A genome-resolved cyanobacterial consortium from the Atacama Desert reveals novel bacterial diversity, stress-resilience potential, chromatic flexibility, and photoprotection

Abstract

The Atacama Desert is one of the most extreme terrestrial environments on Earth, characterized by hyper-aridity, intense solar and ultraviolet radiation, oxidative stress, and metal-rich substrates. Here, we characterized an enriched cyanobacteria-associated consortium obtained from a high-altitude, river-influenced site in Quebrada Talabre, Atacama Desert. Deep shotgun metagenomic sequencing, achieving 99.7% estimated community coverage, enabled the reconstruction of 14 high-quality metagenome-assembled genomes representing five bacterial phyla. Genome-resolved analyses revealed multiple putative novel bacterial lineages, including a potential novel family-level lineage within Thermomicrobiales, putative novel species of Allosphingosinicella , Flavobacterium , and Caulobacter , and a distinct Nostocaceae lineage corresponding to the dominant cyanobacterium, tentatively named Talabrenema galetoviciae TAL-12. Functional annotation revealed marked differentiation among consortium members. Heterotrophic bacteria encoded predicted functions associated with aromatic compound degradation, nitrogen and sulfur turnover, iron acquisition, metal-biocide resistance, and oxidative-stress responses, whereas the TAL-12 cyanobacterial metagenome-assembled genome encoded the core machinery for oxygenic photosynthesis, carbon fixation, and pigment biosynthesis. Phylogenomic analyses supported T. galetoviciae TAL-12 as a novel species and likely novel genus within Nostocaceae. Comparative genomic and structural analyses revealed a diversified phycobiliprotein repertoire comprising phycocyanin, allophycocyanin, and phycoerythrocyanin components, together with divergent but structurally conserved paralogs and variable accessory pigment modules across related Nostocaceae genomes, consistent with enhanced light-harvesting flexibility. Pigment fractionation supported the absence of canonical phycoerythrin production and confirmed phycocyanin enrichment. Purified TAL-12 phycocyanin displayed moderate thermal stability, while the cyanobacterial component of TAL-12 consortium cultures retained chlorophyll during prolonged exposure to elevated temperature. In addition, the TAL-12 cyanobacterial genome encoded a Nostocales-like scytonemin biosynthetic gene cluster consistent with UV photoprotection, while lacking canonical cyanotoxin biosynthetic gene clusters. Together, these findings reveal previously underexplored bacterial diversity and predicted functional complementarity within an Atacama cyanobacteria-associated consortium, while identifying T. galetoviciae TAL-12 as a distinctive Nostocaceae lineage with light-harvesting, thermal-resilience, and photoprotective traits relevant to extremophile-based bioinnovation.