Transcriptome analysis applied to survival of Shewanella oneidensis MR-1 exposed to ionizing radiation

Abstract

The ionizing radiation (IR) dose that yields 20% survival (D20) of Shewanella oneidensis MR-1 is lower by factors of 20 and 200 than those for Escherichia coli and Deinococcus radiodurans, respectively. Transcriptome analysis was used to identify the genes of MR-1 responding to 40 Gy (D20). We observed the induction of 170 genes and repression of 87 genes in MR-1 during a 1-h recovery period after irradiation. The genomic response of MR-1 to IR is very similar to its response to UV radiation (254 nm), which included induction of systems involved in DNA repair and prophage synthesis and the absence of differential regulation of tricarboxylic acid cycle activity, which occurs in IR-irradiated D. radiodurans. Furthermore, strong induction of genes encoding antioxidant enzymes in MR-1 was observed. DNA damage may not be the principal cause of high sensitivity to IR, considering that MR-1 carries genes encoding a complex set of DNA repair systems and 40 Gy IR induces less than one double-strand break in its genome. Instead, a combination of oxidative stress, protein damage, and prophage-mediated cell lysis during irradiation and recovery might underlie this organism's great sensitivity to IR.

FIG. 1.

Survival of Shewanella species exposed to acute gamma radiation (⁶⁰Co). Solid triangles, S. oneidensis MR-1 (ATCC 700550); solid squares, S. putrefaciens CN-32 (ATCC BAA-453); open diamonds, S. amazonensis (ATCC 700329); open squares, E. coli K-12 (MG1655). Strains were grown to an OD₆₀₀ of 0.9 and irradiated on ice as previously described (4).

FIG. 2.

Global gene expression trend in response to IR during a 1-h recovery period in S. oneidensis MR-1. Solid squares represent up-regulated genes, and open squares represent down-regulated genes. A positive number on the y axis represents the number of up-regulated genes, and a negative number represents the number of down-regulated genes.

FIG. 3.

Functional distribution of the differentially expressed genes in COG's functional categories. The total number of up-regulated genes is 170, and the total number of down-regulated genes is 87. C, energy production and conversion; E, amino acid transport and metabolism; F, nucleotide transport and metabolism; G, carbohydrate transport and metabolism; H, coenzyme metabolism; I, lipid metabolism; J, translation, ribosomal structure, and biogenesis; K, transcription; L, DNA replication, recombination, and repair; M, cell envelope biogenesis, outer membrane; N, cell motility and secretion; O, posttranslational modification, protein turnover, and chaperones; P, inorganic ion transport and metabolism; Q, secondary metabolite biosynthesis, transport, and catabolism; R, general function prediction only; S, function unknown; T, signal transduction mechanisms; V, defense mechanisms.