Mol Gen Genet (1988) 214:562-569
© Springer-Verlag 1988
Cloning and comparative sequence analysis of the gene coding
for isopenicillin N synthase in Streptomyces
Dov Shiffman 1, Moshe Mevarech 1, Susan E. Jensen 2, Gerald Cohen 1, and Yair Aharonowitz 1
1 Tel Aviv University, The George S. Wise Faculty of Life Sciences, Department of Microbiology, Ramat Aviv, 69978, Israel
z University of Alberta, Department of Microbiology, Edmonton, Alberta, Canada, T6G 2E9
Summary. The genes coding for isopenicillin N synthase
(IPNS) in Streptomyces jumonjinensis and S. Iipmanii were
isolated from recombinant phage lambda libraries using the
S. clavuligerus IPNS gene as a heterologous probe. The
S. jumonjinensis IPNS gene has an open reading frame cod-
ing for 329 amino acids, identical in size to that of the
previously cloned S. clavuligerus IPNS gene. A partial nu-
cleotide sequence was also determined for the S. lipmanii
IPNS gene. Comparison of the predicted amino acid se-
quences of all three streptomycete IPNS proteins shows
that they exhibit more than 70% similarity, close to that
found in comparisons among fungal IPNS proteins and
significantly greater than that found, approximately 60%,
between Streptomyces and fungal IPNS proteins. We con-
clude that procaryotic and eucaryotic IPNS genes are sub-
groups of a single family of microbial IPNS genes. Hybrid-
ization probes prepared from IPNS genes of the above
streptomycete species were used to detect analogous genes
in eight other strains that included both penicillin and ce-
phalosporin producers and non-producers. Each producer
strain responded with all three probes implying the presence
of an IPNS gene. Surprisingly, several non-producer strains
also responded with one or two of the probes. Our results
suggest that IPNS-related genes may be more prevalent in
Streptomyces than previously believed.
Key words: Isopenicillin-N synthase - Streptomyces - B -
lactam antibiotics - Sequence similarity - Cloning
Introduction
Microorganisms that produce/%lactam antibiotics are wide-
spread in nature (Elander 1983). Originally these com-
pounds were discovered in fungi and found to consist of
two main classes, the penicillins and cephalosporins. Peni-
cillins are made by several funsal species including Penicil-
lium chrysogenum and Aspergillus nidulans. Cephalosporins
are found in Cephalosporium acremonium. More recently
fl-lactam antibiotics have been shown to be made in a much
more diverse group of taxonomically unrelated species.
Thus, many new fl-lactam compounds have been isolated
Offprint requests to: Y. Aharonowitz
from actinomycetes and in particular from the genus Strep-
tomyces. Moreover, with the development of more sensitive
methods for detection of/~-lactam antibiotics a variety of
gram-negative bacteria, Pseudomonas, Gluconobacter, Ace-
tobacter and Flavobacterium, have also been shown to make
these types of metabolites (Elander 1983). Microbial//-lac-
tams are conveniently classified according to their chemical
structure: most important of these are the penicillins, ce-
phalosporins, cephamycins, clavams, carbapenems and the
monocyclic/Mactams comprising nocardicins and sulfaze-
cins. In the present study our analysis is confined to the
first three classes.
The early steps in the biosynthesis of penicillins, cepha-
losporins and cephamycins are essentially the same in eucar-
yotic and procaryotic organisms (Jensen 1986). A multi-
functional enzyme, ACV synthetase, mediates the initial
steps in their synthesis through formation of a linear tripep-
tide 6-(L-~-aminoadipyl)-L-cysteinyl-D-valine (ACV) (Banko
and Demain 1987). The enzyme isopenicillin N synthase
(IPNS) then catalyzes the oxidative cyclization of the tripep-
tide, in the presence of Oz, Fe 2÷ and ascorbate, to form
the first /?-lactam intermediate isopenicillin N (Konomi
et al. 1979). IPNS has been extensively purified from two
funsal species, P. chrysogenum (Ramos et al. 1985) and C.
acremonium (Pang et al. 1984) and two streptomycete spe-
cies, Streptomyces clavuligerus (Jensen et al. 1986) and
S. Iactamdurans (Castro et al. 1988). In the case of C. acre-
monium and S. clavuligerus partial amino acid sequences
were made at the NH2-terminal end of the IPNS proteins
and the information used to construct oligodeoxynucleotide
probes for isolating the corresponding genes (Samson et al.
1985; Leskiw et al. 1988). These genes can, in turn, serve
as hybridization probes to isolate heterologous IPNS genes
in other related fl-lactam producing organisms. Thus, the
IPNS gene of C. acremonium was used to clone the analo-
gous genes ofP. chrysogenum (Carr et al. 1986) and A. nidu-
lans (Ramon et al. 1987).
In this paper we describe the use of a hybridization
probe derived from the S. clavuligerus IPNS gene to isolate
the corresponding IPNS genes from S.jumonjinensis and
S. lipmanii. The protein-coding regions of these genes were
sequenced and the data used to compare their predicted
amino acid sequences with those of other funsal and strep-
tomycete IPNS genes. We also describe the use of hybridiza-
tion probes from Streptomyces IPNS genes to detect analo-
gous genes in other streptomycete species.