LAUSR

Simple Summary Although the two-component system is known to play considerable roles in sensing and responding to environmental signals, there is little information regarding the two-component systems of thermophilic cyanobacteria. Herein, we investigated the structure and architecture of two-component systems in 17 well-described thermophilic cyanobacteria. The results revealed a fascinating complexity and diversity of these systems. Moreover, the distinct composition of genes related to these systems existed among these thermophilic cyanobacteria. In addition, we found diversified domain architectures of histidine kinases and response regulators, putatively in association with various functions. Furthermore, horizontal gene transfer, as well as duplications events, might be involved in the evolutionary history of genes relevant to these systems in certain genera. The obtained data will highlight that the genomes of thermophilic cyanobacteria have a broad potential for acclimations to environmental fluctuations. Abstract Two-component systems (TCSs) play crucial roles in sensing and responding to environmental signals, facilitating the acclimation of cyanobacteria to hostile niches. To date, there is limited information on the TCSs of thermophilic cyanobacteria. Here, genome-based approaches were used to gain insights into the structure and architecture of the TCS in 17 well-described thermophilic cyanobacteria, namely strains from the genus Leptodesmis, Leptolyngbya, Leptothermofonsia, Thermoleptolyngbya, Thermostichus, and Thermosynechococcus. The results revealed a fascinating complexity and diversity of the TCSs. A distinct composition of TCS genes existed among these thermophilic cyanobacteria. A majority of TCS genes were classified as orphan, followed by the paired and complex cluster. A high proportion of histidine kinases (HKs) were predicted to be cytosolic subcellular localizations. Further analyses suggested diversified domain architectures of HK and response regulators (RRs), putatively in association with various functions. Comparative and evolutionary genomic analyses indicated that the horizontal gene transfer, as well as duplications events, might be involved in the evolutionary history of TCS genes in Thermostichus and Thermosynechococcus strains. A comparative analysis between thermophilic and mesophilic cyanobacteria indicated that one HK cluster and one RR cluster were uniquely shared by all the thermophilic cyanobacteria studied, while two HK clusters and one RR cluster were common to all the filamentous thermophilic cyanobacteria. These results suggested that these thermophile-unique clusters may be related to thermal characters and morphology. Collectively, this study shed light on the TCSs of thermophilic cyanobacteria, which may confer the necessary regulatory flexibility; these findings highlight that the genomes of thermophilic cyanobacteria have a broad potential for acclimations to environmental fluctuations.