Abstract
Ionizing radiation is a major environmental variable for cells on Earth, and so organisms have adapted to either prevent or to repair damages caused by it, primarily from the appearance and accumulation of reactive oxygen species (ROS). In this study, we measured the differential gene expression in Deinococcus radiodurans UWO298 cultures deprived of background ionizing radiation (IR) while growing 605 m underground at the Waste Isolation Pilot Plant (WIPP), reducing the dose rate from 72.1 to 0.9 nGy h–1 from control to treatment, respectively. This reduction in IR dose rate delayed the entry into the exponential phase of the IR-shielded cultures, resulting in a lower biomass accumulation for the duration of the experiment. The RNASeq-based transcriptome analysis showed the differential expression of 0.2 and 2.7% of the D. radiodurans genome after 24 and 34 h of growth in liquid culture, respectively. Gene expression regulation after 34 h was characterized by the downregulation of genes involved in folding newly synthesized and denatured/misfolded proteins, in the assimilation of nitrogen for amino acid synthesis and in the control of copper transport and homeostasis to prevent oxidative stress. We also observed the upregulation of genes coding for proteins with transport and cell wall assembly roles. These results show that D. radiodurans is sensitive to the absence of background levels of ionizing radiation and suggest that its transcriptional response is insufficient to maintain optimal growth.
Highlights
We observed the upregulation of genes coding for proteins with transport and cell wall assembly roles. These results show that D. radiodurans is sensitive to the absence of background levels of ionizing radiation and suggest that its transcriptional response is insufficient to maintain optimal growth
Deinococcus radiodurans belongs in a phylum widely distributed in nature, occupying niches from deep ocean subsurface and hot springs to arid desert soils (Daly, 2009), and it is understood that its ability to survive acute exposure to ionizing radiation (∼17 kGy) is likely due to its niche of high temperature and low water availability (Mattimore and Battista, 1996; Rainey et al, 2005)
The present study shows a growth deceleration response in D. radiodurans cultures directly related to an artificial dose of ionizing radiation approximately 80 times lower than background levels (Figure 1A)
Summary
The role of background ionizing radiation (IR) as an environmental cue in cells has been previously documented in various models that include multicellular (Planel et al, 1987; Kawanishi et al, 2012; Van Voorhies et al, 2020) and unicellular (Satta et al, 1995) eukaryotes, mammalian cell cultures (Satta et al, 2002; Fratini et al, 2015), and bacteria (Planel et al, 1987; Smith et al, 2011; Castillo et al, 2018). Deinococcus radiodurans belongs in a phylum widely distributed in nature, occupying niches from deep ocean subsurface and hot springs to arid desert soils (Daly, 2009), and it is understood that its ability to survive acute exposure to ionizing radiation (∼17 kGy) is likely due to its niche of high temperature and low water availability (Mattimore and Battista, 1996; Rainey et al, 2005) This adaptation is the result of cellular and molecular mechanisms that protect its proteins and DNA from extreme degradation and to the modification of its proteins to prevent degradation and to retain catalytic activity for metabolic and DNA repair processes (Liu et al, 2003). Compared with radiation-sensitive Escherichia coli, D. radiodurans’ RecA is more efficient repairing double-stranded DNA breaks (Pobegalov et al, 2015), has at least four layers in its thick cell wall (Brooks and Murray, 1981), and its DNA is organized in a toroidal conformation (Englander et al, 2004). Lim et al (2019) have found a surprising diversity of radiation-resistant genes that are spread across Deinococcus species, whereas regulatory genes that control radiation/desiccation regulons were conserved
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