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

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 oxidantsmore » 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.« less

Authors:
ORCiD logo [1];  [2];  [3];  [1];  [4]
  1. New Mexico State Univ., Las Cruces, NM (United States). Dept. of Biology
  2. Oregon State Univ., Corvallis, OR (United States). Dept. of Botany and Plant Pathology
  3. National Center for Genome Resources, Santa Fe, NM (United States)
  4. Chuo Univ., Tokyo (Japan)
Publication Date:
Research Org.:
New Mexico State Univ., Las Cruces, NM (United States)
Sponsoring Org.:
USDOE Office of Environmental Management (EM)
OSTI Identifier:
1499892
Grant/Contract Number:  
EM0002423
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 13; Journal Issue: 5; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
63 RADIATION, THERMAL, AND OTHER ENVIRON. POLLUTANT EFFECTS ON LIVING ORGS. AND BIOL. MAT.

Citation Formats

Castillo, Hugo, Li, Xiaoping, Schilkey, Faye, Smith, Geoffrey B., and Taguchi, Y-h. Transcriptome analysis reveals a stress response of Shewanella oneidensis deprived of background levels of ionizing radiation. United States: N. p., 2018. Web. doi:10.1371/journal.pone.0196472.
Castillo, Hugo, Li, Xiaoping, Schilkey, Faye, Smith, Geoffrey B., & Taguchi, Y-h. Transcriptome analysis reveals a stress response of Shewanella oneidensis deprived of background levels of ionizing radiation. United States. doi:10.1371/journal.pone.0196472.
Castillo, Hugo, Li, Xiaoping, Schilkey, Faye, Smith, Geoffrey B., and Taguchi, Y-h. Wed . "Transcriptome analysis reveals a stress response of Shewanella oneidensis deprived of background levels of ionizing radiation". United States. doi:10.1371/journal.pone.0196472. https://www.osti.gov/servlets/purl/1499892.
@article{osti_1499892,
title = {Transcriptome analysis reveals a stress response of Shewanella oneidensis deprived of background levels of ionizing radiation},
author = {Castillo, Hugo and Li, Xiaoping and Schilkey, Faye and Smith, Geoffrey B. and Taguchi, Y-h.},
abstractNote = {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.},
doi = {10.1371/journal.pone.0196472},
journal = {PLoS ONE},
number = 5,
volume = 13,
place = {United States},
year = {2018},
month = {5}
}

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