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Functional Genomic Analysis of Three Nitrogenase Isozymes in the Photosynthetic Bacterium Rhodopseudomonas palustris

Yasuhiro Oda,^1, Sudip K. Samanta,^2, Federico E. Rey,^1,2 Liyou Wu,³ Xiudan Liu,^3,4 Tingfen Yan,³ Jizhong Zhou,³ and Caroline S. Harwood^1*

Department of Microbiology, University of Washington, Seattle, Washington 98195-7242,¹ Department of Microbiology, University of Iowa, Iowa City, Iowa 52242,² Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831,³ School of Minerals Processing and Bioengineering, Central South University, Changsha, 410083 Hunan, People's Republic of China⁴

Received 17 June 2005/ Accepted 26 August 2005

The photosynthetic bacterium Rhodopseudomonas palustris is one of just a few prokaryotes described so far that has vnf and anf genes for alternative vanadium cofactor (V) and iron cofactor (Fe) nitrogenases in addition to nif genes for a molybdenum cofactor (Mo) nitrogenase. Transcriptome data indicated that the 32 genes in the nif gene cluster, but not the anf or vnf genes, were induced in wild-type and Mo nitrogenase-expressing strains grown under nitrogen-fixing conditions in Mo-containing medium. Strains that were unable to express a functional Mo nitrogenase due to mutations in Mo nitrogenase structural genes synthesized functional V and Fe nitrogenases and expressed vnf and anf genes in nitrogen-fixing growth media that contained Mo and V at concentrations far in excess of those that repress alternative nitrogenase gene expression in other bacteria. Thus, not only does R. palustris have multiple enzymatic options for nitrogen fixation, but in contrast to reports on other nitrogen-fixing bacteria, the expression of its alternative nitrogenases is not repressed by transition metals. Between 95 and 295 genes that are not directly associated with nitrogenase synthesis and assembly were induced under nitrogen-fixing conditions, depending on which nitrogenase was being used by R. palustris. Genes for nitrogen acquisition were expressed at particularly high levels during alternative nitrogenase-dependent growth. This suggests that alternative nitrogenase-expressing cells are relatively starved for nitrogen and raises the possibility that fixed nitrogen availability may be the primary signal that controls the synthesis of the V and Fe nitrogenases.

Supplemental material for this article may be found at http://jb.asm.org/.

Y.O. and S.K.S. contributed equally to this work.

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