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Appl Environ Microbiol, April 1998, p. 1420-1429, Vol. 64, No. 4
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Differential Effects of Dimethylsulfoniopropionate, Dimethylsulfonioacetate, and Other S-Methylated Compounds on the Growth of Sinorhizobium meliloti at Low and High Osmolarities

Vianney Pichereau,1 Jean-Alain Pocard,1,* Jack Hamelin,2 Carlos Blanco,1 and Théophile Bernard1

Groupe Membranes et Osmorégulation, UPRES-A CNRS 6026,1 and Synthèse et Electrosynthèse Organiques 3, UMR CNRS 6510,2 Université de Rennes 1, Rennes, France

Received 1 December 1997/Accepted 27 January 1998

An extract from the marine alga Ulva lactuca was highly osmoprotective in salt-stressed cultures of Sinorhizobium meliloti 102F34. This beneficial activity was due to algal 3-dimethylsulfoniopropionate (DMSP), which was accumulated as a dominant compatible solute and strongly reduced the accumulation of endogenous osmolytes in stressed cells. Synthetic DMSP also acted as a powerful osmoprotectant and was accumulated as a nonmetabolizable cytosolic osmolyte (up to a concentration of 1,400 nmol/mg of protein) throughout the growth cycles of the stressed cultures. In contrast, 2-dimethylsulfonioacetate (DMSA), the sulfonium analog of the universal osmoprotectant glycine betaine (GB), was highly toxic to unstressed cells and was not osmoprotective in stressed cells of wild-type strains of S. meliloti. Nonetheless, the transport and accumulation of DMSA, like the transport and accumulation of DMSP and GB, were osmoregulated and increased fourfold in stressed cells of strain 102F34. Strikingly, DMSA was not toxic and became highly osmoprotective in mutants that are impaired in their ability to demethylate GB and DMSA. Furthermore, 2-methylthioacetate and thioglycolic acid (TGA), the demethylation products of DMSA, were excreted, apparently as a mechanism of cellular detoxification. Also, exogenous TGA and DMSA displayed similar inhibitory effects in strain 102F34. Thus, on the basis of these findings and other physiological and biochemical evidence, we infer that the toxicity of DMSA in wild-type strains of S. meliloti stems from its catabolism via the GB demethylation pathway. This is the first report describing the toxicity of DMSA in any organism and a metabolically stable osmoprotectant (DMSP) in S. meliloti.

* Corresponding author. Mailing address: Groupe Membranes et Osmorégulation, UPRES-A CNRS 6026, Bâtiment 14, Université de Rennes 1, Campus de Beaulieu, Av. du Général Leclerc, F-35042 Rennes Cedex, France. Phone and Fax: 33 (0)2 99 28 61 40. E-mail: pocard{at}univ-rennes1.fr.




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