1887

Microbiology Society logo

Volume 150, Issue 7

The nitrogen-fixing gene () of : a case of lateral gene transfer? Free

Abstract

Nitrogen fixation is catalysed by some photosynthetic bacteria. This paper presents a phylogenetic comparison of a nitrogen fixation gene () with the aim of elucidating the processes underlying the evolutionary history of . In the NifH phylogeny, strains of were placed in close association with spp. and other phototrophic purple non-sulfur bacteria belonging to the -, separated from its close relatives and the phototrophic rhizobia ( spp. IRBG 2, IRBG 228, IRBG 230 and BTAi 1) as deduced from the 16S rRNA phylogeny. The close association of the strains of with those of and , as well as , was supported by the mol% G+C of their gene and by the signature sequences found in the sequence alignment. In contrast, comparison of a number of informational and operational genes common to CGA009, USDA 110 and 2.4.1 suggested that the genome of is more related to that of than to the genome. These results strongly suggest that the of is highly related to those of the phototrophic purple non-sulfur bacteria included in this study, and might have come from an ancestral gene common to these phototrophic species through lateral gene transfer. Although this finding complicates the use of to infer the phylogenetic relationships among the phototrophic bacteria in molecular diversity studies, it establishes a framework to resolve the origins and diversification of nitrogen fixation among the phototrophic bacteria in the -.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26940-0
2004-07-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/7/mic1502237.html?itemId=/content/journal/micro/10.1099/mic.0.26940-0&mimeType=html&fmt=ahah

References

  1. Adachi J., Hasegawa M. 1996 MOLPHY: Programs for Molecular Phylogeny, Version 2.3 Tokyo: Institute of Statistical Mathematics;
  2. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
     [Google Scholar]
  3. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. 1995 Current Protocols in Molecular Biology vol I New York: Wiley;
  4. Cantera J. J. L., Kawasaki H., Seki T. 2002; Evolutionary relationship of phototrophic bacteria in the α-Proteobacteria based on farnesyl diphosphate synthase. Microbiology 148:1923–1929
     [Google Scholar]
  5. Eaglesham A. R. J., Ellis J. M., Evans W. R., Fleischman D. E., Hungria M., Hardy R. W. F. 1990; The first photosynthetic N2-fixing Rhizobium: characteristics. In Nitrogen Fixation: Achievements and Objectives pp. 805–811Edited by Gresshoff P. M., Roth L. E., Stacey G., Newton W. L. London: Chapman & Hall;
     [Google Scholar]
  6. Eardly B. D., Young J. P. W., Selander R. K. 1992; Phylogenetic position of Rhizobium sp. strain Or 191, a symbiont of bothMedicago sativa and Phaseolus vulgaris, based on partial sequences of the 16S rRNA and nifH genes. . Appl Environ Microbiol 58:1809–1815
     [Google Scholar]
  7. Fleischman D. E., Evans W. R., Miller I. M. 1995; Bacteriochlorophyll-containing Rhizobium species. Adv Photosynth 2:123–126
     [Google Scholar]
  8. Haukka K., Lindström K., Young J. P. W. 1998; Three phylogenetic groups of nodAand nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. Appl Environ Microbiol 64:419–426
     [Google Scholar]
  9. Hennecke H., Kaluza K., Fuhrmann M., Ludwig W., Stackebrandt E., Thöny B. 1985; Concurrent evolution of nitrogenase genes and 16S rRNA in Rhizobium species and other nitrogen-fixing bacteria. Arch Microbiol 142:342–348 [CrossRef]
     [Google Scholar]
  10. Hirsch A. M., McKhann H. I., Reddy A., Liao J., Fang Y., Marshall C. R. 1995; Assessing horizontal transfer of nifHDK genes in eubacteria: nucleotide sequence ofnifK from Frankia strain HFPCc13. . Mol Biol Evol 12:16–27 [CrossRef]
     [Google Scholar]
  11. Hurek T., Egener T., Reinhold-Hurek B. 1997; Divergence in nitrogenases of Azoarcus spp., Proteobacteria of the β subclass.. J Bacteriol 179:4172–4178
     [Google Scholar]
  12. Igarashi N., Harada J., Nagashima S., Matsuura K., Shimada K., Nagashima K. V. P. 2001; Horizontal transfer of the photosynthesis gene cluster and operon rearrangement in purple bacteria. J Mol Evol 52:333–341
     [Google Scholar]
  13. Imhoff J. F., Pfennig N., Trüper H. G. 1984; Rearrangement of the species and genera of the phototrophic “purple nonsulfur bacteria”. Int J Syst Bacteriol 34:340–343 [CrossRef]
     [Google Scholar]
  14. Inui M., Roh J. H., Zahn K., Yukawa H. 2001; Sequence analysis of the cryptic plasmid pMG101 from Rhodopseudomonas palustris and construction of stable cloning vectors. Appl Environ Microbiol 66:54–63
     [Google Scholar]
  15. Jeanmougin F., Thompson J. D., Gouy M., Higgins D. G., Gibson T. J. 1998; Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405 [CrossRef]
     [Google Scholar]
  16. Kawasaki H., Hoshino Y., Yamasato K. 1993; Phylogenetic diversity of phototrophic purple non-sulfur bacteria in the Proteobacteria α group. FEMS Microbiol Lett 112:61–66
     [Google Scholar]
  17. Ladha J. K., So R. B. 1994; Numerical taxonomy of photosynthetic rhizobia nodulating Aeschynomene species. Int J Syst Bacteriol 44:62–73 [CrossRef]
     [Google Scholar]
  18. Lisdiyanti P., Kawasaki H., Seki T., Yamada Y., Uchimura T., Komagata K. 2000; Systematic study of the genus Acetobacter with descriptions of Acetobacter indonesiensis sp.nov., Acetobacter tropicalis sp. nov., Acetobacter orleanensis (Hannenberg 1906) comb. nov., Acetobacter lovaniensis (Frateur 1950)comb. nov., and Acetobacter estunensis (Carr 1958) comb. nov.. J Gen Appl Microbiol 46:147–165 [CrossRef]
     [Google Scholar]
  19. Meyer J., Kelley B. C., Vignais P. M. 1978; Effect of light nitrogenase function and synthesis in Rhodopseudomonas capsulata. J Bacteriol 136:201–208
     [Google Scholar]
  20. Nagashima K. V. P., Hiraishi A., Shimada K., Matsuura K. 1997; Horizontal transfer of genes coding for the photosynthetic reaction centers of purple bacteria. J Mol Evol 45:131–136 [CrossRef]
     [Google Scholar]
  21. Normand P., Bousquet J. 1989; Phylogeny of nitrogenase sequences in Frankia and other nitrogen-fixing microorganisms. J Mol Evol 29:436–444 [CrossRef]
     [Google Scholar]
  22. Ohkuma M., Noda S., Usami R., Horikoshi K., Kudo T. 1996; Diversity of nitrogen fixation genes in the symbiotic intestinal microflora of the termite Reticulitermes speratus. Appl Environ Microbiol 62:2747–2752
     [Google Scholar]
  23. Ohkuma M., Noda S., Kudo T. 1999; Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl Environ Microbiol 65:4926–4934
     [Google Scholar]
  24. Page R. D. M. 1996; TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
     [Google Scholar]
  25. Perrière G., Gouy M. 1996; WWW-Query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369 [CrossRef]
     [Google Scholar]
  26. Ruvkum G. B., Ausubel F. M. 1980; Interspecies homology of nitrogenase genes. Proc Natl Acad Sci U S A 77:191–195 [CrossRef]
     [Google Scholar]
  27. Saitoh N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
     [Google Scholar]
  28. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467 [CrossRef]
     [Google Scholar]
  29. Stackebrandt E., Rainey F. A., Ward-Rainey N. 1996; Anoxygenic phototrophy across the phylogenetic spectrum: current understanding and future perspectives. Arch Microbiol 166:211–223 [CrossRef]
     [Google Scholar]
  30. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
     [Google Scholar]
  31. Torok I., Kondorosi A. 1981; Nucleotide sequence of the R. meliloti nitrogenase reductase (nifH) gene. Nucleic Acids Res 9:5711–5723 [CrossRef]
     [Google Scholar]
  32. Ueda T., Suga Y., Yahiro N., Matsuguchi T. 1995; Remarkable N2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis ofnifH gene sequences. J Bacteriol 177:1414–1417
     [Google Scholar]
  33. Widmer R., Shaffer B. T., Porteous L. A., Seidler J. 1999; Analysis of nifH gene pool complexity in soil and litter at a Douglas fir forest site in the Oregon cascade mountain range. Appl Environ Microbiol 65:374–380
     [Google Scholar]
  34. Woese C. R. 1987; Bacterial evolution. Microbiol Rev 51:221–271
     [Google Scholar]
  35. Woese C. R., Stackebrandt E., Weisburg W. G. & 8 other authors; 1984; Phylogeny of purple bacteria: the alpha subdivision. Syst Appl Microbiol 5:315–326 [CrossRef]
     [Google Scholar]
  36. Wong F. Y. K., Stackebrandt E., Ladha J. K., Fleischman D. E., Date R. A., Fuerst J. A. 1994; Phylogenetic analysis of Bradyrhizobium japonicum and photosynthetic stem-nodulating bacteria from Aeschynomene species grown in separated geographical regions. Appl Environ Microbiol 60:940–946
     [Google Scholar]
  37. Xiong J., Inoue K., Bauer C. E. 1998; Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci U S A 95:14851–14856 [CrossRef]
     [Google Scholar]
  38. Young J. P. W. 1992; Phylogenetic classification of nitrogen-fixing organisms. In Biological Nitrogen Fixation pp. 43–86Edited by Stacey G., Burris R. H., Evans H. J. New York: Chapman & Hall;
     [Google Scholar]
  39. Young J. P., Downer H. L., Eardly B. D. 1991; Phylogeny of phototrophic Rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA segment. J Bacteriol 173:2271–2277
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26940-0
Loading
The nitrogen-fixing gene (nifH) of Rhodopseudomonas palustris: a case of lateral gene transfer?
Microbiology 150, 2237 (2004); https://doi.org/10.1099/mic.0.26940-0
/content/journal/micro/10.1099/mic.0.26940-0
/content/journal/micro/10.1099/mic.0.26940-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error