Transcriptome analysis reveals a stress response of Shewanella oneidensis deprived of background levels of ionizing radiation

PLoS One. 2018 May 16;13(5):e0196472. doi: 10.1371/journal.pone.0196472. eCollection 2018.

Abstract

Natural ionizing background radiation has exerted a constant pressure on organisms since the first forms of life appeared on Earth, so that cells have developed molecular mechanisms to avoid or repair damages caused directly by radiation or indirectly by radiation-induced reactive oxygen species (ROS). In the present study, we investigated the transcriptional effect of depriving Shewanella oneidensis cultures of background levels of radiation by growing the cells in a mine 655 m underground, thus reducing the dose rate from 72.1 to 0.9 nGy h-1 from control to treatment, respectively. RNASeq transcriptome analysis showed the differential expression of 4.6 and 7.6% of the S. oneidensis genome during early- and late-exponential phases of growth, respectively. The greatest change observed in the treatment was the downregulation of ribosomal proteins (21% of all annotated ribosomal protein genes during early- and 14% during late-exponential) and tRNA genes (14% of all annotated tRNA genes in early-exponential), indicating a marked decrease in protein translation. Other significant changes were the upregulation of membrane transporters, implying an increase in the traffic of substrates across the cell membrane, as well as the up and downregulation of genes related to respiration, which could be interpreted as a response to insufficient oxidants in the cells. In other reports, there is evidence in multiple species that some ROS not just lead to oxidative stress, but act as signaling molecules to control cellular metabolism at the transcriptional level. Consistent with these reports, several genes involved in the metabolism of carbon and biosynthesis of amino acids were also regulated, lending support to the idea of a wide metabolic response. Our results indicate that S. oneidensis is sensitive to the withdrawal of background levels of ionizing radiation and suggest that a transcriptional response is required to maintain homeostasis and retain normal growth.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amino Acids / metabolism
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Dose-Response Relationship, Radiation
  • Electron Transport / genetics
  • Electron Transport / radiation effects
  • Gene Expression Profiling
  • Gene Expression Regulation, Bacterial / radiation effects
  • Gene Ontology
  • Genome, Bacterial / radiation effects
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism
  • Microbial Interactions
  • Oxidative Stress / radiation effects
  • RNA, Bacterial / genetics
  • RNA, Bacterial / metabolism
  • Ribosomal Proteins / genetics
  • Ribosomal Proteins / metabolism
  • Shewanella / genetics*
  • Shewanella / metabolism
  • Shewanella / radiation effects*
  • Transcription, Genetic / radiation effects

Substances

  • Amino Acids
  • Bacterial Proteins
  • Membrane Transport Proteins
  • RNA, Bacterial
  • Ribosomal Proteins

Grant support

This work was supported by Department of Energy Office of Environmental Management, award #DE-EM0002423. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.