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Abstract Thermophilic cyanobacteria thrive in extreme environments, making their thermoresistant enzymes valuable for industrial applications. Common habitats include hot springs, which act as evolutionary accelerators for speciation due to geographical isolation. The family Thermosynechococcaceae comprises thermophilic cyanobacteria known for their ability to thrive in high‐temperature environments. These bacteria are notable for their photosynthetic capabilities, significantly contributing to primary production in extreme habitats. Members of Thermosynechococcaceae exhibit unique adaptations that allow them to perform photosynthesis efficiently at elevated temperatures, making them subjects of interest for studies on microbial ecology, evolution, and potential biotechnological applications. In this study, the genome of a thermophilic cyanobacterium, isolated from a hot spring near Okahandja in Namibia, was sequenced using a PacBio Sequel IIe long‐read platform. Cultivations were performed at elevated temperatures of 40, 50, and 55°C, followed by proteome analyses based on the annotated genome. Phylogenetic investigations, informed by the 16S rRNA gene and aligned nucleotide identity (ANI), suggest that the novel cyanobacterium is a member of the family Thermosynechococcaceae. Furthermore, the new species was assigned to a separate branch, potentially representing a novel genus. Whole‐genome alignments supported this finding, revealing few conserved regions and multiple genetic rearrangement events. Additionally, 129 proteins were identified as differentially expressed in a temperature‐dependent manner. The results of this study broaden our understanding of cyanobacterial adaptation to extreme environments, providing a novel high‐quality genome of Thermosynechococcaceae cyanobacterium sp. Okahandja and several promising candidate proteins for expression and characterization studies.

Thermophilic cyanobacteria thrive in extreme environments, making their thermoresistant enzymes valuable for industrial applications. Common habitats include hot springs, which act as evolutionary accelerators for speciation due to geographical isolation. The family Thermosynechococcaceae comprises thermophilic cyanobacteria known for their ability to thrive in high-temperature environments. These bacteria are notable for their photosynthetic capabilities, significantly contributing to primary production in extreme habitats. Members of Thermosynechococcaceae exhibit unique adaptations that allow them to perform photosynthesis efficiently at elevated temperatures, making them subjects of interest for studies on microbial ecology, evolution, and potential biotechnological applications. In this study, the genome of a thermophilic cyanobacterium, isolated from a hot spring near Okahandja in Namibia, was sequenced using a PacBio Sequel IIe long-read platform. Cultivations were performed at elevated temperatures of 40, 50, and 55°C, followed by proteome analyses based on the annotated genome. Phylogenetic investigations, informed by the 16S rRNA gene and aligned nucleotide identity (ANI), suggest that the novel cyanobacterium is a member of the family Thermosynechococcaceae. Furthermore, the new species was assigned to a separate branch, potentially representing a novel genus. Whole-genome alignments supported this finding, revealing few conserved regions and multiple genetic rearrangement events. Additionally, 129 proteins were identified as differentially expressed in a temperature-dependent manner. The results of this study broaden our understanding of cyanobacterial adaptation to extreme environments, providing a novel high-quality genome of Thermosynechococcaceae cyanobacterium sp. Okahandja and several promising candidate proteins for expression and characterization studies., (© 2024 The Author(s). MicrobiologyOpen published by John Wiley & Sons Ltd.)

[Display omitted] • Thermosynechococcus spp. characterized with polyphasic approach. • Eight species within the Thermosynechococcus. • New thermophilic genus proposed – Parathermosynechococcus. • Non-thermophilic genus identified within Thermosynechococcaceae. • Conserved genomic core of Thermosynechococcus pan-genome. Thermophilic unicellular cyanobacteria of the family Thermosynechococcaceae are essential primary producers and integral components of many microbial mats found in hot springs of Asia and North America. Historically, based on their simple morphology, these organisms, along with members of taxonomically unrelated thermophilic Thermostichaceae have been described with a generic term, " Synechococcus ", used for elongated unicellular cyanobacteria. This has created significant misperception in the scientific literature regarding the taxonomic status of these essential thermophilic primary producers and their relationship with Synechococcus sensu stricto. In this manuscript, we attempted a genome-driven taxonomic reevaluation of the family Thermosynechococcaceae. Application of genomic analyses such as GTDB classification, ANI/AAI and phylogenomics support the delineation of eight species within genus Thermosynechococcus. Two subspecies were further identified within T. taiwanensis by dDDH and phylogenomics. Moreover, the results also suggest the presence of two putative new genera phylogenetically alongside genus Thermosynechococcus , a thermophilic genus Parathermosynechococcus represented by PCC 6715 and a non-thermophilic genus represented by PCC 6312. The proposed genospecies and new genera were further integrated with morphological and/or ecological information. Interestingly, the phylogeny of 16S-23S ITS achieved a better taxonomic relationship than that of 16S rRNA and supported the genome-based classification of Thermosynechococcus spp. Finally, the pan-genome analysis indicated a conserved pattern of genomic core among known members of Thermosynechococcus. [ABSTRACT FROM AUTHOR]