2-Sulfotrehalose, a novel osmolyte in haloalkaliphilic archaea

Abstract

A novel 131 ␣-linked glucose disaccharide with sulfate at C-2 of one of the glucose moieties, 1-(2-O-sulfo-␣-D-glucopyranosyl)-␣-D-glycopyranose, was found to be the major organic solute accumulated by a Natronococcus sp. and several Natronobacterium species. The concentration of this novel disaccharide, termed sulfotrehalose, increased with increasing concentrations of external NaCl, behavior consistent with its identity as an osmolyte. A variety of noncharged disaccharides (trehalose, sucrose, cellobiose, and maltose) were added to the growth medium to see if they could suppress synthesis and accumulation of sulfotrehalose. Sucrose was the most effective in suppressing biosynthesis and accumulation of sulfotrehalose, with levels as low as 0.1 mM being able to significantly replace the novel charged osmolyte. Other common osmolytes (glycine betaine, glutamate, and proline) were not accumulated or used for osmotic balance in place of the sulfotrehalose by the halophilic archaeons.

Osmoadaptation and osmoregulation in archaea

“…Drosophila melanogaster and a number of fish accumulate urea (46) but need to accumulate 'urea-counteracting' solutes to mitigate the toxic effects of urea. All of these noncharged osmolytes are relatively rare (and in most cases not found) in archaea, although as mentioned above N. occultus internalizes sucrose from the medium and uses this nonionic solute to balance osmotic stress (19).…”

“…Natronococcus sp. have been shown to accumulate sucrose from the medium (19). As little as 0.1 mM external sucrose will dramatically suppress synthesis of endogenous osmolytes.…”

“…The negative charge is provided by carboxylate, phosphate and sulfate groups; these modified solutes serve as counterions for K + . As shown in table 1, these solutes include glucosylglycerate (37), beta-mannosylglycerate (47), alpha-diglycerol phosphate (39), di-myo-inositol-1-phosphate (DIP) (48,49), and sulfotrehalose (19). Anionic carbohydrates are much less common in bacteria, although alphamannosylglycerate has been detected in Rhodothermus sp.…”

Exploring biodegradable polymer production from marine microbes

“…Halophiles are found in all the three domains of life; they basically adapt two different metabolic pathways to survive on this high salt concentration; the first is to regulate concentrations of KCl with that of NaCl in the external environment, thus maintaining the osmotic pressure and enhancing survival [100,101]. Some haloalkaliphilic bacteria such as Natronococcus occultus and N. gregoryi use 2-sulfotrehalose instead of KCl to some extent to counterbalance these external stimuli when cultured in nutrient limited medium [102]. The second adaptation is similar to that of the earlier one whereas bacteria and eukarya maintain low concentration of salt by accumulating low molecular weight organic compounds known as osmolytes [100,101].…”

Biocompounds from Haloarchaea and Their Uses in Biotechnology

“…(ii) Borderline extreme halophiles: growing best in media containing 1.5-4.0 M salt; (i) Cells accumulate high KCl intracellular concentrations or some osmolytes such as 2-sulfotrehalose to deal with high ionic strength [9]. This "salt-in" strategy is mainly used by haloarchaea and it requires the adaptation of the intracellular enzymatic machinery, as proteins should maintain their proper conformation and activity at nearsaturating salt concentrations [1,3,4].…”