Mol Gen Genet (1989) 215:345-348
© Springer-Verlag 1989
Short communications
Identification of two fix loci controlling the expression
of nif genes in Rhizobium meliloti 41
Z. Banfalvi, V. Petkova, M. Lados, K. Slaska-Kiss, P. Putnoky, C.H. Ung, and A. Kondorosi*
Institute of Genetics, Biological Research Center, Hungarian Academy of Sciences, Szeged, PO Box 521, H-6701, Hungary
Summary. Recently, Fix- mutants of Rhizobium meliloti
41 defective for nifHDK transcription in the bacteroid state
have been described. Two of these mutants have been used
to identify bacterial genes involved in the regulation of n/f
gene expression. A nifA:: lacZ fusion was introduced into
the mutant strains and/~-galactosidase activity was assayed
in nodule bacteria, as well as in bacteria grown under micro-
aerobic conditions. One of the mutants did not express the
nifA gene in symbiosis, suggesting that the gene inactivated
by mutation fix-24 is involved in controlling the expression
of the nif structural genes via the regulatory gene nifA.
The mutation fix-24 also impaired the expression of nifA
under microaerobic conditions. These data are in agreement
with earlier findings that low oxygen concentration may
serve as a signal for n/f gene expression in symbiosis. The
fix gene marked by the mutation fix-24 might be a positive
regulator of nifA expression in R. meliloti 41. The other
mutation (fix-25) represented another cluster off ix genes
which also affected the expression of nifA. This influence,
however, was specific for symbiosis. The fix genes OCix-24,
fix-25) were localized on the symbiotic megaplasmid
pRme41b. The two genes are 10 kb apart from each other
and are located at 200 kb downstream of the n/f structural
genes in R. meliloti 41.
Key words: Rhizobium- Symbiosis- Oxygen regulation
- n/f genes - Fix mutants
In nitrogen fixing microorganisms the conversion of molec-
ular nitrogen into ammonia is catalyzed by the nitrogenase
enzyme complex. The synthesis and functioning of nitrogen-
ase is determined by the nitrogen fixation (n/f) genes which
are expressed only under certain conditions.
In Rhizobium meliloti, the symbiotic partner of Medi-
eago sativa (alfalfa), effective nitrogen fixation takes place
only in root nodules, special plant organs developed as a
result of the host specific Rhizobium-plant interaction. The
mfgenes of R. meliloti, together with the fix genesfixABCX
and the nodulation genes (host specific - hsn and "com-
mon" nod) are located on one of the two megaplasmids
characteristic for R. meliloti (Banfalvi et al. 1981, 1985; Ro-
senberg et al. 1981 ; Kondorosi et al. 1984; Earl et al. 1987;
Dusha et al. 1987). Although R. meliloti does not fix nitro-
Offprint requests to .' A. Kondorosi
gen ex planta, the mf structural genes (nifHDK) can be
activated by the NtrC protein when the cells are grown
in nitrogen limiting media. For symbiotic nitrogen fixation,
however, the NtrC protein is not required (Szeto et al.
1987). The n/f genes of R. meliloti are activated also by
low oxygen concentration. Under these conditions, the ex-
pression of nifA is independent of ntrC and the transcrip-
tion of nifA starts at the nifA promoter (Ditta et al. 1987).
This promoter is active in symbiosis as well (Kim et al.
1986; Buikema et al. 1985).
Recently, in our laboratory (Putnoky et al. 1988) nod-
ules induced by 64 random Fix- mutants of R. meliloti
41 were assayed for the ability to express 'late' nodulin
genes of M. sativa (leghemoglobin and nodulin-25 genes)
and two of the structural nitrogenase genes (nifHD) of R.
meliloti. Based on Northern hybridizations using the Lb,
nod-25 and nifHD gene probes, six Fix- mutants defective
for nifHD transcription in bacteroid form have been identi-
fied. Two of them (AK1487, AKI490) were obtained by
random Tn5 mutagenesis (Kondorosi et al. 1984). These
mutants have now been used to identify bacterial genes
involved in n/f regulation. A preliminary account of this
work was presented at the 7th International Congress on
N2 Fixation (Kondorosi et al. 1988). Using different ap-
proaches, very recently two other groups have also identi-
fied common regulatory elements controlling symbiotic and
microaerobic induction of nifA in R. meliloti 102F34 and
2011 (Virts et al. 1988; Kahn et al. 1988).
The fix genes mutated in AK1487 (fix-24) and AK1490 (fix-
25) control the expression ofnif structural genes via nifA
The lack of nifHD expression in the mutant bacteroids was
originally detected by Northern hybridization. To gain fur-
ther support for the inability of mutants AK1487 and
AK1490 to express ntf genes, plasmid pRKP9 carrying the
nifH: :lacZ fusion (Szeto et al. 1987) was introduced into
the two mutants and the/%galactosidase activities of the
nodules induced by the transconjugants were assayed. No
appreciable nifH expression was detected by this method
in AK1487. The fl-galactosidase activity of the AK1490
nodules was 20% of that found in the wild-type bacteroids.
The reduced level of nifH expression, however, was specific
for the mutation fix-25 (AK1490). Under the same condi-
tions, 2 weeks after inoculation no alteration could be de-
tected in a nifD:: Tn5 mutant (ZB277; Banfalvi et al. 1983)
used as a control in mfexpression experiments (Table 1).