Vol. 169, No. 9
JOURNAL OF BACTERIOLOGY, Sept. 1987, p. 4024-4029
0021-9193/87/094024-06$02.00/0
Copyright © 1987, American Society for Microbiology
Comparative Organization of Nitrogen Fixation-Specific Genes from
Azotobacter vinelandii and Klebsiella pneumoniae: DNA Sequence
of the nifUSV Genes
JIM BEYNON,' ABDUL ALLY,' MAURA CANNON,' FRANK CANNON,' MARTY JACOBSON,2
VALERIE CASH,2 AND DENNIS DEAN2*
BioTechnica International, Inc., Cambridge, Massachusetts 02140,1 and Department of Anaerobic Microbiology, Virginia
Polytechnic Institute and State University, Blacksburg, Virginia 24060'
Received 4 March 1987/Accepted 15 June 1987
In the facultative anaerobe Klebsiella pneamoniae 17 nitrogen fixation-specific genes
(nif genes) have been
identified. Homologs to 12 of these genes have now been isolated from the aerobic diazotroph Azotobacter
vinelandii. Comparative studies have indicated that these diverse microorganisnms share strikiig similarities in
the genetic organization of their nif genes and in the primary structure of their individual nif gene products.
In this study the complete nucleotide sequences of the nifUSV gene clusters from both K. pneumoniae and A.
vinelandii were determined. These genes are identically organized on their respective genomes, and the
individual genes and their products exhibit a high degree of interspecies sequence homology.
Nitrogen fixation is catalyzed by the enzyme nitrogenase,
a complex two-component metalloenzyme. In the facultative
anaerobe Klebsiella pneumoniae there are at least 17 genes
whose products are likely to be required for the synthesis
and assembly of a fully active nitrogen-fixing system. These
genes include nifHDK (nitrogenase structural components);
nipF and nifJ (electron transport components); nifQ, niJB,
niJE, nijN, and nifV (FeMo-cofactor biosynthetic compo-
nents); nifA and nifL (positive and negative regulatory
elements); nifM (Fe protein maturation component); and
nifY, nJX, nifU, and nifS (functions not known). For a
recent review, see reference 7. The nif genes are clustered
on the K. pneumoniae chromosome and are organized into
eight transcriptional units (1). A gene-product relationship
has been established,for many of the K. pneumoniae nif-
specific components (9, 18), yet only those products encoded
by the nitrogenase structural genes and those encoded by the
electronl transport-specific genes (16, 24) have been purified
in their native form. Since the function of a number of the
uncharacterized nif gene products is likely to involve a
catalytic action upon a nitrogenase structural component,
for example, metallocenter assembly, it is probable that
some of these gene products are present in nitrogen-fixing
cells in only low amounts. This possibility and the prospect
that many of the ancillary nif gene products will share with
the structural components an extreme sensitivity to oxygen
potentially present a formidable challenge for nif gene prod-
uct isolation and biochemical characterization.
One approach for initiating the characterization of nif gene
products is the determination of their polypeptide sequences
deduced from DNA sequence analysis. Such an approach
can provide (i) insights into the structural features of the
encoded polypeptides, (ii) DNA sequence information nec-
essary for the construction of hybrid plasmids that can be
used to enhance the production of the individual nif poly-
peptides, and (iii) the information and materials needed for
the directed mutagenesis of the individual nif genes. In this
regard, comparative studies of the primary sequences of
individual nif-specific components from diverse diazotrophic
*
Corresponding author.
species are of particular relevance because conserved se-
quences among homologous proteins are likely to indicate
their important structural features.
In the case of the nitrogenase structural components, a
high degree of interspecies sequence homology has permit-
ted the isolation of nitrogenase structural genes from numer-
ous diazotrophic species (20). Similarly, the demonstration
of interspecies homologies among other individual nif genes
should also permit the identification and isolation of such
genes from a variety of diazotrophs. Summarized here are
results obtained by using this approach for the isolation and
mapping of nif genes from the aerobic diazotroph Azotobac-
ter vinelandii. A comparison of the physical organization of
nif genes established for K. pneumoniae with that currently
developed for A. vinelandii is presented. In addition, we
have determined and compared the nucleotide sequences of
the nifUSV gene clusters from both K. pneumoniae and A.
vinelandii and compared their respective encoded polypep-
tides.
MATERIALS AND METHODS
The results of physical and genetic mapping procedures
used to define the K. pneulnoniae nifUSV gene cluster are
summarized in reference 1. The identification of the A.
vinelandii nifUSV gene cluster was based on its homology to
the K. pneumoniae nifUSV gene cluster (see Results). The
DNA sequences of the A. vinelandii and K. pneumoniae
nifUSV gene clusters were determined by the dideoxy chain
termination procedure (21) by using hybrids of filamentous
phage vectors described by Messing (15). For A. vinelandii
sequencing experiments, the hybrid plasmids used as DNA
sources are shown in Fig. 1A. For these experiments purified
DNA fragments were digested with the individual restriction
enzymes Sau3A, EcoRI, SmaI, XhoI, PstI, Sall, HinclI,
HinPI, and MspI or some combination of these restriction
enzymes and ligated into the appropriately digested replica-
tive form of the filamentous phage vector DNA. Approxi-
mately 200 base pairs were determined in each sequencing
experiment. All sequences were determined in an overlap-
ping fashion and in both directions. For K. pneumoniae
sequencing experiments, the hybrid plasmid pWK25 (17)
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