Low nitrogen fertilization adapts rice root Microbiome to low nutrient environment by changing biogeochemical functions

Microbes and Environments

Volumn 29, Issue 1, 2014, Pages 50-59

  Ikeda, Seishi ^a,b   Sasaki, Kazuhiro ^a   Okubo, Takashi ^a   Yamashita, Akifumu ^a   Terasawa, Kimihiro ^a   Bao, Zhihua ^a   Liu, Dongyan ^c   Watanabe, Takeshi ^c   Murase, Jun ^c   Asakawa, Susumu ^c   Eda, Shima ^a   Mitsui, Hisayuki ^a   Sato, Tadashi ^a   Minamisawa, Kiwamu ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b NATIONAL AGRICULTURAL RESEARCH CENTER FOR HOKKAIDO REGION   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

Metagenome analysis; Methane cycle; Nitrogen fertilizer; Rice paddy field; Root microbiome

Indexed keywords

FERTILIZER; NITROGEN;

ARCHAEON; ARTICLE; BACTERIUM; BIODIVERSITY; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MICROFLORA; MOLECULAR GENETICS; PHYLOGENY; PLANT ROOT; RICE;

ARCHAEA; BACTERIA; BIODIVERSITY; FERTILIZERS; MICROBIOTA; MOLECULAR SEQUENCE DATA; NITROGEN; ORYZA SATIVA; PHYLOGENY; PLANT ROOTS; SOIL MICROBIOLOGY;

EID: 84898741297     PISSN: 13426311     EISSN: 13474405     Source Type: Journal    
DOI: 10.1264/jsme2.ME13110     Document Type: Article

References (50)

1. Banger, K., H. Tian, and C. Lu. 2012. Do nitrogen fertilizers stimulate or inhibit methane emissions from rice fields? Global Change Biol. 18:3257-3267.
2. Barraquio, W.L., M.L.G. Daroy, A.C. Tirol, J.K. Ladha, and I. Watanabe. 1986. Laboratory acetylene reduction assay for relative measurement of N2-fxing activities associated with field-grown wetland rice plants. Plant Soil 90:357-372.
3. Blaha, D., C. Prigent-Combaret, S. Mirza, and Y. Moenne-Loccoz. 2006. Phylogeny of the 1-aminocyclopropane-1-carbxylic acid deaminase-encoding gene acdS in phytobenefcial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol. Ecol. 56:455-470.
4. Bodelier, P.E.L. 2011. Interactions between nitrogenous fertilizers and methane cycling in wetland and upland soils. Curr. Opin. Environ. Sustain. 3:379-388.
5. Bodelier, P.L.E., P. Roslev, T. Henckel, and P. Frenzel. 2000. Stimulation by ammonium-based fertilizer of methane oxidation in soil around rice roots. Nature 403:421-424.
6. Chaintreuil, C., E. Giraud, Y. Prin, J. Lorquin, A. Ba, M. Gillis, P. de Lajudie, and B. Dreyfus. 2000. Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl. Environ. Microbiol. 66:5437-5447.
7. Conrad, R. 2007. Microbial ecology of methanogens and methano-trophs. Adv. Agron. 96:1-63.
8. Cornells, P. 2011. Iron uptake and metabolism in pseudomonads. Appl. Microbiol. Biotechnol. 86:1637-1645.
9. Costello, A.M., and M.E. Lidstrom. 1999. Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl. Environ. Microbiol. 65:5066- 5074.
10. Dianou, D., C. Ueno, T. Ogiso, M. Kimura, and S. Asakawa. 2012. Diversity of cultivable methane-oxidizing bacteria in microsites of rice paddy field: Investigation by cultivation method and fuorescence in site hybridization (FISH). Microbes Environ. 27:278-287.
11. Galloway, J.N., A.R. Townsend, J.W. Erisman, M. Bekunda, Z. Cai, J.R. Freney, L.A. Martinelli, S.P. Seitzinger, and M.A. Sutton. 2008. Transformation of the nitrogen cycle: Recent trends, questions, and potential solution. Science 320:889-892.
12. Giraud, E., L. Moulin, D. Vallenet, et al. 2007. Legume symbioses: Absence of Nod genes in photosynthetic bradyrhizobia. Science 316:1307-1312.
13. Hamady, M., C. Lozupone, and R. Knight. 2009. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 4:17-27.
14. Hardoim, P.R., F.D. Andreote, B. Reinhold-Hurek, A. Sessitish, L.S. van Overbeek, and J.D. van Elsas. 2011. Rice root-associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol. Ecol. 77:154-164.
15. Holmes, A.J., A. Costello, M.E. Lindstrom, and J.C. Murrell. 1995. Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol. Lett. 132:203-208.
16. Ikeda, S., M. Anda, S. Inaba, et al. 2011. Autoregulation of nodulation interferes with impact of nitrogen fertilization levels on the leaf-associated bacterial community in soybeans. Appl. Environ. Microbiol. 77:1973-1980.
17. Ikeda, S., K.N. Watanabe, K. Minamisawa, and N. Ytow. 2004. Evaluation of soil DNAs from arable lands in Japan with a modifed direct extraction method. Microbes Environ. 19:301-309.
18. Ikeda, S., T. Kaneko, T. Okubo, et al. 2009. Development of a bacterial cell enrichment method and its application to the community analysis in soybean stems. Microbiol. Ecol. 58:703-714.
19. Ikeda, S., T. Okubo, M. Anda, et al. 2010. Community- and genome-based views of plant-associated bacteria: Plant-bacterial interactions in soybean and rice. Plant Cell Physiol. 51:1398-1410.
20. Ikeda, S., T. Okubo, T. Kaneko, et al. 2010. Community shifts of soybean-associated bacteria responding to different nodulation phenotypes and N levels. ISME J. 4:315-326.
21. Ishii, S., S. Ikeda, K. Minamisawa, and K. Senoo. 2011. Nitrogen cycling in rice paddy environments: Past achievements and future challenges. Microbes Environ. 26:282-292.
22. Ju, X.T., G.X. Xing, X.P. Chen, et al. 2009. Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc. Natl. Acad. Sci. U.S.A. 106:3041-3046.
23. Kertesz, M.A., E. Fellows, and A. Schmalenberger. 2007. Rhizobacteria and plant sulfur supply. p. 239-259. In Advances in Applied Microbiology, Vol 62. Elsevier, San Francisco.
24. Knief, C., N. Delmotte, S. Chaffron, M. Stark, G. Innerebner, R. Wassmann, C. von Mering, and J.A. Vorholt. 2011. Meta-proteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. IMSE J. 6:1378-1390.
25. Kogel-Knabner, I., W. Amelung, Z. Cao, S. Fiedler, P. Franzel, R. Jahn, K. Kalbitz, A. Kolbl, and M. Schloter. 2010. Biogeochemistry of paddy soils. Geoderma 157:1-14.
26. Kolb, S., C. Knief, S. Stubner, and R. Conrad. 2003. Quantitative detection of methanotrophs in soil by novel pmoA-targeted real-time PCR assays. Appl. Environ. Microbiol. 69:2423-2429.
27. Lehmann-Richter, S., R. Grosskopf, W. Liesack, P. Frenzel, and R. Conrad. 1999. Methanogenic archaea and CO2-dependent methano-genesis on washed rice roots. Environ. Microbiol. 1:159-166.
28. Liesack, W., S. Schnell, and N.P. Revsbech. 2000. Microbiology of fooded rice paddies. FEMS Microbiol. Rev. 24:625-645.
29. Lozupone, C.A., and R. Knight. 2007. Global patterns in bacterial diversity. Proc. Natl. Acad. Sci. U.S.A. 103:11436-11440.
30. Luton, P.E., J.M. Wayane, R.J. Sharp, and P.A. Riley. 2002. The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfll. Microbiology 148:3521-3530.
31. Masuda, S., S. Eda, S. Ikeda, H. Mitsui, and K. Minamisawa. 2010. Thiosulfate-dependent chemolithoautotrophic growth of Bradyrhizobium japonicum. Appl. Environ. Microbiol. 76:2402- 2409.
32. Mattos, K.A., V.L.M. Padue, A. Romeiro, et al. 2008. Endophytic colonization of rice (Oryza sativa L.) by the diazotrophic bacterium Burkholderia kururiensis and its ability to enhance plant growth. An. Acad. Bras. Cienc. 80:477-493.
33. Mayumi, D., T. Yoshimoto, H. Uchiyama, N. Nomura, and T. Nakajima-Kambe. 2010. Seasonal change in methanotrophic diversity and populations in a rice field soil assessed by DNA-stable isotope probing and quantitative real-time PCR. Microbes Environ. 25:156-163.
34. Mendes, R., M. Kruijt, I. de Bruijn, et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097-1100.
35. Meyer, F., D. Parrmann, and M. D'Souza, 2008. The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386.
36. Molina, M.A., P. Godoy, M.I. Ramos-Gonzales, N. Munoz, J.L. Ramos, and M. Espinosa-Urgel. 2005. Role of iron and the TonB system in colonization of core seeds and roots by Pseudomonas putida KT2440. Environ. Microbiol. 7:443-449.
37. Mulvaney, R.L., S.A. Khan, and T.R. Ellsworth. 2009. Synthetic nitrogen fertilizers deplete soil nitrogen: A global dilemma for sustainable cereal production. J. Environ. Qual. 38:2295-2314.
38. Murrell, J.C., and S.M. Jetten. 2009. The microbial methane cycle. Environ. Microbiol. Rep. 1:279-284.
39. Onofre-Lemus, J., I. Hernandes-Lucas, L. Girard, and J. Caballero-Mellado. 2009. ACC (1-aminocyclopropane-1carboxylate) deaminase activity, a widespread trait in Burkholderia species, and its growth-promoting effect on tomato plants. Appl. Environ. Microbiol. 75:6581-6590.
40. Sakai, S., H. Imachi, S. Hanada, A. Ohashi, H. Harada, and Y. Kamagata. 2008. Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the frst isolate of the lineage 'Rice Cluster I', and proposal of the new archaeal order Methanocellales ord. nov. Int. J. Syst. Evol. Microbiol. 58:929-936.
41. Sakai, S., H. Imachi, Y. Sekiguchi, A. Ohashi, H. Harada, and Y. Kamagata. 2007. Isolation of key methanogens for global methane emission from rice paddy fields: a novel isolate affliated with the clone cluster rice cluster I. Appl. Environ. Microbiol. 73:4326-4331.
42. Sawada, H., L.D. Kuykendall, and J.M. Young. 2003. Changing concepts in the systematics of bacterial nitrogen-fxing legume symbi-onts. J. Gen. Appl. Microbiol. 49:155-179.
43. Sessitsch, A., P. Hardoim, J. Döring, et al. 2012. Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenome analysis. Mol. Plant-Microbe. Interact. 25:28-36.
44. Shrestha, M., P.M. Shrestha, P. Frenzel, and R. Conrad. 2010. Effect of nitrogen fertilization on methane oxidation, abundance, community structure, and gene expression of methanotrophs in the rice rhizo-sphere. ISME J. 4:1545-1556.
45. Sugawara, M., G.R. Shah, M.J. Sadowsky, O. Paliy, J. Speck, A.W. Vail, and P. Gyaneshwar. 2011. Expression and functional roles of Bradryrhizobium japonicum genes involved in the utilization of inorganic and organic sulfur compounds in free-living and symbiotic conditions. Mol. Plant-Microbe. Interact. 24:451-457.
46. Trevisan, S., O. Francioso, S. Quaggiotti, and S. Nardi. 2010. Humic substances biological activity at the plant-soil interface. Plant Signal. Behav. 5:635-643.
47. Watanabe, T., G. Wang, K. Taki, Y. Ohashi, M. Kimura, and S. Asakawa. 2010. Vertical changes in bacterial and archaeal communities with soil depth in Japanese paddy fields. Soil Sci. Plant Nutr. 56:705-715.
48. Xie, B., X. Zheng, Z. Zhou, et al. 2010. Effects of nitrogen fertilizer on CH4 emission from rice fields: multi-site field observation. Plant Soil 326:393-401.
49. Zehr, J.P., B.D. Jenkins, S.M. Short, and G.F. Steward. 2003. Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ. Microbiol. 5:539-554.
50. Zhang, H., S. Hanada, T. Shigamatsu, K. Shibuya, Y. Kamagata, T. Kanagawa, and R. Kurane. 2000. Burkholderia kururiensis sp. nov., a tricholoroethylene (TCE)-degrading bacterium isolated from an aquifer polluted with TCE. Int. J. Syst. Evol. Microbiol. 50:743-749.