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Previous Article | Next Article 
Journal of Bacteriology, August 2000, p. 4654-4657, Vol. 182, No. 16
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
3-Deoxy-D-manno-oct-2-ulosonic
Acid (Kdo) Transferase of Legionella pneumophila Transfers
Two Kdo Residues to a Structurally Different Lipid A Precursor of
Escherichia coli
Werner
Brabetz,*
Christiane E.
Schirmer, and
Helmut
Brade
Research Center Borstel, Center for Medicine
and Biosciences, Division of Medical and Biochemical Microbiology,
D-23845 Borstel, Germany
Received 22 February 2000/Accepted 25 May 2000
 |
ABSTRACT |
The 3-deoxy-D-manno-oct-2-ulosonic acid
(Kdo) transferase gene of Legionella pneumophila was cloned
and sequenced. Despite remarkable structural differences in lipid A,
the gene complemented a corresponding Escherichia coli
mutant and was shown to encode a bifunctional enzyme which transferred
2 Kdo residues to a lipid A acceptor of E. coli.
| |
TEXT |
Lipopolysaccharides (LPS) of
gram-negative bacteria consist of a lipid component, termed lipid A,
and a covalently bound polysaccharide which is subdivided into a lipid
A proximal core oligosaccharide and, in smooth-type bacteria, a lipid A
distal O antigen (21). The LPS of Legionella
pneumophila, the causative agent of Legionnaires' disease
(8), shows unique structural characteristics such as unusually long fatty acids attached to the lipid A and extremely hydrophobic sugar residues within the outer core oligosaccharide and
the O antigen (14-16, 26). Due to these peculiarities of the LPS, L. pneumophila possesses a very hydrophobic cell
surface which may contribute to the spread and virulence of this
microorganism (19, 26).
The inner core oligosaccharide of L. pneumophila LPS
is characterized by a
3-deoxy-D-manno-oct-2-ulosonic acid (Kdo)
disaccharide [
-Kdo-(2
4)--Kdo-(26)] linked to lipid A
which is conserved within many gram-negative bacteria and is essential
for microbial growth (4, 21, 25). Remarkably, as shown for
Escherichia coli (3), Acinetobacter
spp. (6), and Chlamydiaceae (5, 18,
20), there is only one enzyme necessary for the transfer of all
Kdo residues, even in different linkages. Therefore, these transferases
are multifunctional.
The carbohydrate backbone of the lipid A of L. pneumophila
is composed of a biphosphorylated 
(16)-linked disaccharide of 2,3-diamino-2,3-dideoxy-D-glucose substituting for
glucosamine, which is present in the majority of structurally
characterized LPS (21). Consequently, all fatty acids are
amide bound to positions 2, 2', 3, and 3' in the lipid A of L. pneumophila (26). To date, Kdo transferases from
bacteria containing this structural element have not been studied.
Bacterial strains and growth conditions.
L. pneumophila
serogroup 1 (strain Philadelphia 1, ATCC 33152) was grown at 37°C on
buffered charcoal yeast extract agar (Oxoid). E. coli
strains and Corynebacterium glutamicum R163 (17)
were cultivated at 37 or 30°C, respectively, in 2× YT
(23) supplemented with the appropriate antibiotics (20 mg of
kanamycin/liter and 100 mg of ampicillin/liter, the latter applied only
to E. coli).
Cloning and sequence analysis of the waaA gene of
L. pneumophila.
The three degenerate primers +880-1
(5'-GTNCCNMGNCAYNYNGAAA-3'), +880-2
(5'-GTNCCNMGNCAYNYNGAAG-3'), and 
1010
(5'-TCNARNRRRTTRTGNCCNC-3') were designed based on two
stretches of identical amino acids between known WaaA sequences and
were used in PCR with chromosomal DNA from L. pneumophila as
described previously (6). A corresponding DNA fragment of
146 bp was obtained, blunt ended, and ligated into the SrfI
site of pCR-ScriptAmpSC(+) (Stratagene) to produce plasmid pLPO1.
The plasmid was transformed into E. coli
XL1BlueMRF'Kanr (Stratagene), and its insert was sequenced.
The DNA fragment was then used as a probe in Southern experiments
to clone a 3.5-kb StuI fragment from the chromosome of
L. pneumophila into the SmaI site of pMBL19
(22). The corresponding plasmid was termed pLPO28, and both
strands of the DNA insert were sequenced.
Computer analysis (GeneWorks; Intelligenetics) of the nucleotide
sequence of the cloned insert revealed two complete open reading
frames, oriented in opposite directions (Fig.
1). These open reading frames were
homologous to waaA and djlA, respectively, as
shown by a TBLASTN (1) search at the National Center for Biotechnology Information. The Kdo transferase was encoded by a DNA
segment of 1,260 bp starting with an AUG and terminating with a UAG
codon. Its deduced amino acid sequence was aligned with all known
complete WaaA proteins by using the programs ClustalX 1.8 (24) and GeneDoc 2.5 (K. B. Nicholas and H. B. Nicholas, Jr., 1997 [http://www.cris.com/~Ketchup/genedoc.shtml])
(Fig. 2). All sequences shared in total
5% identical and 9.8% similar (according to the Dayhoff-PAM250
matrix) amino acids, respectively. More than 50% of the conserved
residues matched into a segment of approximately 140 amino acids within
the C-terminal half of all Kdo transferases which defines a
glycosyltransferase group 1 domain (Pfam database accession number
PF00534) (2).
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FIG. 1.
Cloned and sequenced DNA fragment of L. pneumophila serogroup 1. The positions (nucleotide numbers in
parentheses) of some restriction sites are shown. waaA, Kdo
transferase gene; djlA, dnaJ-like A
gene; orf1' and orf2', putative open reading
frames which showed no homology to known genes.
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FIG. 2.
Comparative analysis of the amino acid sequences of WaaA
proteins. On top, the consensus of all aligned complete amino acid
sequences of Kdo transferases is diagrammed to scale (with the N
terminus on the left). Thick segments correspond to more-conserved
regions of the protein. The dashed line represents an insertion of 41 amino acids which is present only in the N terminus of WaaA from
Rickettsia prowazekii. Vertical lines mark the positions of
highly conserved amino acids. A glycosyltransferase group 1 domain
(Pfam database accession number PF00534) is shaded, and the amino acid
sequence alignment of the central part of this region is shown in
detail at the bottom. Dashes represent gaps introduced to optimize the
alignment. Amino acids which are identical for at least 75% of all
sequences are shaded. Horizontal arrows indicate the regions which were
used to design the totally degenerate primers. Abbreviations of species
names (with GenBank accession numbers of the corresponding DNA
sequences given in parentheses) are as follows: Lpn, L. pneumophila (AJ011775); Eco, E. coli (M60670); Sma,
Serratia marcescens (U52844); Kpn, Klebsiella
pneumoniae (AF146532); Hin, H. influenzae (U32748);
Aba, Acinetobacter baumannii (Z96925); Aha,
Acinetobacter haemolyticus (Z96927); Bbr, Bordetella
bronchiseptica (AJ007747); Bpe, Bordetella pertussis
(X90711); Chs, Chlamydophila psittaci (X69476); Cha,
Chlamydophila abortus (AF111203); Chp, Chlamydophila
pneumoniae (Z31593); Ctr, Chlamydia trachomatis
(Z22659); Hpy, Helicobacter pylori (AE000604); Aeo,
Aquifex aeolicus (AE000684); Rpr, R. prowazekii
(AJ235269).
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|
Subcloning of waaA.
The waaA gene was
amplified from pLPO28 using Pfu DNA polymerase and the
specific oligonucleotides LP1
(5'-TGTGTTTGGATCCTGTTTATGC-3' [the
BamHI site is underlined and the start codon is boldfaced]) and LP2 (5'-GAATTTGTCGACAAGCTAATATCCCAA-3'
[the SalI site is underlined, and the stop codon is
boldfaced]), cut with BamHI and SalI, and
ligated between the corresponding restriction sites of the E. coli-C. glutamicum expression vector pCB20 (6) to produce plasmid pLPO10. The kanamycin resistance gene of pLPO10 was
further replaced by an ampicillin gene. For this purpose a 1,280-bp
SmaI-PstI fragment from pLPO10, a 1,190-bp
BglI-PstI fragment from pBTac2 (11),
and a 2,042-bp BglI-BalI fragment from pBR322
(10) were ligated to produce plasmid pLPO11.
Complementation of an E. coli waaA mutant.
E.
coli CJB26 (4), which harbors a knockout insertion of a
kanamycin resistance gene within the essential chromosomal
waaA and is complemented by an intact copy of the gene
encoded on a temperature-sensitive plasmid, was transformed with pLPO11
and selected at 44°C with ampicillin and kanamycin. One positive
clone, termed E. coli WBB54, was confirmed by Southern
hybridization and PCR (data not shown) and showed the same growth
behavior and similar LPS on a silver-stained sodium dodecyl
sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) gel
(6) as strain CJB26 (data not shown).
Activity of the cloned Kdo transferase.
pLPO10 was transformed
into the gram-positive bacterium C. glutamicum R163
(17), which made it possible to study the enzymatic activity
of the cloned transferase without interference by host cell enzymes
(6, 18). Cell extracts were prepared from recombinant strains, and the Kdo transferase assay was performed under standard conditions, as described previously (6). Briefly, the enzyme reaction mixture (20 µl) contained Tris-HCl (50 mM; pH 7.5),
MgCl2 (10 mM), Triton X-100 (3.2 mM), Kdo (2 mM), CTP (5 mM), the synthetic biphosphorylated tetraacyl lipid A precursor 406 (0.1 mM) (13), CMP-Kdo synthetase (1.67 pkat; prepared from
C. glutamicum R163/pJKB14 [6]), and cell
extracts (40 µg of protein). The in vitro test mixtures were
incubated for 30 to 60 min at 37°C, and reactions were stopped by
spotting 5 µl onto silica-60 thin-layer chromatography (TLC) plates
(Merck). TLC plates were developed with a solvent consisting of
chloroform-pyridine-88% formic acid-water in a ratio of 30:70:16:10
(by volume). Radioactive [4'-32P]-labeled 406 was
synthesized from the monophosphorylated tetraacyl lipid A precursor 405 as described previously (9) by using lipid A 4'-kinase
prepared from E. coli BLR(DE3)/pLysS/pJK2 (12). The specific activity was adjusted with unlabeled 406 to
approximately 15,000 to 20,000 cpm nmol
1. Radioactive
products were detected and quantified with a PhosphorImager and
ImageQuant software (Molecular Dynamics).
The cloned Kdo transferase from L. pneumophila was able to
transfer up to 2 Kdo residues to compound 406 (Fig. 3A). The enzyme activity clearly depended on the presence of Kdo and CMP-Kdo synthetase (Fig. 3A, lanes 5 to 7). CTP could be
provided, but in limiting amounts, from cell-free lysates of
recombinant C. glutamicum (Fig. 3A, lane 8). A complete
reaction mixture with a cell extract from C. glutamicum
R163/pCB20 (6) was used as a negative control, and no
conversion of [4'-32P]-radiolabeled 406 was observed in
this case (data not shown). The reaction products of the cloned WaaA
had the same Rf values as isolated,
radioactively labeled standards of Kdo-406 and Kdo2-406 (Fig. 3A) (reaction products of in vitro assays with the recombinant Kdo transferases of E. coli and Haemophilus
influenzae were purified from TLC plates as described in reference
9). In addition, the transfer of Kdo could be
confirmed by Western blot analysis of the same TLC plate (6,
18) by using the Kdo-specific monoclonal antibody A20
(7) (Fig. 3B). Furthermore, this technique clearly allowed
us to distinguish between a nonspecific impurity present in the
radioactively labeled acceptor preparation (see Fig. 3A, lanes 1, 6, and 7) and Kdo-406, which also differed slightly in its
Rf value. In addition, 5-µl samples were
withdrawn from a reaction mixture (40 µl) at different time points
and reactions were stopped with 10 µl of ice-cold ethanol. Aliquots
(12 µl) of the inactivated samples were then separated by TLC, and
reaction products were detected (Fig. 4A)
and quantified (Fig. 4B) as described above. A continuous increase in
Kdo2-406, the major product of the enzyme reaction, was
observed. The specific activity for its formation within the
corynebacterial cell extract was calculated as 1.1 nmol
min1 mg of protein1 at 37°C. In addition,
Kdo-406 was formed in small amounts during the first 5 min until a
constant level was achieved. A reaction product with 1 Kdo residue was
also reported by Belunis et al. (3) as a minor in vitro
by-product of the bifunctional WaaA of E. coli, and similar
reactivities were obtained for a cell extract of a recombinant C. glutamicum strain which expressed the cloned enzyme of E. coli (reference 6 and data not shown).
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FIG. 3.
In vitro activity of the cloned Kdo transferase of
L. pneumophila. The enzyme assay was performed with cell
extracts of C. glutamicum/pLPO10 as described in the text.
Detection of the radioactively labeled substrates and reaction products
was performed after TLC with a PhosphorImager (A) or after blotting
from the TLC plate onto a nitrocellulose membrane by immunostaining
with the Kdo-specific monoclonal antibody A20 (B). The positions of the
detected compounds are indicated on the right. Lane 1, isolated
compound 406; lane 2, mixture of isolated compounds 406 and Kdo-406;
lane 3, isolated Kdo-406; lane 4, isolated Kdo2-406; lane
5, complete reaction mixture with recombinant WaaA of L. pneumophila; lane 6, assay without Kdo; lane 7, assay without
CMP-Kdo synthetase; lane 8, assay without CTP.
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FIG. 4.
Time course of the enzyme reaction with the cloned Kdo
transferase of L. pneumophila. Kinetic experiments were
performed as described in the text. The reaction products were
separated by TLC and were detected (A) and quantified (B) by using a
PhosphorImager and ImageQuant software (Molecular Dynamics). The
specific enzyme activity for the formation of Kdo2-406
within cell extracts of recombinant C. glutamicum strains
was determined as 1.1 nmol · min1 · mg of
protein1. The positions of the detected compounds in
panel A are indicated on the right. Symbols in panel B:  , compound
406;  , compound Kdo-406;  , compound Kdo2-406.
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In conclusion, waaA of L. pneumophila encodes a
bifunctional Kdo transferase that is able to complement a corresponding
E. coli mutant and to transfer 2 Kdo residues to compound
406. The overall enzyme reaction did not depend on specific
structural prerequisites of the lipid A of L. pneumophila
(26). Neither 2,3-diamino-2,3-dideoxy-D-glucose,
which is present in lipid A of L. pneumophila and
substitutes for glucosamine in compound 406, nor
2,3-dihydroxy-12-methyl tridecanoic acid, 2,3-dihydroxytetradecanoic acid, and 3-hydroxyoctadecanoic acid, which were identified in amide
linkages in lipid A of L. pneumophila and substitute for 3-hydroxytetradecanoic acid in compound 406, were required for the
enzyme activity. However, differences in the relative reactivity of the
enzyme between the applied substrate and the native lipid A acceptor of
L. pneumophila, which is not yet available, may exist. The
results presented in this study further support the hypothesis that, in
general, Kdo transferases share a common acceptor motif for catalytic
activity, which is located in the carbohydrate backbone of lipid A and
comprises at least a (16)-linked disaccharide of a
gluco-configured aminosugar with a phosphate group in
position 4' of the nonreducing sugar moiety (3, 6, 9, 18).
This basic structure could serve as a starting point for the rational design of new chemotherapeutics which may inhibit all LPS-specific Kdo transferases.
Nucleotide sequence accession number.
The sequence of the
cloned chromosomal DNA fragment from L. pneumophila has been
submitted to the EMBL nucleotide database and is available under
accession number AJ011775.
| |
ACKNOWLEDGMENTS |
This work was financially supported by the Deutsche
Forschungsgemeinschaft (SFB470/grant A1 to H.B.).
We thank P. Kosma (Vienna, Austria) for synthetic Kdo, S. Kusumoto
(Osaka, Japan) for synthetic 405 and 406, and C. R. H. Raetz
(Durham, N.C.) for E. coli BLR (DE3)/pLysS/pJK2 and E. coli CJB26. The excellent technical assistance of A. Denzin is
gratefully acknowledged.
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FOOTNOTES |
*
Corresponding author. Mailing address: Research Center
Borstel, Center for Medicine and Biosciences, Department of Medical and
Biochemical Microbiology, Parkallee 22, D-23845 Borstel, Germany. Phone: 49-4537-188488. Fax: 49-4537-188686. E-mail: wbrabetz{at}fz-borstel.de.
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Journal of Bacteriology, August 2000, p. 4654-4657, Vol. 182, No. 16
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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(2001). Cloning, sequencing, and functional analysis of three glycosyltransferases involved in the biosynthesis of the inner core region of Klebsiella pneumoniae lipopolysaccharide. Innate Immunity
7: 25-33
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