A trehalose biosynthetic enzyme doubles as an osmotic stress sensor to regulate bacterial morphogenesis

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.

Carbohydrate Metabolism and Signaling in Squash Nectaries and Nectar Throughout Floral Maturation

“…8D), it is unlikely that increased Tre6P is causing the reduced nectar in the trehalose-treated samples. It should also be noted that trehalose plays a highly conserved role in the regulation of cellular responses to osmotic stress, ranging from bacteria to plants and animals (Iturriaga et al, 2009;Chen et al, 2017). Although a molecular mechanism for the involvement of trehalose within the context of our study is unclear, secretory nectaries are exposed to a tremendous amount of osmotic stress due to a high intracellular concentration of Suc (Fig.…”

Stress-induced formation of cell wall-deficient cells in filamentous actinomycetes

“…Actinobacteria display a wide diversity of morphologies, including cocci ( Rhodococcus ), rods ( Mycobacterium and Corynebacterium ) and mycelia ( Streptomyces and Kitasatospora ), or even multiple shapes ( Arthrobacter ) 11 , 12 . Species belonging to these genera are able to change their morphology to adapt to extreme environments.…”

“…Arthrobacter species also exhibit high resistance to desiccation and cold stresses. Upon hyperosmotic stress, these cells can modulate the synthesis of osmoprotectants and switch between rod-shaped and myceloid cells 12 .…”

GREACE-assisted adaptive laboratory evolution in endpoint fermentation broth enhances lysine production by Escherichia coli

“…Bacteria have naturally evolved multiple mechanisms to cope with environmental stress, such as increased synthesis of aquaporin to accelerate water export [27], regulated expression of potassium transporters to increase intracellular potassium concentration [28], expression of mechanosensitive channels [29], accumulation of osmoprotectants like glycine betaine, trehalose, ectoine and proline [30–32], and enhancement of cytoplasmic membrane stability [21]. However, these naturally evolved mechanisms are generally inadequate to prevent the strains from dramatically enhanced complex and combinatorial stress encountered in industrial conditions.…”