A Novel Adaptation Mechanism Underpinning Algal Colonization of a Nuclear Fuel Storage Pond

Geochemical analyses alongside molecular techniques were used to characterize the microbial ecology and biogeochemistry of an outdoor spent nuclear fuel storage pond at Sellafield, United Kingdom, that is susceptible to seasonal algal blooms that cause plant downtime. 18S rRNA gene profiling of the filtered biomass samples showed the increasing dominance of a species closely related to the alga Haematococcus pluvialis, alongside 16S rRNA genes affiliated with a diversity of freshwater bacteria, including Proteobacteria and Cyanobacteria High retention of ¹³⁷Cs and ⁹⁰Sr on pond water filters coincided with high levels of microbial biomass in the pond, suggesting that microbial colonization may have an important control on radionuclide fate in the pond. To interpret the unexpected dominance of Haematococcus species during bloom events in this extreme environment, the physiological response of H. pluvialis to environmentally relevant ionizing radiation doses was assessed. Irradiated laboratory cultures produced significant quantities of the antioxidant astaxanthin, consistent with pigmentation observed in pond samples. Fourier transform infrared (FT-IR) spectroscopy suggested that radiation did not have a widespread impact on the metabolic fingerprint of H. pluvialis in laboratory experiments, despite the 80-Gy dose. This study suggests that the production of astaxanthin-rich encysted cells may be related to the preservation of the Haematococcus phenotype, potentially allowing it to survive oxidative stress arising from radiation doses associated with the spent nuclear fuel. The oligotrophic and radiologically extreme conditions in this environment do not prevent extensive colonization by microbial communities, which play a defining role in controlling the biogeochemical fate of major radioactive species present.IMPORTANCE Spent nuclear fuel is stored underwater in large ponds prior to processing and disposal. Such environments are intensively radioactive but can be colonized by microorganisms. Colonization of such inhospitable radioactive ponds is surprising, and the survival mechanisms that microbes use is of fundamental interest. It is also important to study these unusual ecosystems, as microbes growing in the pond waters may accumulate radionuclides present in the waters (for bioremediation applications), while high cell loads can hamper management of the ponds due to poor visibility. In this study, an outdoor pond at the U.K. Sellafield facility was colonized by a seasonal bloom of microorganisms, able to accumulate high levels of ¹³⁷Cs and ⁹⁰Sr and dominated by the alga Haematococcus This organism is not normally associated with deep water bodies, but it can adapt to radioactive environments via the production of the pigment astaxanthin, which protects the cells from radiation damage.