The ecology and evolutionary history of the Deinococcaceae family
Deinococcus radiodurans is the most studied member of the Deinococcaceae family for its outstanding capability to withstand extreme doses of gamma radiation and prolonged desiccation. D. radiodurans is also type species and the first described member of the Deinococcus genus. It demonstrates approximately 3000 times more radiation resistance capability than humans and 50 times more than Escherichia coli. The remarkable radiation resistance phenotype in D. radiodurans and certain members of this family has established the conventional belief that radiation resistance is the defining characteristic of Deinococcaceae. Consequently, microbiologists used gamma radiation as a pre-culture treatment to enrich radioresistant isolates in environmental samples before cultivation. However, a few studies did not use gamma radiation as an enrichment method and isolated sensitive Deinococcus species. These findings demonstrated that the radiation resistance capacity is highly diverse among Deinococcus species, with variations in the order of magnitude ranging from 1.5 kGy to 15 kGy. Because of this variability, the prevailing view is that genomic data cannot predict radiation resistance and that this phenotype remains without a genotype. Moreover, Deinococcus members have been isolated from diverse environments, including Antarctica, hot springs, deserts, atmospheric dust, animals, and garden soil. Nevertheless, the origins of this ubiquity have remained unexplored. Here, I discuss how the biased isolation methods and focus on highly resistant species created a gap in our understanding of the true ecology and evolution of Deinococcaceae. This thesis addresses this knowledge gap using comparative genomics methods by answering three questions. (I) What factors drive the ubiquity of the Deinococcus species? (ii) What drives the diversity of radiation resistance in the Deinococcus genus, and can we predict this phenotype using genomic data? (iii) How did the radiation resistance phenotype evolve, and what are the primary needs for the common ancestor of Deinococcaceae (proto-Deinococcus)? Our results indicate that the ubiquity of the Deinococcus genus arises from its large pangenome. A high abundance of transposase genes and efficient homologous recombination mechanisms enhanced their genetic flexibility and enabled Deinococcus to survive in diverse habitats. Conversely, this ecologically advantageous trait forms a dynamic accessory genome and impacts the radiation resistance phenotype. Phylogenomic and statistical analyses revealed a pattern in the radiation resistance level. The presence of 186 gene families, mainly related to metal and redox-related cofactors, can predict lower levels of resistance in two different clades of the Deinococcus genus. This observation contradicts the conventional wisdom that radiation resistance is the defining characteristic of the Deinococcaceae family because the accessory genome controls this phenotype. Furthermore, we used the gene tree-species tree reconciliation method to infer the evolutionary events that gave rise to the proto-Deinococcus. The ancestral reconstruction analysis indicated that the proto-Deinococcus underwent significant genome expansion by gaining 1000 gene families, which is about 50% of the genome size of its ancestor, while Thermaceae retained the same genome size as their common ancestor. Overall, we conclude that the ubiquity of Deinococcus species is the result of acquiring diverse functions and surviving in various environments. While this is a beneficial evolution for the family, gaining specific genes can lower the radiation resistance capability. Therefore, radiation resistance is not the defining characteristic of Deinococcaceae. Moreover, ancestral reconstruction reveals that this proto-Deinococcus underwent genome expansion and likely gained genes that induced radiation resistance traits and genomic flexibility.
Radiation resistance, Deinococcus, Ecology, Evolution, Deinococcaceae, Radiation sensitivity, Pangenome
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