). Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant and Soil, 248: 43-59.
  101. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., (2013). Package “vegan.” Community Ecology Package, Version, 2.
  102. Yuan, Q., Pump, J., and Conrad, R. (2012). Partitioning of CH4 and CO2 Production Originating from Rice Straw, Soil and Root Organic Carbon in Rice Microcosms. PLoS ONE, 7: e49073.
  103. Steinberg, L. M., and Regan, J. M. (2008). Phylogenetic Comparison of the Methanogenic Communities from an Acidic, Oligotrophic Fen and an Anaerobic Digester Treating Municipal Wastewater Sludge. Applied and Environmental Microbiology, 74: 6663-6671.
  104. McMurdie, P. J., and Holmes, S. (2013). phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS One, 8: e61217.
  105. Hedderich, R., and Whitman, W. B. (2006). Physiology and Biochemistry of the Methane-Producing Archaea. In The Prokaryotes: Volume 2: Ecophysiology and Biochemistry (pp. 1050-1079). M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt (ed.). Springer New York.
  106. Frenzel, P. (2000). Plant-Associated Methane Oxidation in Rice Fields and Wetlands. In Advances in Microbial Ecology (pp. 85-114). B. Schink (ed.). Springer, Boston.
  107. Flessa, H., and Fischer, W. R. (1992). Plant-induced changes in the redox potentials of rice rhizospheres. Plant and Soil, 143: 55-60.
  108. Rovira, A. D. (1969). Plant root exudates. The Botanical Review, 35: 35-57.
  109. Xie, C.-H., and Yokota, A. (2005b). Pleomorphomonas oryzae gen. nov., sp. nov., a nitrogen-fixing bacterium isolated from paddy soil of Oryza sativa. International Journal of Systematic and Evolutionary Microbiology, 55: 1233-1237.
  110. Whiting, G. J., and Chanton, J. P. (1993). Primary production control of methane emission from wetlands. Nature, 364: 794-795.
  111. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22: 2688-2690.
  112. Yuan, Y., Conrad, R., and Lu, Y. (2009). Responses of methanogenic archaeal community to oxygen exposure in rice field soil. Environmental Microbiology Reports, 1: 347-354.
  113. Nguyen, C. (2003). Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie, 23: 375-396.
  114. Manoharachary, C., and Mukerji, K. G. (2006). Rhizosphere Biology - an Overview. In Soil Biology Microbial Activity in the Rhizoshere (pp. 1-15). Mukerji, K. G., Manoharachary, C. and Singh, J. (ed.). Springer Berlin Heidelberg.
  115. Saarnio, S., Wittenmayer, L., and Merbach, W. (2004). Rhizospheric exudation of Eriophorum vaginatum L. - Potential link to methanogenesis. Plant and Soil, 267: 343-355.
  116. Gilbert, B., and Frenzel, P. (1998). Rice roots and CH4 oxidation: the activity of bacteria, their distribution and the microenvironment. Soil Biology and Biochemistry, 30: 1903-1916.
  117. Frenzel, P., Bosse, U., and Janssen, P. H. (1999). Rice roots and methanogenesis in a paddy soil: ferric iron as an alternative electron acceptor in the rooted soil. Soil Biology and Biochemistry, 31: 421-430.
  118. Curl, E. A., and Truelove, B. (1986). Root Exudates. In The Rhizosphere (pp. 55-92). Curl, E. A. and Truelove, B. (ed.). Springer Berlin Heidelberg.
  119. Lin, M., and You, C. (1989). Root exudates of rice (Oryza sativa L.) and its interaction with Alcaligenes faecalis. Scientia Agricultura Sinicia, 22: 6-12.
  120. Jenny, H., and Grossenbacher, K. (1963). Root-Soil Boundary Zones as Seen in the Electron Microscope1. Soil Science Society of America Journal, 27: 273-277.
  121. Gregory, P. J. (2006). Roots, rhizosphere and soil: the route to a better understanding of soil science? European Journal of Soil Science, 57: 2-12.
  122. van der Heijden, M. G. A., and Schlaeppi, K. (2015). Root surface as a frontier for plant microbiome research. Proceedings of the National Academy of Sciences, 112: 2299-2300.
  123. Hoshikawa, K., Matsuo, T., and Center, P. R. (1993). Science of the Rice Plant, vol 1: Morphology. Nobunkyo, Tokyo, 133-186.
  124. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26: 2460-2461.
  125. Graystone, S. J., Wang, S., Campbell, C. D., and Edwards, A. C. (1998). Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol.Biochem., 30: 369-378.
  126. Conrad, R., and Klose, M. (2000). Selective inhibition of reactions involved in methanogenesis and fatty acid production on rice roots. FEMS Microbiology Ecology, 34: 27-34.
  127. Fetzer, S., Bak, F., and Conrad, R. (1993). Sensitivity of methanogenic bacteria from paddy soil to oxygen and desiccation. FEMS Microbiology Ecology, 12: 107-115.
  128. Heinz, E., Kraft, P., Buchen, C., Frede, H. G., Aquino, E., and Breuer, L. (2013). Set Up of an Automatic Water Quality Sampling System in Irrigation Agriculture. Sensors, 14: 212-228.
  129. Girvan, M. S., Bullimore, J., Pretty, J. N., Osborn, A. M., and Ball, A. S. (2003). Soil Type Is the Primary Determinant of the Composition of the Total and Active Bacterial Communities in Arable Soils. Applied and Environmental Microbiology, 69: 1800-1809.
  130. Conrad, R., Klose, M., Noll, M., Kemnitz, D., and Bodelier, P. (2008). Soil type links microbial colonization of rice roots to methane emission. Global Change Biology, 14: 657-669.
  131. Kraffczyk, I., Trolldenier, G., and Beringer, H. (1984). Soluble root exudates of maize: Influence of potassium supply and rhizosphere microorganisms. Soil Biology and Biochemistry, 16: 315- 322.
  132. Lüdemann, H., Arth, I., and Liesack, W. (2000). Spatial Changes in the Bacterial Community Structure along a Vertical Oxygen Gradient in Flooded Paddy Soil Cores. Applied and Environmental Microbiology, 66: 754-762.
  133. Dufrene, M., and Legendre, P. (1997). Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs, 67: 345-366.
  134. Tan, Z., Hurek, T., Vinuesa, P., Müller, P., Ladha, J. K., and Reinhold-Hurek, B. (2001). Specific Detection of Bradyrhizobium andRhizobium Strains Colonizing Rice (Oryza sativa) Roots by 16S-23S Ribosomal DNA Intergenic Spacer-Targeted PCR. Applied and Environmental Microbiology, 67: 3655-3664.
  135. Treude, N., Rosencrantz, D., Liesack, W., and Schnell, S. (2003). Strain FAc12, a dissimilatory iron-reducing member of the Anaeromyxobacter subgroup of Myxococcales. FEMS Microbiology Ecology, 44: 261-269.
  136. Yuan, Q., Pump, J., and Conrad, R. (2014). Straw application in paddy soil enhances methane production also from other carbon sources. Biogeosciences, 11: 237-246.
  137. Lu, Y., Rosencrantz, D., Liesack, W., and Conrad, R. (2006). Structure and activity of bacterial community inhabiting rice roots and the rhizosphere. Environmental Microbiology, 8: 1351- 1360.
  138. Edwards, J., Johnson, C., Santos-Medellín, C., Lurie, E., Podishetty, N. K., Bhatnagar, S., Sundaresan, V. (2015). Structure, variation, and assembly of the root-associated microbiomes of rice. Proceedings of the National Academy of Sciences of the United States of America, 112: 911-920.
  139. Noll, M., Matthies, D., Frenzel, P., Derakshani, M., and Liesack, W. (2005). Succession of bacterial community structure and diversity in a paddy soil oxygen gradient. Environmental Microbiology, 7: 382-395.
  140. Schink, B., and Stams, A. J. M. (2013). Syntrophism Among Prokaryotes. In The Prokaryotes: Prokaryotic Communities and Ecophysiology (pp. 471-493). Rosenberg, E., DeLong, E. F., Lory, S., Stackebrandt, E. and Thompson, F. (ed.). Springer Berlin Heidelberg.
  141. Yang, S., Liebner, S., Alawi, M., Ebenhöh, O., and Wagner, D. (2014). Taxonomic database and cut-off value for processing mcrA gene 454 pyrosequencing data by MOTHUR. Journal of Microbiological Methods, 103: 3-5.
  142. Ponnamperuma, F. N. (1972). The Chemistry of Submerged Soils. Advances in Agronomy, 24: 29- 96.
  143. Dietrich, C., Köhler, T., and Brune, A. (2014). The Cockroach Origin of the Termite Gut Microbiota: Patterns in Bacterial Community Structure Reflect Major Evolutionary Events. Applied and Environmental Microbiology, 80: 2261-2269.
  144. Fierer, N., and Jackson, R. B. (2006). The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America, 103: 626-631.
  145. Ström, L., Ekberg, A., Mastepanov, M., and Røjle Christensen, T. (2003). The effect of vascular plants on carbon turnover and methane emissions from a tundra wetland. Global Change Biology, 9: 1185-1192.
  146. Sakai, S., Conrad, R., and Imachi, H. (2014). The Family Methanocellaceae. In The Prokaryotes: Other Major Lineages of Bacteria and The Archaea (pp. 209-214). Rosenberg, E., DeLong, E. F., Lory, S., Stackebrandt, E. and Thompson, F. (ed.). Springer Berlin Heidelberg.
  147. Prinn, R. G. (1994). The Interactive Atmosphere: Global Atmospheric-Biospheric Chemistry. Ambio, 23: 50-61.
  148. Fujii, Y. (1974). The morphology and physiology of rice roots. Technical Bulletin - Asian and Pacific Council. 20:17.
  149. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature, 444: 323-329.
  150. Good, I. J. (1953). The population frequencies of spiecies and the estimation of population parameters. Biometrika, 40: 237-264.
  151. Raaijmakers, J. M., Paulitz, T. C., Steinberg, C., Alabouvette, C., and Moenne-Loccoz, Y. (2009). The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil Plant and Soil, 321: 341-361.
  152. Pinton, R., Varanini, Z., and Nannipieri, P. (2001). The Rhizosphere as a Site of Biochemical Interactions Among Soil Components, Plants and Microoorganisms. In The Rhizosphere: Biochemistry, and Organic Substances at the Soil Interface (pp. 1-17). Pinton, R., Varanini, Z. and Nannipieri, P. (ed.). Marcel Dekker Incorporation, New York.
  153. Yoshida, S., S., H. (1982). The rice root system: Its development and function. In Drought resistance in crops with emphasis on rice (pp. 97-114). Los Banos, Laguna, Philippines.
  154. Greaves, M. P., and Darbyshire, J. F. (1972). The ultrastructure of the mucilaginous layer on plant roots. Soil Biology and Biochemistry, 4: 443-449.
  155. Hoagland, D., and Arnon, D. I. (1950). The water-culture method for growing plants without soil. Circular.California Agricultural Experiment Station, 347: 1-32.
  156. Ge, T., Liu, C., Yuan, H., Zhao, Z., Wu, X., Zhu, Z. Wu, J. (2015). Tracking the photosynthesized carbon input into soil organic carbon pools in a rice soil fertilized with nitrogen. Plant and Soil, 392: 17-25.
  157. Krylova, N. I., Janssen, P. H., and Conrad, R. (1997). Turnover of propionate in methanogenic paddy soil. FEMS Microbiology Ecology, 23: 107-117.
  158. Edgar, R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10: 996-998.
  159. Wu, W. X., Liu, W., Lu, H. H., Chen, Y. X., Devare, M., and Thies, J. (2009). Use of 13C labeling to assess carbon partitioning in transgenic and nontransgenic (parental) rice and their rhizosphere soil microbial communities. FEMS Microbiology Ecology, 67: 93-102.


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