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A more recent version of this article appeared on July 9, 2004 Originally published In Press as doi:10.1074/jbc.M313103200 on June 3, 2004
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Papers In Press, published online ahead of print April 21, 2004
J. Biol. Chem, 10.1074/jbc.M313103200
Submitted on December 2, 2003
Revised on April 19, 2004
Accepted on April 21, 2004

Trehalose is required for growth of mycobacterium smegmatis

Peter J. Woodruff, Brian L. Carlson, Bunpote Siridechadilok, Matthew R. Pratt, Spencer J. Williams, and Carolyn R. Bertozzi

Chemistry, University of California, Berkeley, Berkeley, CA 94720

Corresponding Author: crb{at}uclink.berkeley.edu

Mycobacteria contain high levels of the disaccharide trehalose in free form as well as within various immunologically relevant glycolipids such as cord factor and sulfolipid-1. By contrast, most bacteria use trehalose solely as a general osmoprotectant or thermoprotectant. Mycobacterium tuberculosis and Mycobacterium smegmatis possess three pathways for the synthesis of trehalose. Most bacteria possess only one trehalose biosynthesis pathway and do not elaborate the disaccharide into more complex metabolites, suggesting a distinct role for trehalose in mycobacteria. We disabled key enzymes required for each of the three pathways in M. smegmatis by allelic replacement. The resulting trehalose biosynthesis mutant was unable to proliferate and enter stationary phase unless supplemented with trehalose. At elevated temperatures, however, the mutant was unable to proliferate even in the presence of trehalose. Genetic complementation experiments showed that each of the three pathways was able to recover the mutant in the absence of trehalose, even at elevated temperatures. From a panel of trehalose analogs, only those with the native alpha , alpha -(1,1) anomeric stereochemistry rescued the mutant, whereas alternate stereoisomers and general osmo- and thermoprotectants were inactive. These findings suggest a dual role for trehalose as both a thermoprotectant and a precursor of critical cell wall metabolites.


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