Genomic insights into adaptations to survival and toxicity of cyanobacteria in hot springs: a study comprising cyanobacterial genomes from Europe, Iceland, and Central Asia

<h4>Aim of the study</h4>Genomic resources for thermophilic cyanobacteria remain limited, hindering understanding of their ecology and adaptations to extreme high-temperature environments. This study characterizes the genomic features of thermophilic cyanobacteria from thermal springs, focusing on their strategies to cope with energy limitations and the genetic basis of secondary metabolite production.<h4>Material and methods</h4>We analyzed six newly assembled genomes, and compared them with reference genomes from thermophilic and mesophilic cyanobacteria. Functional gene analysis, genome size comparisons, and biosynthetic gene cluster (BGC) mining were performed to assess adaptations.<h4>Results</h4>Genome sizes varied substantially, with <i>Hillbrichtia pamiria</i> showing a notably reduced genome, whereas <i>Calothrix thermalis</i> and <i>Thermoleptolyngbya hindakii</i> were similar to or larger than related mesophiles. Secondary metabolite BGCs were generally reduced in thermophiles, especially in <i>H. pamiria</i>, although larger genomes retained diverse BGCs, including cyanotoxins, nonribosomal peptide synthetases (NRPS), ribosomally synthesized and post-translationally modified peptides (RiPPs) and terpenes. Core functions, the Calvin cycle and nitrogen fixation, were conserved, while lineage-specific variation occurred in Tricarboxylic Acid (TCA) cycle, sulfur assimilation, and denitrification genes. <i>Amphirytos necridicus</i> harbors features suggesting adaptation to low-energy environments, like alternative TCA cycle enzymes.<h4>Conclusions and relevance</h4>These findings expand the genomic and functional landscape of thermophilic cyanobacteria, reveal lineage-specific adaptations, and underscore the value of learning from these natural strategies for potential biotechnological applications.