Dps Protects Cells against Multiple Stresses during Stationary Phase

Abstract

Dps, the nonspecific DNA-binding protein from starved cells, is the most abundant protein in stationaryphase Escherichia coli. Dps homologs are found throughout the bacteria and in at least one archaeal species. Dps has been shown to protect cells from oxidative stress during exponential-phase growth. During stationary phase, Dps organizes the chromosome into a highly ordered, stable nucleoprotein complex called the biocrystal. We show here that Dps is required for long-term stationary-phase viability under competitive conditions and that dps mutants have altered lag phases compared to wild-type cells. We also show that during stationary phase Dps protects the cell not only from oxidative stress but also from UV and gamma irradiation, iron and copper toxicity, thermal stress, and acid and base shock. The protective roles of Dps are most likely achieved through a combination of functions associated with the protein-DNA binding and chromosome compaction, metal chelation, ferroxidase activity, and regulation of gene expression.Dps, the DNA-binding protein from starved cells, is among the most abundant proteins in stationary-phase Escherichia coli. As cells transition from exponential-phase growth to stationary phase, Dps is induced in an RpoS-dependent manner, reaching up to 200,000 molecules per cell (2). Dps is also regulated by OxyR and 70 in response to oxidative stress during exponential phase (3). The protein has nonspecific DNA-binding activity, affects the expression of at least three dozen genes, and plays a role in various stress responses, including protection from oxidative damage (2, 18). The protein's active form is a hollow, spherical, dodecamer with an outer diameter of ϳ90 Å and an interior core diameter of ϳ45 Å (2, 27). During stationary phase, Dps binds the chromosome, forming a highly ordered and stable nucleoprotein complex called a biocrystal. This biocrystalline form is distinct from the exponential-phase configuration of the nucleoid and is unique to stationary-phase cells (12,19,27). Biocrystal formation contributes to the ability of Dps to affect gene expression and protects chromosomal DNA. Dps shows significant structural homology to the ferritins, a highly conserved family of proteins found in virtually all organisms, and possesses ferroxidase activity and the ability to sequester iron (15). This iron-binding activity very likely plays a significant role in the ability of Dps to protect the chromosome from oxidative damage.For E. coli, most studies of Dps have focused on its role in oxidative damage protection, particularly against peroxides, during exponential phase (2, 18). Here we expand the repertoire of potential stressors to include long-term stationaryphase incubation under conditions of nutrient stress and competition, the presence of oxidizing agents and heavy metals, thermal stress, ionizing and UV radiation, and extremes of pH. Our working hypothesis is that this multifunctional protein is involved in many cellular processes and probably functions via several different mecha...

An archaeal antioxidant: Characterization of a Dps-like protein from Sulfolobus solfataricus

“…Whereas this putative metal-binding motif is distinct from that (47). Whereas dps expression is generally considered specific to oxidative stress during exponential growth, Dps proteins have been shown to effectively protect against a broad spectrum of different stresses while in stationary phase (48). SsDps is also likely to confer protection against a broader range of environmental stress during stationary phase; however, growth of S. solfataricus is limited by the accumulation of inorganic ions and thus complicates studies aimed at understanding S. solfataricus physiologies under true nutrient limitation (49).…”

Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx - mutants of Escherichia coli

“…Dps was initially identified as a protein that coats DNA in vitro, and subsequent electron microscopy studies have indicated that it does so in vivo in stationary-phase bacteria (43,44). This behavior was rationalized on the grounds that by coating the DNA, the protein would protect it from chemical damage, including oxidants.…”

Identification and biochemical properties of Dps (starvation‐induced DNA binding protein) from cyanobacterium Anabaena sp. PCC 7120

“…E. coli Dps, first characterized as an antioxidant protein, was abundantly expressed during the stationary phase in response to nutrient stress or oxidative stress (10). It was shown to incorporate DNA without sequence specificity and further exert protection against hydrogen peroxide stress, Dnase cleavage, UV radiation and acid shock (10,11). Based on sequence analysis, Dps are endowed with conserved ferroxidase domain, implicating that they also belong to ferritin family.…”

“…In E. coli, the structure, biochemical characterization and cellular regulation of Dps protein have been extensively investigated (5 -9). E. coli Dps, first characterized as an antioxidant protein, was abundantly expressed during the stationary phase in response to nutrient stress or oxidative stress (10). It was shown to incorporate DNA without sequence specificity and further exert protection against hydrogen peroxide stress, Dnase cleavage, UV radiation and acid shock (10,11).…”