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J. Biol. Chem., Vol. 282, Issue 39, 28566-28576, September 28, 2007

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Commonality and Biosynthesis of the O-Methyl Phosphoramidate Capsule Modification in Campylobacter jejuni^*

David J. McNally¹², Marc P. Lamoureux², Andrey V. Karlyshev, Laura M. Fiori, Jianjun Li, Gillian Thacker, Russell A. Coleman, Nam H. Khieu, Brendan W. Wren, Jean-Robert Brisson, Harold C. Jarrell³, and Christine M. Szymanski⁴

From the Institute for Biological Sciences, National Research Council of Canada, 100 Sussex Drive, Ottawa, Ontario K1A 0R6, Canada and the Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London WC1E 7HT, United Kingdom

In this study we investigated the commonality and biosynthesis of the O-methyl phosphoramidate (MeOPN) group found on the capsular polysaccharide (CPS) of Campylobacter jejuni. High resolution magic angle spinning NMR spectroscopy was used as a rapid, high throughput means to examine multiple isolates, analyze the cecal contents of colonized chickens, and screen a library of CPS mutants for the presence of MeOPN. Sixty eight percent of C. jejuni strains were found to express the MeOPN with a high prevalence among isolates from enteritis, Guillain Barré, and Miller-Fisher syndrome patients. In contrast, MeOPN was not observed for any of the Campylobacter coli strains examined. The MeOPN was detected on C. jejuni retrieved from cecal contents of colonized chickens demonstrating that the modification is expressed by bacteria inhabiting the avian gastrointestinal tract. In C. jejuni 11168H, the cj1415-cj1418 cluster was shown to be involved in the biosynthesis of MeOPN. Genetic complementation studies and NMR/mass spectrometric analyses of CPS from this strain also revealed that cj1421 and cj1422 encode MeOPN transferases. Cj1421 adds the MeOPN to C-3 of the -D-GalfNAc residue, whereas Cj1422 transfers the MeOPN to C-4 of D-glycero--L-gluco-heptopyranose. CPS produced by the 11168H strain was found to be extensively modified with variable MeOPN, methyl, ethanolamine, and N-glycerol groups. These findings establish the importance of the MeOPN as a diagnostic marker and therapeutic target for C. jejuni and set the groundwork for future studies aimed at the detailed elucidation of the MeOPN biosynthetic pathway.

Received for publication, May 30, 2007 , and in revised form, July 13, 2007.

^* This work was supported by the National Research Council of Canada Genomics and Health Initiative, the Ontario Ministry of Agriculture and Food, Dow AgroSciences, the Biotechnology and Biological Sciences Research Council, and the Leverhulme Trust. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables 1-3 and Figs. 1 and 2.

¹ Recipient of funding from Dr. H. Jennings.

² Both authors contributed equally to this work.

³ To whom correspondence may be addressed. Tel.: 613-993-5900; Fax: 613-952-9092; E-mail: harold.jarrell{at}nrc-cnrc.gc.ca. ⁴ To whom correspondence may be addressed. Tel.: 613-990-1569; Fax: 613-952-9092; E-mail: christine.szymanski{at}nrc-cnrc.gc.ca.

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