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Appl Environ Microbiol, February 1998, p. 763-767, Vol. 64, No. 2
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Cloning and Nucleotide Sequencing of a
Staphylococcus aureus Gene Encoding a
Branched-Chain-Amino-Acid Transporter
Uriwan
Vijaranakul,
Anming
Xiong,
Katherine
Lockwood, and
R. K.
Jayaswal*
Department of Biological Sciences, Illinois
State University, Normal, Illinois 61790-4120
Received 11 August 1997/Accepted 4 December 1997
 |
ABSTRACT |
We recently characterized a transposon-induced NaCl-sensitive
mutant of Staphylococcus aureus (U. Vijaranakul, M. J. Nadakavukaren, D. O. Bayles, B. J. Wilkinson, and R. K. Jayaswal, Appl. Environ. Microbiol. 63:1889-1897, 1997). To further
characterize this mutant, we determined the nucleotide sequence at the
insertion site of the transposon on the S. aureus
chromosome. Nucleotide sequencing revealed a 1,326-bp open reading
frame (ORF442) encoding a hydrophobic 442-amino-acid polypeptide with a
calculated molecular mass of 49,058 Da. The hydrophilicity profile of
the gene product revealed the existence of 12 hydrophobic domains
predicted to form membrane-associated 
-helices. Comparison of the
amino acid sequence of ORF442 with amino acid sequences in the GenBank
database showed extensive homology with the branched-chain-amino-acid
transport genes of gram-positive and gram-negative bacteria. This is
the first brnQ gene in staphylococci to be described.
| |
TEXT |
Staphylococcus aureus is
one of the most halotolerant, nonhalophilic bacteria. It causes a
variety of diseases, ranging from simple skin infections to
life-threatening diseases such as endocarditis and food poisoning. One
of the distinguishing characteristics of S. aureus is its
ability to grow in the presence of up to 3.5 M NaCl. It has been
reported that high concentrations of NaCl inhibit growth
(1), decrease toxin synthesis (22), stimulate synthesis of degradative enzymes (17), increase cell size,
and reduce the length of the interpeptide bridge of peptidoglycan (26). However, the mechanisms by which NaCl causes the above physiological and molecular changes in S. aureus are not
known.
Osmoregulation in gram-negative bacteria, mainly Escherichia
coli and Salmonella typhimurium, has been studied
extensively. A number of osmotically regulated genes, such as
envZ and ompR, the kdpABC and
proU operons, the mal and bet
regulons, proQ, phoE, otsB,
treA, osmB, rpoS, and algD,
have been reported (5, 8, 12). In contrast, there are very
few reports of osmotically regulated genes in gram-positive bacteria.
In Bacillus subtilis, DegS-DegU (a two-component system) is
involved in sensing salt stress (17). Another regulatory
gene, clpC (15), that acts downstream from
DegS-DegU and ComP-ComA in the regulatory cascade is induced by
multiple stresses, including heat shock, ethanol, salt stress, oxygen
limitation, and nutrient deprivation (11). Mutations in
these regulatory genes lead to increased levels of expression of the
alternative sigma factor 
B. The expression of genes
controlled by B, such as the ect gene and the
sigB operon, which codes for B and its
associated regulatory proteins, was shown to be dramatically induced by
salt stress (4). Thus, this sigma factor plays an important
role in the increased synthesis of general stress proteins and some
salt-specific stress proteins (10). Recently, the
sigB operon encoding an alternative sigma factor of S. aureus was cloned and sequenced (16, 28). Whether the
sigB operon is involved in salt tolerance in S. aureus remains to be determined.
In an effort to investigate the molecular mechanisms and genes involved
in the NaCl tolerance of S. aureus, we isolated
NaCl-sensitive mutants by transposon mutagenesis. Recently, one of the
NaCl-sensitive mutants was physiologically characterized
(27). This NaCl-sensitive mutant showed a pleiotropic
phenotype in high salt concentrations. It exhibited normal growth rate
and cell division in medium containing a low concentration of NaCl.
However, mutant cells grown in medium containing a high concentration
of NaCl showed a very long lag phase and increased cell size with the
presence of multiple septa. To further characterize this mutant, we
cloned and sequenced the mutated gene with the flanking sequences of
the transposon (Tn) at the insertion site of the mutant. In this study,
we report the cloning, sequencing, and analysis of a gene,
brnQ, encoding a branched-chain-amino-acid transport protein
of S. aureus. The mutation in brnQ caused the
NaCl-sensitive phenotype of S. aureus.
Cloning and nucleotide sequence determination of the region
flanking the mutated gene.
A genomic library of the NaCl-sensitive
mutant was constructed in cosmid pCP13 (6). The mutant
library was screened by colony hybridization to obtain clones
containing Tn sequences. Four of 2,000 cosmid mutant clones showed
strong hybridization with the radiolabeled Tn917 probe.
Southern blot analysis showed that a 6-kb EcoRI fragment of
the positive clones hybridized with the Tn probe. This fragment was
subcloned into the EcoRI site of plasmid pTZ18R and
designated pTSS7.7. Sequencing was performed by either a radioactive
protocol with [-32P]dCTP (ICN Biomedicals, Inc., Costa
Mesa, Calif.) and Taq polymerase (U.S. Biochemical Corp.,
Cleveland, Ohio) or a nonradioactive dye terminator cycle sequencing
protocol with AmpliTaq DNA polymerase (Perkin-Elmer, Foster
City, Calif.) and an automated sequencer, the ABI Prism 310 genetic
analyzer (Perkin-Elmer). Nucleotide sequencing of the 6-kb
EcoRI fragment with M13 primers and internal primers of the
Tn revealed that the cloned fragment had a 2,678-bp region of the Tn
and about 3.3-kb of the S. aureus genome.
Cloning and nucleotide sequence determination of the wild-type
allele.
To obtain the wild-type allele of the mutated gene, a
400-bp region of DNA flanking Tn917 was used as a probe to
screen the cosmid library of RN450, which was the parent strain. Six
positive clones obtained by colony hybridization were further subjected to Southern blot hybridization. A 4.8-kb fragment from one of the
cosmid clones, CRN4, which showed strong hybridization with the probe
was subcloned into pTZ18R and designated pTRN5.
The nucleotide sequence analysis of 1.9 kb (the mutation was localized
within this fragment) of the 4.8-kb fragment revealed one complete open
reading frame (ORF) of 1,326 bp. This ORF was designated ORF442. As
shown in Fig. 1, the putative promoter
sequences (
10 and 35) were identified upstream of the initiation
site and a termination sequence was located downstream of ORF442.
Comparison of the nucleotide sequences of clones pTSS7.7, pTRN5, and
CRN4 showed the Tn917 insertion site at 377 nucleotides
downstream from the initiation codon of ORF442.
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FIG. 1.
Nucleotide sequence of the 1.9-kb chromosomal DNA
fragment containing brnQ. The predicted amino acid sequence
of BrnQ is shown in single-letter code below the nucleotide sequence.
The putative promoter elements (10 and 35) are underlined. The
transcription start site is indicated by +1.
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Analysis of the protein product(s) encoded by ORF442.
The
deduced translation product of ORF442 is a protein with a calculated
molecular mass of 49,058 Da and a pI of 9.96. As shown in Table
1, among 442 amino acids, there are 258 nonpolar amino acids (58.37%), 133 polar amino acids (30.1%), 13 acidic amino acids (2.94%), and 38 basic amino acids (8.6%).
Analysis of the ORF442 transcript.
Total RNA from the
salt-sensitive mutant and parent strains was isolated as described by
Gustafson et al. (9). Ten micrograms of total RNA was
electrophoresed on formaldehyde agarose gels (1.0%) and transferred to
nitrocellulose membranes. The blot was probed with a radiolabeled
2.5-kb DNA fragment encompassing ORF442. Northern blot analysis
revealed that ORF442 codes for a transcript of about 1.3 kb (Fig.
2A). To define the transcription unit
more precisely, the 5' end of the transcript was mapped with the avian myeloblastosis virus reverse transcriptase system (Promega). An 18-base
oligonucleotide (5'-GACCCTATCCAATCCGAG-3') specific to the
coding region was annealed with total RNA and extended in a primer
extension assay. A sequence ladder was generated with the same primer
on a 4.8-kb fragment and was coelectrophoresed to determine the
position of the transcription start site. The primer extension showed
that the first nucleotide of the mRNA was a T residue corresponding to
position 354 in the DNA sequence (Fig. 2B). The transcript initiates
from 1 nucleotide upstream of the predicted translation initiation
site. Thus, the transcript does not contain the Shine-Dalgarno
sequences usually necessary for translation initiation. Although it is
an unusual transcript, similar types of transcripts have been reported
earlier (23). The mechanism by which ribosomes bind to the
mRNA is not known.
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FIG. 2.
Transcript analysis of the brnQ gene. (A)
Northern blot analysis of ORF442. Ten micrograms of an RNA sample was
separated electrophoretically and transferred by Northern blotting onto
a membrane. The blot was probed with a radiolabeled 2.5-kb DNA fragment
encompassing brnQ. The sizes of the ribosomal RNAs are
marked with arrowheads, and the BrnQ product is indicated by an arrow.
(B) Mapping of the 5' end of the brnQ transcript by primer
extension analysis. Total RNA from the parent strain was hybridized
with an oligonucleotide complementary to the mRNA of the
brnQ locus and extended by avian myeloblastosis virus
reverse transcriptase (lane P). Lanes T, G, C, and A correspond to a
dideoxy sequencing reaction performed with the same primer. The
sequence encompassing the initiation start site (marked by an
arrowhead) is enlarged.
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|
Sequence homology.
When the nucleotide sequence of ORF442 was
compared to known sequences by using National Center for Biotechnology
Information BLAST searches, 57% identity to braB of
Clostridium perfringens and 72% identity to brnQ
of S. typhimurium were found.
The predicted amino acid sequence of ORF442 was used to conduct a
homology search. Significant homology of the deduced amino
acid
sequence of ORF442 to the branched-chain-amino-acid carrier
gene
(
brnQ) of gram-positive and gram-negative bacteria was
observed.
The deduced amino acid sequence of the translation product of
ORF442 revealed identity to BraB of
Pseudomonas aeruginosa
(33.9%)
(
13), BrnQ of
B. subtilis (33.5%)
(
3), BraB of
C. perfringens (31.6%)
(
20), BrnQ of
Lactobacillus delbrueckii (30.9%)
(
24),
BrnQ of
S. typhimurium (27.6%)
(
21), BrnQ of
E. coli (28%),
and BraZ of
P. aeruginosa (27.7%) (
14). The amino acid
sequences
are extensively conserved over the entire region (Fig.
3). The
identity at the N terminus (first
100 amino acids) is particularly
prominent, at 45, 45, 42, 44, 41, and
38% between
S. aureus and
BraB of
P. aeruginosa,
BrnQ of
B. subtilis, BraB of
C. perfringens,
BrnQ
of
L. delbrueckii, BrnQ of
E. coli, and BrnQ of
S. typhimurium,
respectively. Therefore, the gene contained
by ORF442 was designated
brnQ of
S. aureus.
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FIG. 3.
Alignment of the predicted amino acid sequences of BrnQ
of S. aureus (Sa), BrnQ of B. subtilis (Bs), BraB
of C. perfringens (Cp), BrnQ of L. delbrueckii
(Ld), BrnQ of S. typhimurium (St), BraB of P. aeruginosa (Pa), BrnQ of E. coli (Ec), and BraZ of
P. aeruginosa (Pa) by the Clustal W alignment program
described by Thompson et al. (25). Identical amino acid
residues are shown in boldface type, and similar amino acid residues
are indicated by plus signs. The protein sequences were aligned by the
insertion of gaps ( ) to obtain maximum sequence identity. The
following amino acids are similar: A, S, and T; D and E; N and Q; R and
K; and I, L, M, V, F, Y, and W.
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|
Further comparisons of the BrnQ protein of
S. aureus with
other branched-chain-amino-acid carrier proteins showed striking
similarities with respect to molecular weight, pI, and percent
composition of various amino acids. Hydrophilicity profile comparisons
of BrnQ of
S. aureus with those of the
branched-chain-amino-acid
transport carriers also showed strong
structural similarities
(data not shown). The hydrophilicity profile of
BrnQ of
S. aureus is highly similar to those reported for
other gram-positive and
gram-negative bacteria. As shown in Fig.
4, BrnQ of
S. aureus contains
approximately 12 membrane-spanning segments flanked by
short
hydrophilic stretches. Thus, BrnQ is extremely hydrophobic.
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FIG. 4.
Hydrophilicity profile of the predicted amino acid
sequence of BrnQ of S. aureus. The x axis
represents amino acid residues measured from the N terminus
(hydrophilicity window size, 7). The y axis is an arbitrary
scale of hydropathy described previously (18), as modified
to represent hydrophilicity (7).
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|
Complementation analysis.
To complement the mutation of a
salt-sensitive mutant, a 4.8-kb fragment containing brnQ was
subcloned into the shuttle vector pCU1 (2). The resultant
plasmid, designated pCUT5, was electroporated into the salt-sensitive
mutant. The transformants were tested for the ability to grow in
defined medium containing 2.5 M NaCl. All of the transformants were
able to grow on solid media containing 2.5 M NaCl. When the
transformants were grown in liquid culture, they showed a reduced lag
phase (~30 h) compared to the mutant strain (>60 h). However, the
lag phase was still longer in the transformants than that observed in
the wild-type strain (~12 h) grown under identical conditions. Thus,
the cloned gene partially complemented the mutation in the
trans position. The reasons that only partial
complementation was observed are unknown.
ORF442 encodes a highly hydrophobic polypeptide of a calculated
molecular mass of 49 kDa and a pI of 9.96. The polypeptide
has high
homology to the Na
+-dependent branched-chain-amino-acid
carriers in
P. aeruginosa (
13,
29) and
S. typhimurium (
19). In addition, the polypeptide
has high
homology to the branched-chain-amino-acid carriers in
B. subtilis,
C. perfringens (
20),
L. delbrueckii (
24), and
E. coli. The striking
identity of the deduced amino acid sequences
throughout the entire
length suggests that the branched-chain-amino-acid
carriers in these
organisms are highly conserved. Based on these
analyses, we propose
that the cloned gene is a branched-chain-amino-acid
carrier gene
(
brnQ) of
S. aureus. BrnQ of
S. aureus, BrnB of
P. aeruginosa and
C. perfringens, and BrnQ of
S. typhimurium,
B. subtilis,
L. delbrueckii, and
E. coli are
similar in size, pH
(basic), and hydropathy profiles. BrnQ of
S. aureus, which is
an extremely hydrophobic protein, contains 12 membrane-spanning
segments flanked by short hydrophilic stretches, as
reported for
other bacteria. These properties are typical of integral
membrane
transport proteins. The most abundant amino acid of the BrnQ
protein
of
S. aureus is isoleucine (67 of 442), followed by
leucine (62
of 442). Although it has been suggested that in
S. aureus, leucine,
isoleucine, and valine use the same transporter,
there is no report
on the branched-chain-amino-acid transport systems
in
S. aureus.
Therefore, this is the first report of a
branched-chain-amino-acid
carrier (BrnQ) in
S. aureus.
To explain the pleiotropic phenotype of the NaCl-sensitive mutant
reported earlier (
27), we propose the following model
for
the transport of branched-chain amino acids in
S. aureus.
There are at least two independent branched-chain-amino-acid transport
systems with respect to substrate specificity and affinity. The
two
systems are a sodium-coupled, branched-chain-amino-acid transport
system and a sodium-independent transport system, which is sensitive
to
environmental stress conditions such as osmolarity, pH, and
temperature. Under nonstress conditions, branched-chain amino
acids are
transported through both systems, whereas under stress
conditions, only
the sodium-coupled transport system functions.
Under low osmotic
conditions (low sodium ions), the mutant shows
normal growth and cell
division, like the parent strain. In the
presence of high sodium ion
concentrations, the mutant shows a
very long lag phase with multiple
septa. This may be due to the
mutation in the sodium-dependent system
and the inability of the
sodium-dependent system to transport
branched-chain amino acids
from the medium. Similarly, at low pH and
high temperature, the
growth of the mutant is retarded. This also may
be due to the
sensitivity of the sodium-independent system to transport
branched-chain
amino acids. To test this hypothesis, we are currently
characterizing
the gene and gene product with respect to substrate
specificity
and the kinetics of the uptake of
[
14C]leucine, [
14C]isoleucine, and
[
14C]valine.
Nucleotide sequence accession number.
The 4.8-kb DNA fragment
of which ORF442 was a part was sequenced, and the nucleotide data was
deposited in the GenBank database under accession no. U87144.
| |
ACKNOWLEDGMENTS |
We express our gratitude to Brian J. Wilkinson for helpful
discussion and Sean Arkins and David Williams for critical reading of
the manuscript.
This study was supported by a student stipend from the American Heart
Association Illinois Affiliate to U.V.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Biological Sciences, Illinois State University, Normal, IL 61790-4120. Phone: (309) 438-5128. Fax: (309) 438-3722. E-mail:
drjay{at}rs6000.cmp.ilstu.edu.
| |
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Appl Environ Microbiol, February 1998, p. 763-767, Vol. 64, No. 2
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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