Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice

ISME Journal

Volumn 6, Issue 7, 2012, Pages 1378-1390

  Knief, Claudia ^a   Delmotte, Nathanaël ^a   Chaffron, Samuel ^b   Stark, Manuel ^b   Innerebner, Gerd ^a   Wassmann, Reiner ^c,d   Von Mering, Christian ^b   Vorholt, Julia A ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

^d KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

metaproteogenomics; microbial community; Oryza sativa; phyllosphere; rhizosphere; rice

Indexed keywords

CARBON; METHANOL; PROTEOME;

CULTIVAR; DATA SET; ENZYME ACTIVITY; GENOMICS; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; PHYLLOSPHERE; PHYSIOLOGY; PROKARYOTE; PROTEIN; RHIZOSPHERE; RICE;

ARCHAEON; ARTICLE; BACTERIUM; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; METAGENOME; METHYLOBACTERIUM; MICROBIOLOGY; RHIZOSPHERE; RICE;

ARCHAEA; BACTERIA; CARBON; METAGENOME; METHANOL; METHYLOBACTERIUM; ORYZA SATIVA; PROTEOME; RHIZOSPHERE;

ARCHAEA; BACTERIA (MICROORGANISMS); METHYLOBACTERIUM; ORYZA SATIVA;

EID: 84862590329     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2011.192     Document Type: Article

References (62)

1. Anesti V, McDonald IR, Ramaswamy M, Wade WG, Kelly DP, Wood AP. (2005). Isolation and molecular detection of methylotrophic bacteria occurring in the human mouth. Environ Microbiol 7: 1227-1238. (Pubitemid 41026523)
2. Anthony C, Williams P. (2003). The structure and mechanism of methanol dehydrogenase. BBA - Proteins Proteom 1647: 18-23. (Pubitemid 38234627)
3. Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C. (2005). Microbial co-operation in the rhizosphere. J Exp Bot 56: 1761-1778. (Pubitemid 40907140)
4. Bastida F, Moreno JL, Nicolas C, Hernandez T, Garcia C. (2009). Soil metaproteomics: A review of an emerging environmental science. Significance, methodology and perspectives. Eur J Soil Sci 60: 845-859.
5. Beattie GA. (2006). Plant-Associated bacteria: Survey, molecular phylogeny, genomics and recent advances. In: Gnanamanickam SS (ed). Plant-Associated bacteria. Springer: Dordrecht, pp 1-56.
6. Bodelier PL, Roslev P, Henckel T, Frenzel P. (2000). Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature 403: 421-424. (Pubitemid 30073089)
7. Bosse U, Frenzel P. (1997). Activity and distribution of methane-oxidizing bacteria in flooded rice soil microcosms and in rice plants (Oryza sativa). Appl Environ Microbiol 63: 1199-1207.
8. Brune A, Frenzel P, Cypionka H. (2000). Life at the oxicanoxic interface: Microbial activities and adaptations. FEMS Microbiol Rev 24: 691-710.
9. Chinnadurai C, Balachandar D, Sundaram SP. (2009). Characterization of 1-Aminocyclopropane-1-carboxylate deaminase producing methylobacteria from phyllosphere of rice and their role in ethylene regulation. World J Microb Biot 25: 1403-1411.
10. Conrad R. (2007). Microbial ecology of methanogens and methanotrophs. Adv Agron 96: 1-63.
11. De Costa DM, Samarasinghe SST, Dias HRD, Dissanayake DMN. (2008). Control of rice sheath blight by phyllosphere epiphytic microbial antagonists. Phytoparasitica 36: 52-65. (Pubitemid 351220220)
12. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R et al. (2009). Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl. Acad. Sci. USA 106: 16428-16433.
13. Derridj S. (1996). Nutrients on the leaf surface. In: Morris CE, Nicot PC, Nguyen-The C (eds). Aerial plant surface microbiology. Plenum Press: New York, pp 25-42.
14. Elbeltagy A, Ando Y. (2008). Expression of nitrogenase gene (NIFH) in roots and stems of rice, Oryza sativa, by endophytic nitrogen-fixing communities. Afr J Biotechnol 7: 1950-1957. (Pubitemid 351919144)
15. Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T et al. (2001). Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 67: 5285-5293. (Pubitemid 33701301)
16. Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato YI, Morisaki H et al. (2000). Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci. Plant. Nutr. 46: 617-629.
17. Eller G, Frenzel P. (2001). Changes in activity and community structure of methane-oxidizing bacteria over the growth period of rice. Appl Environ Microbiol 67: 2395-2403. (Pubitemid 33639706)
18. Frenzel P. (2000). Plant-Associated methane oxidation in rice fields and wetlands. Adv Microb Ecol 16: 85-114.
19. Fürnkranz M, Wanek W, Richter A, Abell G, Rasche F, Sessitsch A. (2008). Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2: 561-570. (Pubitemid 351666975)
20. Hagemeier CH, KrüerM, Thauer RK,Warkentin E, Ermler U. (2006). Insight into the mechanism of biological methanol activation based on the crystal structure of methanol:cobalamin methyltransferase complex MtaBC from Methanosarcina barkeri. Proc. Natl. Acad. Sci. USA 103: 18917-18922. (Pubitemid 350002803)
21. Hakemian AS, Rosenzweig AC. (2007). The biochemistry of methane oxidation. Annu Rev Biochem 76: 223-241.
22. Hanson RS, Hanson TE. (1996). Methanotrophic bacteria. Microbiol Rev 60: 439-471. (Pubitemid 26170914)
23. Hao WY, Ren LX, Ran W, Shen QR. (2010). Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f.sp. niveum. Plant Soil 336: 485-497.
24. Horz HP, Yimga MT, Liesack W. (2001). Detection of methanotroph diversity on roots of submerged rice plants by molecular retrieval of pmoA, mmoX, mxaF, and 16S rRNA and ribosomal DNA, including pmoAbased terminal restriction fragment length polymorphism profiling. Appl Environ Microbiol 67: 4177-4185. (Pubitemid 33641714)
25. Kalyuzhnaya MG, Hristova KR, Lidstrom ME, Chistoserdova L. (2008). Characterization of a novel methanol dehydrogenase in representatives of Burkholderiales: Implications for environmental detection of methylotrophy and evidence for convergent evolution. J Bacteriol 190: 3817-3823. (Pubitemid 351732860)
26. Keppler F, Boros M, Frankenberg C, Lelieveld J, McLeod A, PirttiläAM et al. (2009). Methane formation in aerobic environments. Environ Chem 6: 459-465.
27. Kim MC, Ahn JH, Shin HC, Kim T, Ryu TH, Kim DH et al. (2008). Molecular analysis of bacterial community structures in paddy soils for environmental risk assessment with two varieties of genetically modified rice, Iksan 483 and Milyang 204. J Microbiol Biotechnol 18: 207-218.
28. Knief C, Dunfield PF. (2005). Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environ Microbiol 7: 1307-1317. (Pubitemid 41204925)
29. Knief C, Delmotte N, Vorholt JA. (2011). Bacterial adaptation to life in assoication with plants-A proteomics perspective from culture to in situ conditions. Proteomics 11: 3086-3105.
30. Knief C, Vanitchung S, Harvey NW, Conrad R, Dunfield PF, Chidthaisong A. (2005). Diversity of methanotrophic bacteria in tropical upland soils under different land uses. Appl Environ Microbiol 71: 3826-3831. (Pubitemid 40980552)
31. Kowalchuk GA, Yergeau E, Leveau JHJ, Sessitsch A, Bailey M. (2010). Plant-Associated microbial communities. In: Liu W-T, Jansson JK (eds). Environmental molecular microbiology. Caister Academic Press, pp 131-148.
32. Krüger M, Frenzel P, Conrad R. (2001). Microbial processes influencing methane emission from rice fields. Global Change Biol 7: 49-63. (Pubitemid 34262232)
33. Ladha JK, Reddy PM. (2000). The quest for nitrogen fixation in rice. International Rice Research Institute: Los Baños, Philippines.
34. Liesack W, Schnell S, Revsbech NP. (2000). Microbiology of flooded rice paddies. FEMS Microbiol Rev 24: 625-645.
35. Lu Y, Rosencrantz D, Liesack W, Conrad R. (2006). Structure and activity of bacterial community inhabiting rice roots and the rhizosphere. Environ Microbiol 8: 1351-1360. (Pubitemid 44025329)
36. Lueders T, Friedrich MW. (2002). Effects of amendment with ferrihydrite and gypsum on the structure and activity of methanogenic populations in rice field soil. Appl Environ Microbiol 68: 2484-2494. (Pubitemid 34477848)
37. Madhaiyan M, Poonguzhali S, Kwon SW, Sa TM. (2009). Methylobacterium phyllosphaerae sp. nov., a pink-pigmented, facultative methylotroph from the phyllosphere of rice. Int J Syst Evol Microbiol 59: 22-27.
38. Madhaiyan M, Poonguzhali S, Sa T. (2007). Influence of plant species and environmental conditions on epiphytic and endophytic pink-pigmented facultative methylotrophic bacterial populations associated with field-grown rice cultivars. J Microbiol Biotechnol 17: 1645-1654. (Pubitemid 350090343)
39. Madhaiyan M, Poonguzhali S, SenthilkumarM, Seshadri S, Chung HY, Yang JC et al. (2004). Growth promotion and induction of systemic resistance in rice cultivar Co-47 (Oryza sativa L) by Methylobacterium spp. Bot Bull Acad Sin 45: 315-324. (Pubitemid 39547716)
40. Maliti CM, Basile DV, Corpe WA. (2005). Effects of Methylobacterium spp. strains on rice Oryza sativa L. callus induction, plantlet regeneration, and seedlings growth in vitro. J Torrey Bot Soc 132: 355-367. (Pubitemid 41339218)
41. Mano H, Tanaka F, Nakamura C, Kaga H, Morisaki H. (2007). Culturable endophytic bacterial flora of the maturing leaves and roots of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 22: 175-185.
42. Nakatsu CH, Hristova K, Hanada S, Meng XY, Hanson JR, Scow KM et al. (2006). Methylibium petroleiphilum gen. nov., sp. nov., a novel methyl tert-butyl etherdegrading methylotroph of the Betaproteobacteria. Int J Syst Evol Microbiol 56: 983-989. (Pubitemid 43820821)
43. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. (2003). A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646-4658. (Pubitemid 37082259)
44. Pedraza RO, Bellone CH, de Bellone S, Sorte PMB, Teixeira KRD. (2009). Azospirillum inoculation and nitrogen fertilization effect on grain yield and on the diversity of endophytic bacteria in the phyllosphere of rice rainfed crop. Eur J Soil Biol 45: 36-43.
45. Prakamhang J, Minamisawa K, Teamtaisong K, Boonkerd N, Teaumroong N. (2009). The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L). Appl Soil Ecol 42: 141-149.
46. Prasanna R, Nain L, Pandey AK, Nayak S. (2010). Exploring the ecological significance of microbial diversity and networking in the rice ecosystem. In: Dion P (ed). Soil biology and agriculture in the tropics. Springer Berlin Heidelberg, pp 139-161.
47. Schmidt S, Christen P, Kiefer P, Vorholt JA. (2010). Functional investigation of methanol dehydrogenaselike protein XoxF in Methylobacterium extorquens AM1. Microbiology 156: 2575-2586.
48. Shrestha M, Abraham WR, Shrestha PM, NollM, Conrad R. (2008). Activity and composition of methanotrophic bacterial communities in planted rice soil studied by flux measurements, analyses of pmoA gene and stable isotope probing of phospholipid fatty acids. Environ Microbiol 10: 400-412.
49. Shrestha PM, Kube M, Reinhardt R, Liesack W. (2009). Transcriptional activity of paddy soil bacterial communities. Environ Microbiol 11: 960-970.
50. Stark M, Berger SA, Stamatakis A, von Mering C. (2010). MLTreeMap - Accurate Maximum Likelihood placement of environmental DNA sequences into taxonomic and functional reference phylogenies. BMC Genomics 11: 461.
51. Suzuki R, Shimodaira H. (2006). Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22: 1540-1542. (Pubitemid 43985330)
52. Sy A, Timmers AC, Knief C, Vorholt JA. (2005). Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl Environ Microbiol 71: 7245-7252. (Pubitemid 43194218)
53. Thauer RK. (1998). Biochemistry of methanogenesis: A tribute to Marjory Stephenson. Microbiology 144: 2377-2406.
54. von Ophem PW, van Beeumen J, Duine JA. (1993). Nicotinoprotein [NAD(P)-containing] alcohol/aldehyde oxidoreductases. Purification and characterization of a novel type from Amycolatopsis methanolica. Eur J Biochem 212: 819-826. (Pubitemid 23091730)
55. Vorholt JA, Marx CJ, Lidstrom ME, Thauer RK. (2000). Novel formaldehyde-Activating enzyme in Methylobacterium extorquens AM1 required for growth on methanol. J Bacteriol 182: 6645-6650. (Pubitemid 32249245)
56. Wang HB, Zhang ZX, Li H, He HB, Fang CX, Zhang AJ et al. (2011). Characterization of metaproteomics in crop rhizospheric soil. J Proteome Res 10: 932-940.
57. Wassmann R, Aulakh MS. (2000). The role of rice plants in regulating mechanisms of methane missions. Biol Fertil Soils 31: 20-29. (Pubitemid 30218062)
58. Watanabe I, Hashimoto T, Shimoyama A. (1997). Methaneoxidizing activities and methanotrophic populations associated with wetland rice plants. Biol Fertil Soils 24: 261-265. (Pubitemid 27167697)
59. Wu LK, Wang HB, Zhang ZX, Lin R, Zhang ZY, Lin WX. (2011). Comparative metaproteomic analysis on consecutively Rehmannia glutinosa-monocultured rhizosphere soil. Plos One 6: E20611.
60. Wu LQ, Ma K, Lu YH. (2009). Rice roots select for type I methanotrophs in rice field soil. Syst Appl Microbiol 32: 421-428.
61. Yang JH, Liu HX, Zhu GM, Pan YL, Xu LP, Guo JH. (2008). Diversity analysis of antagonists from rice-Associated bacteria and their application in biocontrol of rice diseases. J Appl Microbiol 104: 91-104.
62. Zhu W, Reich CI, Olsen GJ, Giometti CS, Yates III JR. (2004). Shotgun proteomics of Methanococcus jannaschii and insights into methanogenesis. J Proteome Res 3: 538-548.(Pubitemid 39207358)