Trehalose protects Escherichia coli against carbon stress manifested by protein acetylation and aggregation

Abstract

Summary The disaccharide trehalose is widely distributed in nature and can serve as a carbon reservoir, a signaling molecule for controlling glucose metabolism and a stress protectant. We demonstrated that in Escherichia coli ΔotsA cells, which are unable to synthesize trehalose, the aggregation of endogenous proteins during the stationary phase was increased in comparison to wild‐type cells. The lack of trehalose synthesis boosted Nε‐lysine acetylation of proteins, which in turn enhanced their hydrophobicity and aggregation. This increased Nε‐lysine acetylation could result from carbon overflow and the accumulation of acetyl phosphate caused by the ΔotsA mutation. These findings provide a better understanding of the previously reported protective functions of trehalose in protein stabilization and the prevention of protein aggregation. Our results indicate that trehalose may participate in proteostasis not only as a chemical chaperone but also as a metabolite that indirectly counteracts detrimental protein acetylation. We propose that trehalose protects E. coli against carbon stress – the synthesis and storage of trehalose can prevent carbon overflow, which otherwise is manifested by protein acetylation and aggregation.

Mechanisms Protecting Acinetobacter baumannii against Multiple Stresses Triggered by the Host Immune Response, Antibiotics and Outside-Host Environment

“…A crucial role in desiccation resistance in various microorganisms is played by the non-reducing disaccharide, trehalose. Trehalose acts as an osmolyte, chemical chaperone, and metabolite that can directly or indirectly stabilize proteins and membranes [ 82 , 83 , 84 , 85 ]. It seems that endogenous trehalose is not involved in desiccation tolerance in A. baumannii, but exogenous trehalose was found to efficiently protect A. baumannii on dry surfaces [ 68 ].…”

Trehalose and bacterial virulence

“…It is proposed that similar interactions of trehalose with cis double bonds of the aromatic side chains of some amino acids could prevent protein aggregation [ 2 ]. Protein stabilization may also be associated with the role of trehalose in limiting Nε-lysine acetylation of proteins which would otherwise result in increased protein hydrophobicity and aggregation [ 44 ]. Nε-lysine acetylation of proteins may be a consequence of carbon overflow within the bacterial cell.…”

“…Nε-lysine acetylation of proteins may be a consequence of carbon overflow within the bacterial cell. Therefore, in this case trehalose can function both as a chemical chaperone andas a metabolite that limits carbon overflow in biological systems [ 44 ].…”

Quantitative proteome and PTMome analysis ofArabidopsis thalianaroot responses to persistent osmotic and salinity stress

“…Thus, activation of UGP1 may be linked to increased trehalose biosynthesis in osmotic- and salt-stressed roots. In E. coli , trehalose stabilizes proteins and prevents protein aggregation during osmotic stress (Moruno Algara et al, 2019). This is also true for resurrection plants such as Myrothamnus flabellifolius where trehalose functions as a protectant to stabilize membranes and proteins, allowing them to survive during dehydration-rehydration cycles (Figueroa and Lunn, 2016; O’Hara et al, 2013).…”