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A New Physiological Role for the DNA Molecule as a Protector against Drying Stress in Desiccation-Tolerant Microorganisms.

ABSTRACT: The DNA molecule is associated with the role of encoding information required to produce RNA which is translated into proteins needed by the cell. This encoding involves information transmission to offspring or to other organisms by horizontal transfer. However, despite the abundance of this molecule in both the cell and the environment, its physiological role seems to be restricted mainly to that of a coding and inheritance molecule. In this paper, we report a new physiological role for the DNA molecule as involved in protection against desiccation, in addition to its well-established main information transfer and other recently reported functions such as bio-film formation in eDNA form. Desiccation-tolerant microorganisms such as Microbacterium sp. 3J1 significantly upregulate genes involved in DNA synthesis to produce DNA as part of their defensive mechanisms to protect protein structures and functions from drying according to RNA-seq analysis. We have observed the intracellular overproduction of DNA in two desiccation-tolerant microorganisms, Microbacterium sp. 3J1 and Arthrobacter siccitolerans 4J27, in response to desiccation signals. In addition, this conclusion can be made from our observations that synthetic DNA protects two proteins from drying and when part of a xeroprotectant preparation, DNA from various organisms including desiccation-sensitive species, does the same. Removal of DNA by nuclease treatment results in absence of this additive protective effect. We validated this role in biochemical and biophysical assays in proteins and occurs in trans even with short, single chains of synthetically produced DNA.

SUBMITTER: Garcia-Fontana C

PROVIDER: S-EPMC5177630 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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A New Physiological Role for the DNA Molecule as a Protector against Drying Stress in Desiccation-Tolerant Microorganisms.

García-Fontana Cristina C Narváez-Reinaldo Juan J JJ Castillo Francisco F González-López Jesús J Luque Irene I Manzanera Maximino M

Frontiers in microbiology 20161222

The DNA molecule is associated with the role of encoding information required to produce RNA which is translated into proteins needed by the cell. This encoding involves information transmission to offspring or to other organisms by horizontal transfer. However, despite the abundance of this molecule in both the cell and the environment, its physiological role seems to be restricted mainly to that of a coding and inheritance molecule. In this paper, we report a new physiological role for the DNA ...[more]

PMID: 28066383

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Project description:The growth and persistence of rhizobia and bradyrhizobia in soils are negatively impacted by drought conditions. In this study, we used genome-wide transcriptional analyses to obtain a comprehensive understanding of the response of Bradyrhizobium japonicum to drought. Desiccation of cells resulted in the differential expression of 15 to 20% of the 8,453 [corrected] B. japonicum open reading frames, with considerable differentiation between early (after 4 h) and late (after 24 and 72 h) expressed genes. While 225 genes were universally up-regulated at all three incubation times in response to desiccation, an additional 43 and 403 up-regulated genes were common to the 4/24- and 24/72-h incubation times, respectively. Desiccating conditions resulted in the significant induction (>2.0-fold) of the trehalose-6-phosphate synthetase (otsA), trehalose-6-phosphate phosphatase (otsB), and trehalose synthase (treS) genes, which encode two of the three trehalose synthesis pathways found in B. japonicum. Gene induction was correlated with an elevated intracellular concentration of trehalose and increased activity of trehalose-6-phosphate synthetase, collectively supporting the hypothesis that this disaccharide plays a prominent and important role in promoting desiccation tolerance in B. japonicum. Microarray data also indicated that sigma(54)- and sigma(24)-associated transcriptional regulators and genes encoding isocitrate lyase, oxidative stress responses, the synthesis and transport of exopolysaccharides, heat shock response proteins, enzymes for the modification and repair of nucleic acids, and the synthesis of pili and flagella are also involved in the response of B. japonicum to desiccation. Polyethylene glycol-generated osmotic stress induced significantly fewer genes than those transcriptionally activated by desiccation. However, 67 genes were commonly induced under both conditions. Taken together, these results suggest that B. japonicum directly responds to desiccation by adapting to changes imparted by reduced water activity, such as the synthesis of trehalose and polysaccharides and, secondarily, by the induction of a wide variety of proteins involved in protection of the cell membrane, repair of DNA damage, stability and integrity of proteins, and oxidative stress responses.

Project description:The growth and persistence of rhizobia and bradyrhizobia in soils are negatively impacted by drought conditions. In this study, we used genome-wide transcriptional analyses to obtain a comprehensive understanding of the response of Bradyrhizobium japonicum to drought. Desiccation of cells resulted in the differential expression of 15 to 20% of the 8,480 B. japonicum open reading frames, with considerable differentiation between early (after 4 h) and late (after 24 and 72 h) expressed genes. While 225 genes were universally up-regulated at all three incubation times in response to desiccation, an additional 43 and 403 up-regulated genes were common to the 4/24- and 24/72-h incubation times, respectively. Desiccating conditions resulted in the significant induction (>2.0-fold) of the trehalose-6-phosphate synthetase (otsA), trehalose-6-phosphate phosphatase (otsB), and trehalose synthase (treS) genes, which encode two of the three trehalose synthesis pathways found in B. japonicum. Gene induction was correlated with an elevated intracellular concentration of trehalose and increased activity of trehalose-6-phosphate synthetase, collectively supporting the hypothesis that this disaccharide plays a prominent and important role in promoting desiccation tolerance in B. japonicum. Microarray data also indicated that sigma(54)- and sigma(24)-associated transcriptional regulators and genes encoding isocitrate lyase, oxidative stress responses, the synthesis and transport of exopolysaccharides, heat shock response proteins, enzymes for the modification and repair of nucleic acids, and the synthesis of pili and flagella are also involved in the response of B. japonicum to desiccation. Polyethylene glycol-generated osmotic stress induced significantly fewer genes than those transcriptionally activated by desiccation. However, 67 genes were commonly induced under both conditions. Taken together, these results suggest that B. japonicum directly responds to desiccation by adapting to changes imparted by reduced water activity, such as the synthesis of trehalose and polysaccharides and, secondarily, by the induction of a wide variety of proteins involved in protection of the cell membrane, repair of DNA damage, stability and integrity of proteins, and oxidative stress responses. Keywords: stress response; time course

Dataset Information

A New Physiological Role for the DNA Molecule as a Protector against Drying Stress in Desiccation-Tolerant Microorganisms.

Publications

A New Physiological Role for the DNA Molecule as a Protector against Drying Stress in Desiccation-Tolerant Microorganisms.

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