Understanding low radiation background biology through controlled evolution experiments

Abstract

Biological experiments conducted in underground laboratories over the last decade have shown that life can respond to relatively small changes in the radiation background in unconventional ways. Rapid changes in cell growth, indicative of hormetic behaviour and long‐term inheritable changes in antioxidant regulation have been observed in response to changes in the radiation background that should be almost undetectable to cells. Here, we summarize the recent body of underground experiments conducted to date, and outline potential mechanisms (such as cell signalling, DNA repair and antioxidant regulation) that could mediate the response of cells to low radiation backgrounds. We highlight how multigenerational studies drawing on methods well established in studying evolutionary biology are well suited for elucidating these mechanisms, especially given these changes may be mediated by epigenetic pathways. Controlled evolution experiments with model organisms, conducted in underground laboratories, can highlight the short‐ and long‐term differences in how extremely low‐dose radiation environments affect living systems, shining light on the extent to which epimutations caused by the radiation background propagate through the population. Such studies can provide a baseline for understanding the evolutionary responses of microorganisms to ionizing radiation, and provide clues for understanding the higher radiation environments around uranium mines and nuclear disaster zones, as well as those inside nuclear reactors.

Subjective perceptions and psychological distress associated with the deep underground

“…Despite ventilation, the temperature still approached 30°C in the aisle of a goaf at 1470 m below ground; however, oxygen concentration did not obviously change. As in other deep-underground laboratories, [7] γ radiation dose-rate decreased to <one-half of the value at the surface. The vast majority (97.2%) of the CJEM employees that responded to the survey had a negative impression of their ambient underground conditions, identifying moisture (74.9%) as the most troubling adverse factor in the deep-underground space, followed by heat (33.5%), poor ventilation (32.4%), dim light, and the narrow space.…”

Fruit Flies Provide New Insights in Low-Radiation Background Biology at the INFN Underground Gran Sasso National Laboratory (LNGS)

“…Several studies performed on unicellular systems, including bacteria, yeast and mammalian cultured cells, have already shown that cell physiology is indeed influenced at different levels by deprivation of normal radiation background. The determination of whether low-radiation background could affect life and development of multicellular and complex organisms remains a highpriority task in most underground laboratory agendas (4,11,36,63). At the LNGS we have successfully started to address this complex question using Drosophila melanogaster as a model system.…”

“…The evidence that radiation doses/dose rates comparable to the average radiation background influence cell and tissue homeostasis is not so surprising (11). The evolution of living species over approximately 4 billion years in the presence of a variable radiation environment has eventually led to the integration of this daily stimulus into the normal biochemical and physiological cellular processes.…”

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

“…As Lampe et al ( 61 ) have pointed out, based on the physics of the two radiation fields of background and below background radiation, it is challenging to propose that biological organisms could sense these miniscule differences in ionizing radiation. This point was initially and reasonably brought up by Washington University's Jonathan Katz ( 62 ), and, in our response to his critique in which we agreed with his calculations, we posited the idea that biological “sensors” rival our most sensitive radiation detection instruments [Castillo and Smith response to Professor Katz, Castillo et al ( 63 )].…”