Correlation of Denitrifying Capability with the Existence of nap, nir, nor and nos Genes in Diverse Strains of Soybean Bradyrhizobia

Microbes and Environments

Volumn 21, Issue 3, 2006, Pages 174-184

  Sameshima Saito, Reiko ^a   Chiba, Kaori ^b   Minamisawa, Kiwamu ^b  

^a SHIZUOKA UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

Bradyrhizobium; denitrification; denitrifying genes; nosZ

Indexed keywords

EID: 57149102761     PISSN: 13426311     EISSN: 13474405     Source Type: Journal    
DOI: 10.1264/jsme2.21.174     Document Type: Article

References (38)

1. Asakawa, S. 1993. Denitrifying ability of indigenous strains of Bradyrhizobium japonicum isolated from fields under paddy-upland rotation. Biol. Fertil. Soils 15: 196–200.
2. Baek, S.H. and J.P. Shapleigh. 2005. Expression of nitrite and nitric oxide reductases in free-living and plant-associated Agrobacterium tumefaciens C58 cells. Appl. Environ. Microbiol. 71: 4427–4436.
3. Barton, L.L. 2005. Dissimilatory nitrate reduction. p. 689–694. In Structural and functional relationships in prokaryotes. Springer Science+Business Media, Inc., 233 Spring Street, New York, NY 10013, USA.
4. Breitenbeck, G.A. and J.M. Bremner. 1989. Ability of free-living cells of Bradyrhizobium japonicum to denitrify in soils. Biol. Fertil. Soils. 7: 219–224.
5. Cataldo, D.A., M. Haroon, L.E. Schrader and V.L. Youngs. 1975. Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun. Soil Sci. Plant Anal. 6: 71–80.
6. Cole, M.A. and G.H. Elkan. 1973. Transmissible resistance to penicillin G, neomycin, and chloramphenicol in Rhizobium japonicum. Antimicrob. Agents. Chemother. 4: 248–253.
7. Delgado, M.J., N. Bonnard, A. Tresierra-Ayala, E.J. Bedmar and P. Müller. 2003. The Bradyrhizobium japonicum napEDABC genes encoding the periplasmic nitrate reductase are essential for nitrate respiration. Microbiology 149: 3395–3403.
8. Devereux, R. and S.G. Willis. 1995. Amplification of ribosomal RNA sequences p. 3.3.1–3.3.11. In A.D.L. Akkermans, J.D. van Elsas and F.J. deBruijn (ed.), Molecular microbial ecology manual. Kluwer Academic Publishers, Dordrecht, Netherlands.
9. Galibert, F., T.M. Finan, S.R. Long, A. Puhler, P. Abola, F. Ampe, F. Barloy-Hubler, M.J. Barnett, A. Becker, P. Boistard, G. Botche, M. Boutry, L. Bowser, J. Buhrmester, E. Cadieu, D. Capela, P. Chain, A. Cowie, R.W. Davis, S. Dreano, N.A. Federspiel, R.F. Fischer, S. Gloux, T. Godrie, A. Goffeau, B. Golding, J. Gouzy, M. Gurjal, I. Hernandez-Lucas, A. Hong, L. Huizar, R.W. Hyman, T. Jones, D. Kahn, M.L. Kahn, S. Kalman, D.H. Keating, E. Kiss, C. Komp, V. Lelaure, D. Masuy, C. Palm, M.C. Peck, T.M. Pohl, D. Portetelle, B. Purnelle, U. Ramsperger, R. Surzycki, P. Thebault, M. Vandenbol, F.J. Vorholter, S. Weidner, D.H. Wells, K. Wong, K.C. Ye and J. Batut. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti, Science, 293: 668–672.
10. Isawa, T., R. Sameshima, H. Mitsui and K. Minamisawa. 1999. IS1631 occurrence in Bradyrhizobium japonicum highly reiterated sequence-posessing strains with high copy numbers of repeated sequences RSα and RSβ. Appl. Environ. Microbiol. 65: 3493- 3501.
11. Kaluza, K., M. Hahn and H. Hennecke. 1985. Repeated sequences similar to insertion elements clustered around the nif region of the Rhizobium japonicum genome. J. Bacteriol. 162: 535–542.
12. Kaneko, T., Y. Nakamura, S. Sato, E. Asamizu, T. Kato, S. Sasamoto, A. Watanabe, K. Idesawa, A. Ishikawa, K. Kawa-shima, T. Kimura, Y. Kishida, C. Kiyokawa, M. Kohara, M. Matsumoto, A. Matsuno, Y. Mochizuki, S. Nakayama, N. Nakazaki, S. Shimpo, M. Sugimoto, C. Takeuchi, M. Yamada and S. Tabata. 2000. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7: 331–338.
13. Kaneko, T., Y. Nakamura, S. Sato, K. Minamisawa, T. Uchiumi, S. Sasamoto, A. Watanabe, K. Idesawa, M. Iriguchi, K. Kawa-shima, M. Kohara, M. Matsumoto, S. Shimpo, H. Tsuruoka, T. Wada, M. Yamada and S. Tabata. 2002. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 9: 189–197.
14. Keeney, D.R. and D.W. Nelson. 1982. Nitrite by colorimetric methods. p. 682–687. In A.L. Page (ed) Methods of Soil Analysis, Part 2, Chemical and microbiological properties, second edition, number 9 (part 2) in the series agronomy, American Society of Agronomy, Soil Science Society of America, Madison, Wisconsin USA.
15. Lashof, D.A. and D.R. Ahuja. 1990. Relative contributions of greenhouse gas emissions to global warming. Nature. 3: 529–531.
16. Maniatis, T., E.F. Fritsch and J. Sambrook. 1982. Molecular cloning a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
17. Mesa, S., J.D. Alche, E.J. Bedmar and M.J. Delgado. 2004. Expression of nir, nor and nos denitrification genes from Bradyrhizobium japonicum in soybean root nodules. Physiol Plant 120: 205–211.
18. Mesa, S., L. Velasco, M.E. Manzanera, M.J. Delgado and E.J. Bedmar. 2002. Characterization of the norCBQD genes, encoding nitric oxide reductase, in the nitrogen fixing bacterium Bradyrhizobium japonicum. Microbiology. 148: 3553–3560.
19. Minamisawa, K. and H. Mitsui. 2000. Genetic ecology of soybean bradyrhizobia, p. 349–377. In J. Bollag and G. Stotzky (ed.), Soil biochemistry, vol. 10. Marcel Dekker, NewYork, N.Y.
20. Minamisawa, K., T. Isawa, Y. Nakatsuka and N. Ichikawa. 1998. New Bradyrhizobium japonicum strains that possess high copy numbers of the repeated sequence RSα. Appl. Environ. Microbiol. 65: 1845–1851.
21. Minamisawa, K., T. Seki, S. Onodera, M. Kubota and T. Asami. 1992. Genetic relatedness of Bradyrhizobium japonicum field isolates as revealed by repeated sequences and various other characteristics. Appl. Environ. Microbiol. 58: 2832–2839.
22. Minamisawa, K., Y. Nakatsuka and T. Isawa. 1999. Diversity and field site variation of indigenous populations of soybean bradyrhizobia in Japan by fingerprints with repeated sequences RSα and RSβ. FEMS Microbiol. Ecol. 29: 171–178.
23. Okada, N., N. Nomura, T. Nakajima-Kambe and H. Uchiyama. 2005. Characterization of the aerobic denitrification in Mesorhizobium sp. strain NH-14 in comparison with that in related rhizobia. Microbes Environ. 20: 208–215.
24. Philippot, L. 2002. Denitrifying genes in bacterial and archaeal genomes. Biochim. Biophys. Acta. 1577: 355–376.
25. Saeki, Y., N. Aimi, M. Hashimoto, S. Tsukamoto, A. Kaneko, N. Yoshida, Y. Nagatomo and S. Akao. 2004. Grouping of Bradyrhizobium USDA strains by sequence analysis of 16S rDNA and 16S-23S rDNA internal transcribed spacer region. Soil Sci. Plant Nutr. 50: 517–525.
26. Sameshima, R., T. Isawa, M.J. Sadowsky, T. Hamada, H. Kosai, A. Shutsrirung, H. Mitsui and K. Minamisawa. 2003. Phylogeny and distribution of extra-slow-growing Bradyrhizobium japoni-cum harboring high copy numbers of RSα, RSβ and IS1631. FEMS Microbiol. Ecol. 44: 191–202.
27. Sameshima-Saito, R., K. Chiba, J. Hirayama, M. Itakura, H. Mitsui, S. Eda and K. Minamisawa. 2006. Symbiotic Bradyrhizo-bium japonicum reduces N2O surrounding the soybean root system via nitrous oxide reductase. Appl. Environ. Microbiol. 72: 2526–2532.
28. Sameshima-Saito, R., K. Chiba and K. Minamisawa. 2004. New method of denitrification analysis of Bradyrhizobium field isolates by gas chromatographic determination of 15N-labeled N2. Appl. Environ. Microbiol. 70: 2886–2891.
29. Starkenburg, S.R., P.S.G. Chain, L.A. Sayavedra-Soto, L. Hauser, M.L. Land, F.W. Larimer, S.A. Malfatti, M.G. Klotz, P.J. Bottomely, D.J. Arp and W.J. Hickey. 2006. Genome sequence of the chemolithoautotrophic nitrite-oxidizing bacterium Nitrobacter winogradskyi Nb-255. Appl. Environ. Microbiol. 72: 2050–2063.
30. Tiedje, J.M. 1994. Denitrification p. 245–267. In R.W. Weaver et al. (ed.) Mehods of soil analysis. Part2. Microbiological and Biochemical Properties. SSSA Book Series, no. 5. Soil Science Society of America, Madison, Wis., USA.
31. van Berkum, P. and J.J. Fuhrmann. 2000. Evolutionary relationships among the soybean bradyrhizobia reconstructed from 16S rRNA gene and internally transcribed spacer region sequence divergence. Int. J. Syst. Evol. Microbiol. 50: 2165–2172.
32. van Berkum, P. and H.H. Keyser. 1985. Anaerobic growth and denitrification among different serogroups of soybean rhizobia. Appl. Environ. Microbiol. 49: 772–777.
33. Velasco, L., S. Mesa, C. Xu, M.J. Delgado and E.J. Bedmar. 2004. Molecular characterization of nosRZDFYLX genes coding for denitrifying nitrous oxide reductase of Bradyrhizobium japonicum. Antonie van Leeuwenhoek 85: 229–235.
34. Velasco. L., S. Mesa, M.J. Delgado and E.J. Bedmar. 2001. Characterization of the nirK gene encoding the respiratory, Cu-containing nitrite reductase of Bradyrhizobium japonicum. Biochim. Biophys. Acta. 1521: 130–134.
35. Waibel, A.E., T. Peter, K.S. Carslaw, H. Oelhaf, G. Wetzel, P.J. Crutzen, U. Poschl, A. Tsias, E. Reimer and H. Fischer. 1999. Arctic ozone loss due to denitrification. Science 283: 2064–2069.
36. Xu, L.M., C. Ge, Z. Cui, J. Li and H. Fan. 1995. Bradyrhizobium liaoningense sp. nov. isolated from the root nodules of soybeans. Int. J. Syst. Bacteriol. 45: 706–711.
37. Yamamoto, M., H. Murai, A. Takeda, S. Okunishi and H. Morisaki. 2005. Bacterial flora of the biofilm formed on the submerged surface of the reed Phragmites australis. Microbes Environ. 20: 14–24.
38. Zumft, W.G. 1997. Cell biology and molecular basis of denitrifi-cation. Microbiol. Mol. Biol. Rev. 61: 533–616.