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Chapter 14 : Phase Variation in Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure

Authors: Oliver Kooistra1, Ulrich Zähringer1, Edeltraud Lüneberg2, Matthias Frosch2, Yuriy A. Knirel3
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Affiliations: 1: Division of Immuno-chemistry, Research Center Borstel, Center for Medicine and Biosciences, D-23845 Borstel, Germany; 2: Institute for Hygiene und Microbiology, University of Würzburg, D-97080 Würzburg, Germany; 3: N. D. Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences, 117913 Moscow, Russia
Content Type: Monograph
Publication Year: 2002

Category: Bacterial Pathogenesis

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Phase Variation in Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure, Page 1 of 2

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Abstract:

A change in the lipopolysaccharide (LPS) upon phase variation in serogroup 1, subgroup OLDA, wild-type strain RC1 was detected with the aid of LPS-specific monoclonal antibody MAb 2625. Chromosomal insertion and excision of a 30-kb instable genetic element of possibly phage origin was identified as the molecular mechanism for phase variation. The core of the LPS is a nonasaccharide that lacks heptose and phosphate, contains abundant 6-deoxy sugars, and is highly O- and N-acetylated. The MAb 2625 epitope is present in wild-type RC1 cells and is lost in the spontaneous mutant 811 upon phase variation. Lipid A was prepared by mild acid hydrolysis (0.1 M NaOAc-HOAc buffer, pH 4.4,100№C, 4 h) of LPS each of wild-type RC1 and phase-variant 811 followed by centrifugation and lyophilization of the pellet. LPS biosynthesis pathways involved in assembly of lipid A were also affected by phase variation, which resulted in a specifically altered lipid A structure with a modified profile of fatty acids of a particular type. Phase variation may affect a regulatory factor, which influences LPS biosynthesis, virulence, and serum resistance.

Citation: Kooistra O, Zähringer U, Lüneberg E, Frosch M, Knirel Y. 2002. Phase Variation in Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure, p 68-73. In Marre R, Abu Kwaik Y, Bartlett C, Cianciotto N, Fields B, Frosch M, Hacker J, Lück P (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555817985.ch14

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Phase Variation in Legionella pneumophila Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure
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Citation: Kooistra O, Zähringer U, Lüneberg E, Frosch M, Knirel Y. 2002. Phase Variation in Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure, p 68-73. In Marre R, Abu Kwaik Y, Bartlett C, Cianciotto N, Fields B, Frosch M, Hacker J, Lück P (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555817985.ch14
/content/10.1128/9781555817985.chap14.fig14-1
FIGURE 1

Parts of negative ion mode MALDI-TOF mass spectra of tetraacyl lipid A from serogroup 1, subgroup OLDA, wild-type RC1 (top panel) and phase-variant 811 (bottom panel). Tetraacyl monophos-phoryl lipid A was prepared by de--acylation with hydrazine; one of the phosphate groups (most likely at position 1) was split, probably due to overheating during work-up of the reaction mixture with acetone. The value for [M-H] ions, the calculated chemical molecular mass (in parentheses), and the deduced chain length (the total number of carbons) of the 3−hydroxylated fatty acids at positions 2 and 2′ are given for each major ion peak of tetraacyl lipid A with one residue each of 14:0(3-OH) and 14:0(2,3-di-OH) at positions 3 and 3′. The mass spectra were acquired in reflector configuration with 2,5-dihydroxybenzoic acid as matrix.

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Image of FIGURE 1
FIGURE 1

Parts of negative ion mode MALDI-TOF mass spectra of tetraacyl lipid A from serogroup 1, subgroup OLDA, wild-type RC1 (top panel) and phase-variant 811 (bottom panel). Tetraacyl monophos-phoryl lipid A was prepared by de--acylation with hydrazine; one of the phosphate groups (most likely at position 1) was split, probably due to overheating during work-up of the reaction mixture with acetone. The value for [M-H] ions, the calculated chemical molecular mass (in parentheses), and the deduced chain length (the total number of carbons) of the 3−hydroxylated fatty acids at positions 2 and 2′ are given for each major ion peak of tetraacyl lipid A with one residue each of 14:0(3-OH) and 14:0(2,3-di-OH) at positions 3 and 3′. The mass spectra were acquired in reflector configuration with 2,5-dihydroxybenzoic acid as matrix.

Citation: Kooistra O, Zähringer U, Lüneberg E, Frosch M, Knirel Y. 2002. Phase Variation in Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure, p 68-73. In Marre R, Abu Kwaik Y, Bartlett C, Cianciotto N, Fields B, Frosch M, Hacker J, Lück P (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555817985.ch14
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/content/10.1128/9781555817985.chap14.fig14-2
FIGURE 2

Proposed structure of the major lipid A from serogroup 1, subgroup OLD A, wild-type RC1, and phase-variant 811. The position of the fatty acids is shown according to published data ( ). The chain length of the 3-hydroxylated fatty acids at positions 2 and 2′ is indicated as the total number of carbons = 20 at both GlcN3N residues in wild-type RC1. In the avirulent phase variant 811, the chain length of the 3-hydroxylated fatty acids at positions 2 and 2′ is = 16 at one and = 18 at the other GlcN3N residue.

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10.1128/9781555817985/fig14-2.gif
Image of FIGURE 2
FIGURE 2

Proposed structure of the major lipid A from serogroup 1, subgroup OLD A, wild-type RC1, and phase-variant 811. The position of the fatty acids is shown according to published data ( ). The chain length of the 3-hydroxylated fatty acids at positions 2 and 2′ is indicated as the total number of carbons = 20 at both GlcN3N residues in wild-type RC1. In the avirulent phase variant 811, the chain length of the 3-hydroxylated fatty acids at positions 2 and 2′ is = 16 at one and = 18 at the other GlcN3N residue.

Citation: Kooistra O, Zähringer U, Lüneberg E, Frosch M, Knirel Y. 2002. Phase Variation in Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure, p 68-73. In Marre R, Abu Kwaik Y, Bartlett C, Cianciotto N, Fields B, Frosch M, Hacker J, Lück P (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555817985.ch14
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References

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1. Knirel, Y. A.,, E. T. Rietschel,, R. Marre,, and U. Zahringer. 1994. The structure of the O-specific chain of Legionella pneumophila serogroup 1 lipopolysaccharide. Eur. J. Biochem. 221: 239– 245.
2. Knirel, Y. A.,, H. Moll,, and U. Zahringer. 1996. Structural study of a highly O-acetylated core of Legionella pneumophila serogroup 1 lipopolysaccharide. Carbohydr. Res. 293: 223– 234.
3. Kooistra, O.,, E. Lüneberg,, B. Lindner,, Y. A. Knirel,, M. Frosch,, and U. Zahringer. 2001. Complex O-acetylation in Legionella pneumophila serogroup 1 lipopolysaccharide. Evidence for two genes involved in 8- O-acetylation of legionaminic acid. Biochemistry 40: 7630– 7640.
4. Liineberg, E.,, B. Mayer,, N. Daryab,, O. Kooistra,, U. Zahringer,, M. Rohde,, J. Swanson,, and M. Frosch. 2001. Chromosomal insertion and excision of 30 kb instable genetic element is responsible for phase variation of lipopolysaccharide and other virulence determinants in Legionella pneumophila. Mol. Microbiol. 39: 1259– 1271.
5. Liineberg, E.,, U. Zahringer,, Y. A. Knirel,, D. Steinmann,, M. Hartmann,, I. Steinmetz,, M. Rohde,, J. Kohl,, and M. Frosch. 1998. Phase-variable expression of lipopolysaccharide contributes to the virulence of Legionella pneumophila. J. Exp. Med. 188: 49– 60.
6. Lüneberg, E.,, N. Zetzmann,, D. Alber,, Y. A. Knirel,, O. Kooistra,, U. Zähringer,, and M. Frosch. 2000. Cloning and functional characterization of a 30 kb gene locus required for lipopolysaccharide biosynthesis in Legionella pneumophila. Int. J. Med. Microbiol. 290: 37– 49.
7. Moll, H.,, A. Sonesson,, E. Jantzen,, R. Marre,, and U. Zahringer. 1992. Identification of 27-oxo-octacosanoic acid and heptacosane-1,27-dioic acid in Legionella pneumophila. FEMS Microbiol. Lett. 92: 1– 6.
8. Moll, H.,, Y. A. Knirel,, J. H. Helbig,, and U. Zahringer. 1997. Identification of an α -d-Manp-(1 → 8)-Kdo disaccharide in the inner core region and the structure of the complete core region of the Legionella pneumophila serogroup 1 lipopolysaccharide. Carbohydr. Res. 304: 91– 95.
9. Neumeister, B.,, M. Faigle,, M. Sommer,, U. Zähringer,, F. Stelter,, R. Menzel,, C. Schütt,, and H. Northoff. 1998. Low endotoxic potential of Legionella pneumophila lipopolysaccharide due to failure of interaction with the monocyte lipopolysaccharide receptor CD14. Infect. Immun. 66: 4151– 4157.
10. Tsvetkov, Y. E.,, A. S. Shashkov,, Y. A. Knirel,, and U. Zahringer. 2001. Synthesis and identification in bacterial lipopolysaccharides of 5,7-diacetamido-3,5,7,9-tetradeoxy -d- glycero-d-galacto- and -d- glycero-d- talo-non-2-ulosonic acids. Carbohydr. Res. 331: 233– 237.
11. Zahringer, U-,, Y. A. Knirel,, B. Lindner,, J. H. Helbig,, A. Sonesson,, R. Marre,, and E. T. Rietschel. 1995. The lipopolysaccharide of Legionella pneumophila serogroup 1 (strain Philadelphia 1): chemical structure and biological significance. Prog. Clin. Biol. Res. 392: 113– 139.
12. Zou, C. H.,, Y. A. Knirel,, J. H. Helbig,, U. Zähringer,, and C. S. Mintz. 1999. Molecular cloning and characterization of a locus responsible for O-acetylation of the O-polysaccharide of Legionella pneumophila serogroup 1 lipopolysaccharide. J. Bacteriol. 181: 4137– 4141.

Tables

Phase Variation in Legionella pneumophila Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure
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Citation: Kooistra O, Zähringer U, Lüneberg E, Frosch M, Knirel Y. 2002. Phase Variation in Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure, p 68-73. In Marre R, Abu Kwaik Y, Bartlett C, Cianciotto N, Fields B, Frosch M, Hacker J, Lück P (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555817985.ch14
/content/10.1128/9781555817985.chap14.tab14-1
TABLE 1

Fatty acid composition of lipid A from wild-type RC1 and phase-variant 811

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10.1128/9781555817985/tab14-1.gif
Generic image for table
TABLE 1

Fatty acid composition of lipid A from wild-type RC1 and phase-variant 811

Citation: Kooistra O, Zähringer U, Lüneberg E, Frosch M, Knirel Y. 2002. Phase Variation in Serogroup 1, Subgroup OLDA, Strain RC1 Influences Lipid A Structure, p 68-73. In Marre R, Abu Kwaik Y, Bartlett C, Cianciotto N, Fields B, Frosch M, Hacker J, Lück P (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555817985.ch14

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