Differential effects of dimethylsulfoniopropionate, dimethylsulfonioacetate, and other S-methylated compounds on the growth of Sinorhizobium meliloti at low and high osmolarities

• Published in: Applied and Environmental Microbiology Vol. 64; no. 4; pp. 1420 - 1429
• Main Authors: Pichereau, V. (Universite de Rennes 1, Rennes, France), Pocard, J.A, Hamelin, J, Blanco, C, Bernard, T
• Format: Journal Article
• Language: English
• Published: Washington, DC American Society for Microbiology 01.04.1998
• Subjects: Action of physical and chemical agents on bacteria; ALGAE; Bacteria; Bacteriology; Biodiversity and Ecology; Biological and medical sciences; Biology of microorganisms of confirmed or potential industrial interest; Biotechnology; CRECIMIENTO; CROISSANCE; Environmental Sciences; EXTRACTOS VEGETALES; EXTRAIT D'ORIGINE VEGETALE; Fundamental and applied biological sciences. Psychology; GROWTH; Microbiology; Mission oriented research; Physiology and Biotechnology; Physiology and metabolism; PLANT EXTRACTS; PROPIONATE; PROPIONATES; PROPIONATOS; RHIZOBIUM; Microorganism growth; Osmolarity; Sulfur Organic compounds; Toxicity; Algae; Chlorophycophyta; Osmoregulation; Environmental factor; Extract; Metabolism; Stress; Salinity; Microorganism culture; Bacteria; Physiology; Ulva lactuca; Rhizobiaceae; Sulfonium compound; Thallophyta
• ISSN: 0099-2240; 1098-5336
• DOI: 10.1128/aem.64.4.1420-1429.1998

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