Mol Gen Genet (1986) 205:507-514
MGG
© Springer-Verlag1986
The pyridine nucleotide cycle of Salmonella typhimurium:
Genetic characterization of the pncXA operon
Jean M. Hill-Chappell, Michael P. Spector, and John W. Foster
Marshall University School of Medicine Huntington, WV 25705, USA
Summary. A series of Mudl and TnlO insertions were iden-
tified in the pncA chromosome region of Salmonella typhi-
murium which is responsible for the production of nicotin-
amide deamidase. Both pneA (resulting in no nicotinamide
deamidase activity) and pncX (resulting in lowered nicotin-
amide deamidase activity) insertions were constructed. In
addition, mutants which could utilize nicotinamide as a sole
source of nitrogen were isolated. These mutants, designated
pncH, hyperproduce nicotinamide deamidase. Genetic stu-
dies utilizing pncX-lacZ and pncA- lacZ operon fusions
indicate that pncX::TnlO insertions reduce transcription
ofpncA --lac while pncH mutations increase the expression
of both pncA-lacZ and pncX-lacZ. The gene order was
determined as purB-pncA-pncX-gdh with transcription
of both pncA and pncX occurring in the counterclockwise
direction. Merodiploid studies suggest a model whereby
pncX and pncA form an operon with the major promoter
occurring upstream from pncX. A second, weaker promoter
for pneA must be situated between pncX and pncA. The
pncH mutations appear to occur in the pncX promoter
(pncXp) increasing promoter activity.
Key words: Pyridine nucleotide cycle NAD metabolism
- Salmonella typhimurium Genetics
Introduction
The biosynthesis and metabolism of nicotinamide adenine
dinucleotide (NAD) in Salmonella typhimurium includes a
de novo and several recycling pathways termed pyridine
nucleotide cycles (PNC, Foster and Moat 1980). Two loci
involved in PNC metabolism have been identified based
in part upon the aquisition of analog resistance to 6-amino
nicotinic acid (6ANA) and/or 6-amino nicotinamide
(6ANAm). They are pncA (nicotinamide deamidase,
6ANAm%ANA ~) and pncB (nicotinic acid phosphoribosyl-
transferase [NAPRTase], 6ANAmr6ANAr). Earlier reports
from this laboratory indicated that pncA was constitutively
expressed while pncB was found to exhibit repression fol-
lowing growth on high concentrations of nicotinic acid
(NA), a precursor for NAD (Foster et al. 1979b). The re-
pression ofpncB is presumably due to changes in intracellu-
lar NAD concentrations. Mapping studies have placed
pncA at 27 units on the S. typhimurium linkage map (Foster
etal. 1979a; Sanderson and Roth 1983). A comparison
Offprint requests to. J.W. Foster
with the linkage map of Escherichia coli places pncA within
the major inversion region residing near one end of that
inversion (Foster et al. 1979a; Rosenfeld et al. 1982; Riley
and Anilionis 1978; Bachmann 1983).
Another locus, originally described by Hughes et al.
(1983), has been designatedpncX. In contrast to pncA muta-
tions which lack all demonstrable nicotinamide deamidase
activity, pncX mutations produce a reduced level of this
enzyme. The mutations, all isolated as TnlO insertions,
mapped in the vicinity of pncA. Hughes et al. (1983) sug-
gested that the pncX phenotype may either represent TnlO
insertions into pncA with some transcription ofpncA occur-
ring off an internal TnlO promotor or, alternatively, that
the insertions may inactivate a positive regulatory gene for
pncA.
We describe in this communication the isolation of
pncA::Mud and pncX::Mud insertions using the Mu cts
dl (Ap Lac) and the Mu cts dl-8 (Hughes and Roth, 1983)
vectors. These fusions were used to examine the expression
of pncA and pncX. TnlO insertions into pncA and pncX
were utilized to examine the effect each mutant locus has
upon the expression of the other. In addition, TnlO inser-
tions near pncA were used to construct pncX deletions, in-
versions and point mutations. Additional mutants, desig-
nated pncH, were isolated as hyperproducers of nicotin-
amide deamidase and the effect that pncH mutations have
on the expression of pncA and pncX was examined. The
data indicate that pncX and pncA form an operon with
a major promoter, pncXp, which allows transcription of
both pncX and pncA. A minor promoter occurs between
pncX and pncA that will result in a lowered expression of
pncA.
Materials and methods
Bacterial strains and culture conditions. All strains used in
this study were derivatives of Salmonella typhimurium LT-2
and are listed in Table 1. The minimal medium of Vogel
and Bonner (1956) and complete LB medium were used
and supplemented as described earlier (Foster et al. 1979a).
MOPS medium was as described by Neidhardt et al. (1974)
MOPS medium lacking a nitrogen source is referred to as
MOPS-N.
Chemicals and reagents. All chemicals used were of analyti-
cal quality. Nicotinic acid (NA) and nicotinamide (NAm)
were both used as pyridine sources at a concentration of