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Journal of Bacteriology, October 2000, p. 5911-5915, Vol. 182, No. 20
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Organization and Expression of a Thermus thermophilus
Arginine Cluster: Presence of Unidentified Open Reading Frames and
Absence of a Shine-Dalgarno Sequence
Rony
Sanchez,1
Martine
Roovers,1 and
Nicolas
Glansdorff1,2,3,*
Department of Microbiology, Flanders
Interuniversity Institute for Biotechnology
(VIB),1 Department of Microbiology,
Free University of Brussels (VUB),2 and
Research Institute J. M. Wiame,3
1070 Brussels, Belgium
Received 18 April 2000/Accepted 26 July 2000
 |
ABSTRACT |
A group of genes regulated by arginine was found clustered in the
order argF-ORF1-argC-argJ-ORF4
between other, as yet uncharacterized, open reading frames (ORFs).
Transcription starts were identified immediately upstream from
argF and ORF4. Arginine repressed transcription that was
initiated at argF but induced transcription of
ORF4. The functions of ORF1 and ORF4 are unknown, but analysis of the sequence of ORF4 suggests that it is a membrane protein,
possibly involved in transport of arginine or a related metabolite.
Mobility shift and DNase I footprinting have revealed specific binding of pure Escherichia coli ArgR to the promoter
region of Thermus thermophilus argF. These results
suggest that argF transcription is controlled by a
repressor homologous to those characterized in enteric bacteria
and bacilli. Thermus argF mRNA is devoid of Shine-Dalgarno
(SD) sequences. However, downstream from the ATG start codon of
argF and many other Thermus genes (with or
without an SD box), sequences were found to be complementary to
nucleotides 1392 to 1409 of Thermus 16S rRNA,
suggesting that an mRNA-rRNA base pairing in this region is important
for correct translation initiation.
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TEXT |
In arginine biosynthesis two
alternative pathways have evolved to split off the acetyl group of
N-acetylornithine.
Enterobacteriaceae, Vibrionaceae,
Myxococcus xanthus, and possibly also the archaeon Sulfolobus acidocaldarius use a linear pathway in which the
formation of ornithine is mediated by acetyl ornithinase (encoded
by argE) (14, 12, 31, 36). Other bacteria,
archaea, and eukaryotic microbes recycle the acetyl group by
transacetylation of N-acetylornithine and glutamate
(26). The transacetylation is catalyzed by ornithine acetyltransferase (encoded by argJ), an enzyme which in some
organisms is also able to use acetyl coenzyme A to acetylate glutamate
and in this way bypasses the first step of the linear pathway (11, 26). Ornithine carbamoyltransferase (encoded by argF)
converts ornithine and carbamoyl phosphate (CP) into citrulline. CP is extremely thermolabile, and in Pyrococcus furiosus
(17), Pyrococcus abyssi (25), and
Thermus thermophilus ZO5 (32), it appears to be
protected from thermal decomposition into the indiscriminate carbamoylating agent cyanate, by channeling towards citrulline and
carbamoyl aspartate.
Arginine genes may be either scattered (as in several proteobacteria,
Aquifex aeolicus, cyanobacteria, and archaea) or clustered in two different patterns (2, 36): divergently transcribed clusters (enteric bacteria and Vibrionaceae) or clusters of
variable extension where argC and argJ are found
together, as in the gram-positive organisms Thermotoga
maratima and Thermus (see below). Nevertheless, regulation appears to be similar in most of these organisms: an ArgR
repressor interacts with specific operator sequences (called Arg boxes)
overlapping the promoter region (5, 6, 12, 18, 28).
Homologous proteins were also reported to activate genes involved in
arginine degradation in bacilli (19, 20). However, a
nonhomologous arginine regulatory protein has been identified in
Pseudomonas aeruginosa (22). Except for
proteobacteria and gram-positive organisms, little is known about the
regulation of arginine biosynthesis. T. thermophilus
(24) is an interesting bacterium in two respects, as a
paradigm for investigations on extreme thermophily and as a
representative of a deep-branching division which also contains
Deinococcus radiodurans (its closest relative),
Chloroflexus, and Thermomicrobium
(34). In this study we describe the organization and
expression of an unusual type of arginine gene clustering in T. thermophilus HB27.
For all experiments, Thermus was grown at 75°C in
arginine- and uracil-free liquid medium (4) with 20 mM
pyruvate as the carbon source and 10 mM ammonium sulfate as the
nitrogen source. Chromosomal DNA partially digested with
Sau3A was used to construct a 
-ZAP genomic library
(Stratagene), which was screened as described by Sanchez et al.
(27). Primer extension experiments were performed according
to the method described by Kholti et al. (15) except that
hybridization experiments were performed overnight at 45°C. Primers
were oligonucleotides complementary to the sequences 60 to 80 nucleotides downstream from the ATG codon of each open reading frame
(ORF). S1 nuclease mapping was also done according to the method
described by Kholti et al. (15). For mobility shift assays, pure Escherichia coli and Bacillus stearothermophilus
arginine repressors (final concentration, 45 µg/ml) were
incubated for 30 min at 37°C with a 32P-end-labeled DNA
fragment in binding buffer (1 mM Tris-HCl [pH 7.4], 5 mM
MgCl2, 250 mM KCl, 2.5 mM CaCl2, 0.5 mM
dithiothreitol, and 2.5% glycerol) with a 100-fold excess of sonicated
herring sperm DNA in the presence or absence of 10 mM arginine.
DNA-protein complexes were then immediately loaded on a 6%
polyacrylamide gel. For DNase I footprinting experiments
(10) a single 32P-end-labeled DNA fragment (100 ng/ml) and a 100-fold excess of nonspecific competitor DNA were
incubated for 30 min at 37°C in binding buffer (as for the mobility
shift assay described above) containing pure repressor (9 µg/ml).
DNase I was added at a final concentration of 0.7 mg/ml, and the
digestion was terminated after 30 s by the addition of stop buffer
(0.6 M ammonium acetate and 0.05 M EDTA [final concentration]) and 10 µg of yeast tRNA. After DNA precipitation the reaction products were
analyzed on a 6% denaturating polyacrylamide gel.
Clustering of arginine biosynthetic genes and unidentified
ORFs. By screening the -ZAP library we identified in order of
transcription ORF6-ORF7-ORF8-argF (i.e.,
ORF9)-ORF1-argC (i.e., ORF2)-argJ (i.e.,
ORF3)-ORF4-ORF5 (Fig. 1). The start codon
of argJ overlaps the stop codon of argC. This is
also the case for ORF7 and ORF8. A putative rho-independent terminator
was found between ORF4 and ORF5. A BLAST search showed that ORF6-like
proteins belong to the UPF0078 family (National Center for
Biotechnology Information database). They occur in several bacteria,
such as E. coli (YgiH), Bacillus subtilis (YneS),
and Mycoplasma pneumoniae (YgiH), as potential integral
membrane proteins containing several putative transmembrane regions. At
least five such regions occur in ORF6 (data not shown). Alignment
studies showed highly conserved regions in the N-terminal (GATN) and
central parts (FKGGKAVAT) of the protein. ORF7 encodes a
polypeptide of 113 amino acids; it is homologous to five genes
scattered throughout the genome of Methanococcus jannaschii,
one of which was found next to carB, which encodes a subunit
of CP synthetase. Two exemplars of this gene were found in
Synechocystis. These ORF7 homologues all overlap a
neighboring gene. In Thermus, ORF7 overlaps ORF8. ORF8-like genes occur in E. coli (yaiS), B. subtilis (ypjG), Mycobacterium leprae
(lmbE), and Streptomyces lincolnensis
(lmbE). Few genes homologous to ORF1 or ORF4 were found. An
ORF1 homologue occurs in Synechocystis with 32% identity at
the amino acid level. For ORF4, a similar gene was encountered in
D. radiodurans (31% identical amino acids). Interestingly,
the N-terminal part of ORF4 is similar to the signal sequence of outer
membrane proteins of the OmpA family (Fig.
2). No similarity was found beyond the
signal sequence. ORF4 thus probably encodes a membrane protein; in this
respect it is reminiscent of the P. aeruginosa OpcD porin
(23), which facilitates the diffusion of basic amino acids.
There is no obvious similarity between the two sequences, but
expression of both OpcD and Thermus ORF4 (see below) is
strongly induced by arginine.
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FIG. 1.
Schematic drawing of the organization of arginine
biosynthetic genes in T. thermophilus. The genes involved in
arginine biosynthesis are: argF (ornithine
carbamoyltransferase), argC
(N-acetyl-gamma-glutamyl-phosphate reductase), and
argJ (glutamate N-acetyltransferase). Other ORFs
encode proteins with unknown functions. Arrows show the direction and
starting points of transcription. The number of nucleotides present
between each pair of ORFs is indicated. A putative
rho-independent terminator is present between ORF4 and ORF5.
The deduced C-terminal amino acid sequence of ORF4 is shown; the stop
codon is indicated by an asterisk.
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FIG. 2.
(A) Primer extension mapping of the transcriptional
starting point of the T. thermophilus ORF4 region. Equal
amounts (about 50,000 cpm) of 5'-end-labeled 20-mer primer were mixed
with 100 µg of RNA extracted from cultures grown in minimal medium
(1) or supplemented with arginine (2). After precipitation and
hybridization the extension reaction was performed. The position of the
transcript is indicated by the arrow; the sequence shown is of the
noncoding strand. Lanes G, A, T, and C represent chain-terminating
DNA-sequencing reactions of the noncoding strand with the
oligonucleotide also used as a primer in the primer extension
experiment. (B) Nucleotide and deduced amino acid sequences of a
portion of the T. thermophilus ORF4 gene and its promoter
region. The arrow pointing downward indicates the transcriptional start
site. Also,  35 and 10 promoter sequences are underlined and in bold
type. A putative ribosome binding site is indicated by bold letters.
The underlined amino acids of ORF4 are identical to the signal sequence
of seven proteins of the OmpA family (E coli,
Salmonella enterica serovar Typhimurium, B. subtilis, Pseudomonas luteolum, Serratia
marcescens, Enterobacter aerogenes, and Shigella
dysenteriae).
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Starting points of transcription. Primer extension
experiments performed for each of the genes present in the cluster showed that transcription was initiated just before ORF4 (Fig. 2),
ORF5, and ORF6 (data not shown), whereas no transcription starts were
observed immediately upstream of ORF7, ORF8, ORF1, argC, or
argJ. Transcription from the ORF6 promoter was very weak and
not influenced by arginine, whereas transcription of ORF4 was strongly
activated in the presence of arginine. In primer extension experiments,
argF cDNA synthesis stopped within the coding region,
presumably because of a secondary structure forming in the transcript.
S1 nuclease mapping showed two major bands (Fig.
3) corresponding to a T residue and a C
residue, 2 and 4 nucleotides upstream from the AUG codon, respectively.
The intensity was strongly reduced with RNA extracted from cells grown
in the presence of arginine. Previous experiments already indicated
that arginine represses OTCase synthesis in Thermus
(27, 31). The region thus appears to contain four
consecutive transcription units: ORF6, ORF7, ORF8, argF;
ORF1, argC, argJ; ORF4; and ORF5.
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FIG. 3.
(A) S1 nuclease mapping of the transcriptional starting
point of the argF region. Equal amounts (50,000 cpm) of the
5'-end-labeled 150-bp PCR fragment containing the promoter region of
argF were hybridized with RNA extracted from cultures grown
in minimal medium (lane 1) and minimal medium supplemented with
arginine (lane 2). After precipitation and hybridization, S1 nuclease
activity proceeded. The position of the transcript is indicated by the
arrows; the sequence shown is of the noncoding strand. Lanes G, A, T,
and C represent chain-terminating DNA-sequencing reactions of the
noncoding strand. (B) Nucleotide and deduced amino acid sequences of a
portion of the T. thermophilus argF gene and its promoter
region. The arrows indicate the transcriptional start sites. Also, 35
and 10 promoter sequences are indicated and in bold type. Sequences
showing similarity to the E. coli consensus Arg box are
underlined. Boxed sequences were protected from DNase I treatment.
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In vitro binding of the E. coli arginine repressor to
the Thermus argF promoter region.
Thermus argF promoter sequences overlapping the 35 and
10 elements exhibit similarity to the palindromic sequence of the
E. coli consensus Arg box; the sequence overlapping the 35
region shows up to 62% identity (Fig.
4). We studied the interaction of pure
E. coli ArgR and B. stearothermophilus AhrC with
the promoter region of Thermus argF and ORF4 by mobility shift electrophoresis and footprinting. In the presence of arginine, E. coli ArgR binds to the promoter region of Thermus
argF (Fig. 4), where it protects a 29-nucleotide region from DNase
I digestion (Fig. 5). This region
contains the first putative Arg box covering the 35 region and part
of the second Arg box (Fig. 4). The latter is not completely protected
by E. coli ArgR, probably because of the 7-bp spacing of the
two boxes (3). The B. stearothermophilus Arg
repressor did not interact with the argF promoter. No
arginine repressor was reported so far in Thermus, but in
the genome of D. radiodurans there is an ORF encoding a
protein clearly homologous to the Arg repressor characterized in
enteric bacteria and bacilli. Thus, it appears that Thermus
argF is controlled by such a repressor. No specific interaction
between the E. coli and B. stearothermophilus arginine repressors could be demonstrated with the Thermus
ORF4 promoter region (data not shown). Further studies should show whether repression of argF and induction of ORF4 involve the
same Thermus protein.
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FIG. 4.
Mobility shift experiments for the Thermus
argF promoter region with E. coli ArgR and
B. stearothermophilus AhrC in the absence (A) and presence
(B) of arginine. Lanes l, no added protein; lanes 2, argF
promoter fragment incubated with B. stearothermophilus AhrC;
lanes 3, argF promoter fragment incubated with E. coli ArgR.
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FIG. 5.
DNase I footprinting of the 210-bp fragment of the
Thermus argF promoter region protected by the E. coli arginine repressor. Lanes: G, A, T, and C, sequencing
ladders; 1, DNase I reference ladder (without E. coli ArgR);
2, DNase I treatment in the presence of E. coli ArgR. The
approximately 29-bp-long protected stretch is indicated by a bar.
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Translation initiation signals.
The argF mRNA is
devoid of a Shine-Dalgarno (SD) sequence. Some mRNAs lacking SD
sequences were found in bacteria, archaea, eukarya (35), and
eukaryotic organelles (21), suggesting that information
within the coding sequence may be sufficient to signal the
translational start in diverse biological systems. In several genes of
E. coli and of E. coli bacteriophages,
Sprengart et al. (29) identified sequences complementary to
nucleotides 1469 to 1483 of 16S rRNA. This region is exposed on the
ribosome surface and expected to come into contact with the 3' end of
16S RNA. Mutations were found in the E. coli gln gene which
increase the complementarity of downstream sequences to 16S rRNA and
result in higher translational activity (8). We found that
64% of 130 analyzed genes from Thermus (including
argF) showed such a downstream box, where at least 6 consecutive nucleotides or at least 8 nucleotides out of 12 complemented the nucleotide-1392-to-1409 region of Thermus
16S rRNA (Fig. 6). This sequence differs
from the one mentioned by Sprengart et al. (29, 30) but is
situated in a similarly exposed stem-loop structure (Fig. 6). This
consensus sequence was found in Thermus mRNAs containing an
SD sequence as well as in mRNAs lacking one. These observations suggest
that an mRNA-rRNA interaction at the level of these downstream
sequences could in some cases compensate for absent SD boxes or
reinforce interactions with existing ones.
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FIG. 6.
(A) Sequences at the 3' ends of Thermus and
E. coli 16S rRNAs. The region of the 16S RNA molecule
complementary to sequences downstream of the AUG start codon of several
Thermus and E. coli genes is indicated by boxed
nucleotides. (B) Examples of "downstream boxes" in genes from
Thermus. Sequences complementary to the region of 16S rRNA
shown above are in bold type and underlined. The SD sequence is
underlined, and the start codon is indicated by a grey box
throughout.
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Concluding remarks. Clusters of functionally related genes
containing apparently unrelated ORFs have been reported
in other
organisms (
7,
11). It was claimed that the inclusion
of
genes in unrelated operons may be selectively neutral if the
latter are
constitutive (
16). This is clearly not the case for
ORF1,
which is coregulated with
argF,
argC, and
argJ. One may
argue that the product of coregulated ORFs
could stabilize enzymes
encoded by the same polycystronic mRNA
(
13). However, in
Thermus,
the
argF
and
argJ gene products appear intrinsically stable (
1,
27). Another possibility would be that the unknown ORF product
is
involved in the formation of multienzyme complexes channeling
arginine
metabolic precursors (
17,
32). The situation in
D. radiodurans, the closest known relative of
Thermus, is
also intriguing.
Deinococcus argF is followed at 8 bp by a
homologue of
mutT (encoding
an enzyme degrading 8-oxo-dGTP).
This
mutT gene overlaps
argC,
itself followed at
4 nucleotides by the gene for glycerol-3-phosphate
dehydrogenase
(
33). In
Deinococcus, however, the regulation
of
those genes has not yet been studied. We feel that the inclusion
of unknown or already identified "foreign" genes into defined
operons is a neglected area of molecular physiology in need of
further
investigation.
Nucleotide sequence accession number.
The nucleotide sequence
data reported in this paper are available in the EMBL Nucleotide
Database under accession number Y18353.
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ACKNOWLEDGMENTS |
This work was supported by a grant from the Flanders Scientific
Foundation for Scientific Research (FWO).
We thank D. Charlier for the gift of pure arginine repressor and are
grateful for the excellent help of Nadine Huysveld.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Flanders
Interuniversity Institute for Biotechnology (VIB), Free University of
Brussels (VUB), and Research Institute J. M. Wiame, E. Grysonlaan
1, 1070 Brussels, Belgium. Phone: 32 2 5267275. Fax: 32 2 5267273. E-mail: ceriair{at}ulb.ac.be.
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Journal of Bacteriology, October 2000, p. 5911-5915, Vol. 182, No. 20
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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