Abstract
The dissacharide trehalose is an important intracellular osmoprotectant and the OtsA/B pathway is the principal pathway for trehalose biosynthesis in a wide range of bacterial species. Scaffolding proteins and other cytoskeletal elements play an essential role in morphogenetic processes in bacteria. Here we describe how OtsA, in addition to its role in trehalose biosynthesis, functions as an osmotic stress sensor to regulate cell morphology in Arthrobacter strain A3. In response to osmotic stress, this and other Arthrobacter species undergo a transition from bacillary to myceloid growth. An otsA null mutant exhibits constitutive myceloid growth. Osmotic stress leads to a depletion of trehalose-6-phosphate, the product of the OtsA enzyme, and experimental depletion of this metabolite also leads to constitutive myceloid growth independent of OtsA function. In vitro analyses indicate that OtsA can self-assemble into protein networks, promoted by trehalose-6-phosphate, a property that is not shared by the equivalent enzyme from E. coli, despite the latter’s enzymatic activity when expressed in Arthrobacter. This, and the localization of the protein in non-stressed cells at the mid-cell and poles, indicates that OtsA from Arthrobacter likely functions as a cytoskeletal element regulating cell morphology. Recruiting a biosynthetic enzyme for this morphogenetic function represents an intriguing adaptation in bacteria that can survive in extreme environments.
Highlights
Trehalose (a-D-glucopyranosyl(1,1)-a-D-glucopyranoside) is a non-reducing disaccharide that functions as an important intracellular protectant against a variety of stress conditions including desiccation, dehydration, heat, cold, and oxidation [1]
Little is known about how environmental cues are perceived and translated into changes in cell morphology
We describe how a biosynthetic enzyme involved in synthesis of an important intracellular osmoprotectant doubles as an osmotic stress sensing morphogenetic protein
Summary
Trehalose (a-D-glucopyranosyl(1,1)-a-D-glucopyranoside) is a non-reducing disaccharide that functions as an important intracellular protectant against a variety of stress conditions including desiccation, dehydration, heat, cold, and oxidation [1]. At least four different pathways for trehalose biosynthesis have been reported, described as OtsA/B, TreY/Z, TreS, and TreT [2]. The OtsA/B pathway is the principal pathway for trehalose biosynthesis and is widely distributed in bacteria, fungi and plants (trehalose-6-phosphate synthase and trehalose6-phosphate phosphatase in Arabidopsis thaliana). OtsA utilises UDP-glucose and glucose6-phosphate to synthesize trehalose-6-phosphate (T6P) and subsequently OtsB converts T6P into Pi and trehalose. In Saccharomyces cerevisiae, T6P controls the decision to proceed through cell division [3] and in plants it regulates flowering both in the leaf and in the shoot apical meristem [4]
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