The Phenotypic and Transcriptomic Response of the Caenorhabditis elegans Nematode to Background and Below-Background Radiation Levels

Abstract

Studies of the biological effects of low-level and below-background radiation are important in understanding the potential effects of radiation exposure in humans. To study this issue we exposed the nematode Caenorhabditis elegans to average background and below-background radiation levels. Two experiments were carried-out in the underground radiation biology laboratory at the Waste Isolation Pilot Plant (WIPP) in New Mexico USA. The first experiment used naïve nematodes with data collected within 1 week of being placed underground. The second experiment used worms that were incubated for 8 months underground at below background radiation levels. Nematode eggs were placed in two incubators, one at low radiation (ca.15.6 nGy/hr) and one supplemented with 2 kg of natural KCl (ca. 67.4 nGy/hr). Phenotypic variables measured were: (1) egg hatching success (2) body size from larval development to adulthood, (3) developmental time from egg to egg laying adult, and (4) egg laying rate of young adult worms. Transcriptome analysis was performed on the first experiment on 72 h old adult worms. Within 72 h of being underground, there was a trend of increased egg-laying rate in the below-background radiation treatment. This trend became statistically significant in the group of worms exposed to below-background radiation for 8 months. Worms raised for 8 months in these shielded conditions also had significantly faster growth rates during larval development. Transcriptome analyses of 72-h old naïve nematode RNA showed significant differential expression of genes coding for sperm-related proteins and collagen production. In the below-background radiation group, the genes for major sperm protein (msp, 42% of total genes) and sperm-related proteins (7.5%) represented 49.5% of the total genes significantly up-regulated, while the majority of down-regulated genes were collagen (col, 37%) or cuticle-related (28%) genes. RT-qPCR analysis of target genes confirmed transcriptomic data. These results demonstrate that exposure to below-background radiation rapidly induces phenotypic and transcriptomic changes in C. elegans within 72 h of being brought underground.

Deinococcus radiodurans UWO298 Dependence on Background Radiation for Optimal Growth

“…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 ). Regardless of their taxonomic and physiological differences, most of these models showed, to varying degrees, deleterious effects attributable to their growth under IR dose rates below natural background levels.…”

Underground Radiobiology: A Perspective at Gran Sasso National Laboratory

“…In our experience, Drosophila melanogaster has proven to be particularly responsive to changes in environmental radiation promptly modifying its physiological responses. However, in addition to flies, other organisms are currently being investigated, namely fishes at the SNOLAB ( 23 ) and nematodes at WIPP ( 24 ). The comparison between the responses of the organisms placed at different levels of the phylogenetic tree will provide interesting insights to understand the role of natural radiations in the adaptation and evolution of living organisms.…”

First transcriptome profiling of D. melanogaster after development in a deep underground low radiation background laboratory

“…For this reason, low-background laboratories are located deep underground, equipped with ventilation systems, additional chambers shielding from surrounding rocks and constructed from materials with a low-radionuclide content. All this makes it possible to reduce the total radiation background by 4–10 times [ 22 , 23 ]. However, there are some limits to radiation background reduction in biological experiments.…”

“…The exposition time is defined by purposes of research and by development/life cycle duration for multicellular organisms or generation time for microorganisms. The current results were obtained in such experiments when model organisms were exposed to low-background conditions from several days to about one year [ 11 , 14 , 20 , 22 ]. Effects of low-radiation background on living organisms were determined by comparing experimental and control groups and by registering the changes in parameters suitable for experimental purposes, for instance, growth rate, lifespan, fertility, gene expression or protein abundance [ 12 – 15 , 20 ].…”

“…During several weeks of exposition to low-background conditions, this model organism demonstrated the increased median lifespan for both sexes and fertility reduced by 30% [ 20 ]. After eight months of exposure of nematode Caenorhabditis elegans to low-radiation background the increased egg-laying and relatively faster growth rates during larval development were registered, and after 72 hours in an underground laboratory alterations in expression of genes involved in spermatogenesis (up-regulated), collagen and cuticle metabolism (down-regulated) were observed [ 22 ]. During the ongoing REPAIR project the lake whitefish Coregonus clupeaformis was used in SNOLAB where a significant increase in embryo body length and body weight was registered, but the authors could not explain the reason for these changes [ 27 ].…”