Comparative genomics reveals adaptive traits in novel Antarctic lithic cyanobacteria

Terrestrial polar cyanobacteria persist at the cold limits of life, enduring a suite of extreme stressors including sub-zero temperatures, frequent freeze–thaw cycles, oligotrophic soils, variable light regimes with long periods of darkness, and desiccation. To survive, cyanobacteria have evolved diverse physiological strategies. A key adaptation among Antarctic terrestrial cyanobacteria is niche colonization: inhabiting the undersides of translucent quartz rocks (hypoliths) and the interior spaces of porous rocks (endoliths), which buffer environmental extremes and sustains the potential for photoautotrophic carbon fixation. However, the full genomic repertoire facilitating their resilience is incomplete. We cultivated cyanobacteria from endolithic and hypolithic niches in Victoria Valley, Eastern Antarctica, and recovered four near-complete genomes (100% completeness, < 1% contamination). Three hypolithic genomes showed near-identical sequence similarity (whole genome average nucleotide identity = 99.98%) and phylogenomic proximity to the genus Coleofasciculus, yet represent a novel species, Coleofasciculus caryii H7-2. The fourth genome, derived from an endolith, showed moderate similarity to Aliterella antarctica (whole genome average nucleotide identity = 79.1%), and is proposed as a new species, Aliterella bergstromii E5.1. C. caryii H7-2 possessed a larger genome (~ 6.1 Mbp) than A. bergstromii E5.1 (~ 5.4 Mbp). Both genomes encoded complete pathways for carbon fixation via oxygenic photosynthesis (RuBisCO and phosphoribulokinase), extensive phycobilisomes, and multiple photoprotective mechanisms. Predicted optimal growth temperatures were 21.7 °C and 23.2 °C, respectively. Shared stress-mitigation genes included those for osmotic, thermal and oxidative (superoxide dismutase) stress response. All genomes contained biosynthetic gene clusters associated with stress-adaptive secondary metabolites, including heterocyst glycolipids, siderophores, phenazines, compounds related to nostopeptolide and merocyclophane. The C. caryii H7-2 genome encoded multiple CRISPR-Cas systems, suggesting adaptive immunity and historical phage exposure. In contrast, A. bergstromii E5.1 harboured a single prophage and an array of 24 plasmids. These finding reveal that the newly-described cyanobacteria possess a rich genomic repertoire of adaptations to withstand Antarctic extremes, emphasizing the resilience and ecological importance of lithobiontic cyanobacteria in polar deserts.